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Trophic ecology of piranhas (Characidae : serrasalminae) from savanna and forest regions in the Orinoco River basin of Venezuela

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Title:
Trophic ecology of piranhas (Characidae : serrasalminae) from savanna and forest regions in the Orinoco River basin of Venezuela
Creator:
Nico, Leo G., 1954-
Publication Date:
Language:
English
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xiii, 209 leaves : ill., photos ; 29 cm.

Subjects

Subjects / Keywords:
Animal fins ( jstor )
Ecology ( jstor )
Fish ( jstor )
Fish scales ( jstor )
Forests ( jstor )
Llanos ( jstor )
Rivers ( jstor )
Savannas ( jstor )
Species ( jstor )
Stomach ( jstor )
Dissertations, Academic -- Zoology -- UF
Fishes -- Orinoco River Region (Venezuela and Colombia) ( lcsh )
Piranhas ( lcsh )
Zoology thesis Ph. D
Genre:
bibliography ( marcgt )
theses ( marcgt )
non-fiction ( marcgt )

Notes

Thesis:
Thesis (Ph. D.)--University of Florida, 1991.
Bibliography:
Includes bibliographical references (leaves 198-208).
Additional Physical Form:
Also available online.
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Leo G. Nico.

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University of Florida
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0027082657 ( ALEPH )
25622507 ( OCLC )

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TROPHIC ECOLOGY OF PIRANHAS (CHARACIDAE: SERRASALMINAE)
FROM SAVANNA AND FOREST REGIONS
IN THE ORINOCO RIVER BASIN OF VENEZUELA










By

LEO G. NICO














A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY



UNIVERSITY OF FLORIDA 1991















ACKNOWLEDGEMENTS



I owe a debt of gratitude to many friends and colleagues for their help during the field work, data analysis, and manuscript preparation. During my development as a tropical biologist, I greatly benefited from the guidance of several people. Dr. Jamie Thomerson launched me into the study of neotropical fishes. Dr. Donald Taphorn provided me with the opportunity to do long-term research in the Orinoco River basin. In 1980, he took me to the Llanos where we netted my first piranha while seining the muddy waters of Calo Maraca. The botanist Dr. Basil Stergios invited me to accompany his 1985 expedition to the upper Rio Negro and the Brazo Casiquiare where I fell in love with the rivers and humid forests of southern Venezuela. My graduate committee chairman, Dr. Horst Schwassmann, opened my eyes to the Amazon River; together we crossed part of its estuary, from Bel6m to the Uha de Maraj6, a journey I shall always remember.

My investigations have prospered from discussions with various members of my committee as well as from the exchange of ideas with colleagues and friends, in particular Drs. Donald Taphorn, Steve Walsh, and Kirk Winemiller. Dr. Horst Schwassmann, and other members of my committee -- Drs. Carter Gilbert, Martha Crump, Frank Nordlie, and Nigel Smith -- were always helpful. I thank them for their advice and for reviewing the tedious draft manuscripts. I am also grateful to Drs. Stephen Walsh, Jamie Thomerson, Thomas Keevin, and Carmine Lanciani, and to Frank Jordon for their comments on various sections and drafts of the manuscript.

I thank the following persons for their assistance with collecting fishes in the Venezuelan Llanos: Anielo Barbarino, Linda Delashmidt, Terry Dye, Guillermo Feo, Carter Gilbert, Oscar Leon, Craig Olds, Stewart Reid, Eric Sutton, Donald Taphorn, and



ii









Kirk Winemiller. I am particularly grateful to Donald C. Taphom for providing both a home and work area in Guanare, and for sharing his knowledge of the Venezuelan fish fauna. He has always been unselfish in the sharing of fish specimens and field data from his work in the Orinoco Llanos.

Most of my work in the upper Orinoco resulted from participation in expeditions as part of a natural resource inventory of southern Venezuela, organized and sponsored by Corporaci6n Venezolana Guayana Tecnica Minera (CVG-TECMIN). I thank all those associated with CVG-TECMIN whose assistance made my work possible, for administrative and logistic support these include Dr. Fernando Susach, Victor Fernandez, and Pedro Mata. For occasional help in the field, I express my sincere appreciation to several members of the TECMIN technical staff, Angel Fernandez, Luz:Delgado, Andres Garcia, Guillermo Fuenmayor, Sandra Giner, and Jesus Santiago. I relied heavily on the fishing skills of my field assistants and camp workers hired by CVG-TECMIN: Fabian Morillo, Yovani Aragua, Juan Carlos Castillo, Ambrosio Guayamore, Antonio Gaveln, and Hilario Bolivar. Assistance in the upper Orinoco was also given by Dr. Basil Stergios, Carlos Rivas, Carlos Templa, and Mike Dawson; many of the Yanomamo Indians including Chirino, Pablo and Ram6n, Cesar Timanawd, Ram6n Pokorai; the Curipaco Indians Carlos Antonio Guaruya, Eliasa Guaruya, and Eruerto L6pez; and many individuals whose names I did not record. Together with my field assistants, their intimate knowledge of the fishes, the rivers, and the forests of the upper Orinoco was invaluable to me.

I thank Drs. William Fink and Antonio Machado-Allison for identification of

voucher specimens of many of the serrasalmine fishes, and for providing me with their unpublished key to Venezuelan piranhas. I am also obliged to Dr. Donald Taphorn for identification of fish specimens, and to Dr. Basil Stergios, Gerardo Aymard, and Nidia de Cuellar for identifying plant material. I thank Darryl Harrison for preparing base maps, Angelina Licata for the fish drawings used in many of my figures, Kevin Schuck for help


iii









with computer drawing of dendrograms, and Craig Lilyestrom for help with a few of the graphs and introducing me to the MacIntosh computer.

Parts of my research were funded by National Geographic Society grants no. 381188 and 4183-89. The Department of Zoology, University of Florida, provided additional funds and equipment. I thank all those in the Department of Zoology and Florida Museum of Natural History who gave of their time. I thank George Burgess for use of his library. The Universidad Nacional de los Llanos Occidentales and Museo de Zoologfa (UNELLEZMCNG) gave me lab space and administrative assistance in Venezuela. I am indebted to many of the UNELLEZ administrators and staff for their help during the last ten years. In addition, I thank the Venezuelan people, campesinos, Llaneros, and indigenas, for allowing me do research in their beautiful country.

While conducting this study I came to know many very special people. During my stay in Venezuela, I enjoyed the warm hospitality and friendship of Luis and Sioux Strebin, Jose and Sharon Sutera, and Basil and Anita Stergios; along with Terry Dye, Donald Taphorn, Lucas van Balen and his wife, and Dr. H. Kasem. they brought me through my bout withfalciparum malaria. I express appreciation to Dr. Horst Schwassmann and his wife Satiko for frequently inviting me into their home during my passages through Gainesville. I also thank Dr. Carter Gilbert and all my fellow graduate students, especially Dennis Haney and Dr. Steve Walsh, for their many hospitalities. Finally, I thank my parents and family for their constant love and support, both at home and during the many long separations, and I thank Linda for always being there.













iv
















TABLE OF CONTENTS



ACKNOWLEDGEMENTS ........................................................................ ii

LIST O F TA BLES .................................................................................. vii

LIST OF FIGURES ................................................................................. ix

A B ST R A CT .... .................................................................................... x ii

CHAPTERS

I INTRODUCTION ...................................................................... 1

Introduction to Piranhas ................................................................ 1
Purpose of Present Study .............................................................. 3
Literature R eview ......................................................................... 7
Organization of Dissertation ......................... ................................. 16

2 ENVIRONMENTAL SETTING ..................................................... 18

The Orinoco River Basin .............................................................. 18
History of the Basin .................................................................... 22
The Low Llanos ........................................................................ 24
The Upper Orinoco ...................................................................... 28
Savannas and Forests During the Quaternary ....................................... 30
Present Climate and Seasonality ..................................................... 32

3 M E T H O D S .............................................................................. 35

Field Sam pling .......................................................................... 35
Field Site Locations and Sampling Periods ......................................... 37
Evaluation of Habitats ................................................................. 42
Identification and Nomenclature of Piranhas ........................................ 43
Faunal Comparisons ................................................................... 47
A nalysis of D iets ....................................................................... 49
Nutrient Content Analysis of Food Items ........................................... 53
Intestine L ength ......................................................................... 54
Field and Aquarium Observations ..................................................... 55
Statistical A nalyses ...................................................................... 55

4 COMPOSITION OF PIRA A ASSEMBLAGES ............................... 57



v










CHAPTERS
5 TROPHIC ECOLOGY OF SAVANNA PIRANHAS: THE APURE
DRAINAGE ...........................................................71

Study Area .............................................................. 71
Species Accounts.........................................................75
Comparison of Diets.....................................................91

6 TROPHIC ECOLOGY OF PIRANHAS FROM THE UPPER
ORINOCO............................................................ 97

Species Accounts ....................................................... 100
Summary of Upper Orinoco Trophic Patterns............................. 123
Comparison with Savanna Populatons................................... 131
Ecomorphological Correlates: Intestine Length and Diet ..................143

7 NUTRIENT VALUES OF PIRANHA PREY............................148

Animal Matter .........................................................148
Plant Matter............................................................. 153

8 DISCUSSION AND CONCLUSIONS.................................. 155

Composition of Piranha Assemblages ................................... 155
Trophic Patterns ............................ .......................... 163
Ecomorphological. Correlates ............................................ 175
A Phylogenetic Perspective ............................................... 177


APPENDICES

A MATERIAL EXAMINED ................................................ 181

B DATA ANALYSIS....................................................... 191

LITERATURE CITED ............................................................ 198

BIOGRAPHICAL SKETCH ...................................................... 209















vi














LIST OF TABLES


Table
1-1 Summary of principal field studies investigating piranha feeding and diets in
order of publication date .............................................................. 9
3-1 List of abbreviations used in figures and tables for piranhas and other
serrasalm ine fishes ...................................................................... 46
4-1 Occurrence of piranha species in samples from nine drainages in the
Orinoco River basin, Venezuela ................................................. 59

4-2 Distance between drainages and Coefficient of Biogeographic Resemblance
among nine sampled drainages in the Orinoco River basin ..................... 62

4-3 Number of shared piranha species and Coefficient of Biogeographic
Resemblance among nine sampled drainages in the Orinoco River basin ........ 64 4-4 Summary of piranha species occurrence by habitat and water type, based on
samples in Orinoco River basin, Venezuela ..................................... 70
5-1 Food items of Pygocentrus caribe from the Apure River drainage (Calo
Caicara area) by size class ........................................................... 79

5-2 List of vertebrate prey taxa identified from the stomach contents of the four
most common piranhas from the Cafio Caicara area, Apure River drainage,
in the low Llanos of Venezuela ........................................................ 80
5-3 Food items of Serrasalmus irritans from the Apure River drainage (Caflo
Caicara area) by size class ........................................................81

5-4 Food items of Serrasalmus medinai from the Apure River drainage (Calo
Caicara area) by size class ........................................................ 83
5-5 Food items of Serrasalmus rhombeus from the Apure River drainage (Caflo
Caicara area) by size class ........................................................ 84
5-6 Food items of Serrasalmus elongatus from the Apure River drainage (Cafro
Caicara area) by size class ........................................................ 86
5-7 Food items of Serrasalmus altuvei from the Apure River drainage (Caio
Caicara area) by size class .................................... 88




vii








Table2

5-8 Food items of Pristobrycon striolatus from the Apure River drainage (Caiio
Caicara area) by size class ........................................................ 89

5-9 Food items of Catoprion mento from the Apure River drainage (Calo
Caicara area) by size class ........................................................ 90

5-10 Food items of small juvenile piranhas (Size Class I, 10-19 mm SL),
tentatively identified as Pygocentrus caribe, from the Apure River drainage
(Caflo Caicara area) .................................................................. 92

5-11 Matrix of diet overlaps among different size classes of piranhas from Apure
River drainage, low Llanos ........................................................ 95

6-1 List of taxa identified from the stomach contents of the three most common
piranha species from upper Orinoco River drainages, Venezuela ............... 103

6-2 Food items of Serrasalmus rhombeus from the upper Orinoco River basin
by size class ............................................................................ 104

6-3 Food items of Serrasalmus manueli from the upper Orinoco River basin by
size class ............................................................................... 107

6-4 Food items of Serrasalmus cf. eigenmanni from the upper Orinoco River
basin by size class ................................................................... 111

6-5 Food items of Serrasalmus altuvei from the upper Orinoco River basin by
size class .............................................................................. 113

6-6 Food items of Pristobrycon striolatus from the upper Orinoco River basin
by size class .......................................................................... 115

6-7 Food items of Pygopristis denticulatus from the upper Orinoco River basin
by size class .......................................................................... 118

6-8 Matrix of diet overlaps among different size classes of serrasalrnine fishes
from upper Orinoco River drainages .............................................. 124

6-9 Incidence of herbivory in piranhas ( 80 mm SL) as associated with the low
Llanos and upper Orinoco ......................................................... 136

6-10 One-tailed Mann-Whitney U-test results testing the prediction that piranha
species (> 80 mm SL) from upper Orinoco River drainages fed more on
plant material than those from the low Llanos ..................................... 140
7-1 Estimates of the lipid, protein, ash, carbohydrate, and caloric contents of
fins, scales, and whole fish for two taxa of typical prey fish .................... 149

8-1 Orinoco River basin piranhas categorized by adult diet ........................... 158





viii















LIST OF FIGURES


Figure PAZe

1-1 Hypothesized phylogenetic relationships among genera of the subfamily
Serrasalminae as proposed by Machado-Allison (redrawn from MachadoA llison 1985) ............................................................................. 2

2-1 Map of northern South America showing Orinoco River basin ................... 19

2-2 Major savanna and forest ecosystems in the Orinoco River basin ................. 25

2-3 Approximate distribution of open savanna (low Llanos) in Venezuelan state
of Apure, Orinoco River basin ....................................................... 26

2-4 Approximate distribution of lowland forests in Federal Amazon Territory of
V enezuela ................................................................................ 29

2-5 Monthly rainfall recorded at representative sites in Ofinoco River basin,
Venezuela. (1) Upper Orinoco: monthly average 1971-1977 from Santa
Maria de Los Guaicas, mouth of Ocamo River, Federal Territory of
Amazonas, and (2) Low Llanos: for year 1972 from Cafto Caicara area,
Apure River drainage, Apure State .................................................... 34

3-1 Map of Venezuela showing nine selected drainages in Orinoco River basin
sampled during present study ........................................................ 38

3-2 Map of Apure State, Venezuela, showing principal low Llanos sampling
locations .................................................................................. 39

3-3 Map of 1988-1991 sampling sites in upper Orinoco, Federal Territory of
A m azonas, Venezuela .................................................................. 41

4-1 Schematic representation showing relative distances among the nine
sampled drainages and their approximate location along Orinoco River main
channel ................................................................................... 58

4-2 Scatter diagram showing relationship between number of piranha species
per drainage and log of the drainage area size (km2) for nine sampled
drainages in Orinoco River basin, Venezuela ........................................ 63

4-3 Scatter diagram showing similarity in piranha species composition between
adjacent sampled drainages versus distance between adjacent drainages ......... 65




ix









Fiz=r Plg=
4-4 Scatter diagram showing similarities in piranha species composition
between all possible paired drainages and the distance between paired
drainages .............................................................................. 66
4-5 Dendrogram from cluster analysis depicting similarities among nine sampled
drainages of Orinoco River basin based on piranha species composition ........ 67

5-1 Location of Carlo Caicara study area, Apure River drainage, in low Llanos
of Apure State, Venezuela .......................................................... 72

5-2 General body form and major fin markings of seven piranha species (55-70
mm SL) and Catoprion mento from Calo Caicara study area, Apure River
drainage, in the low Llanos of Venezuela ............................................ 73
5-3 Diets by size class of seven piranha species and Catoprion mento from Calo
Caicara study area, Apure River drainage, in the low Llanos of Venezuela ...... 76
5-4 Diet breadths estimated for seven piranha species and Catoprion mento, by
size class, from the Caflo Caicara area of the low Llanos, Apure River
drainage, Orinoco River basin, Venezuela ....................................... 94

5-5 Dendrograrn from cluster analysis depicting similarities among diets of
piranha species (by size class) from the Calo Caicara area of the low
Llanos, Apure River drainage, Orinoco River basin, Venezuela .................. 96

6-1 Eight piranha species from the upper Orinoco River basin of Venezuela ......... 98

6-2 Diets by size class (>40 mm SL) of eight piranha species from the upper
Orinoco River basin, Venezuela ..................................................... 101

6-3 Diets of selected small juvenile piranhas (10-19 mm SL) from upper
Orinoco River drainages and the low Llanos, Venezuela ......................... 108

6-4 Diets by size class ( 80 mm SL) of four common serrasalmine species from
the upper Orinoco River basin: Catoprion mento, Myleus asterias, M.
schomburgkii, and M. torquatus .................................................... 120

6-5 Dendrogram from cluster analysis depicting similarities among diets of
piranha and related species (by size class) from the upper Orinoco River
basin, V enezuela ...................................................................... 127
6-6 Diet breadths estimated for eight piranha species, by size class, from the
upper Orinoco River basin, Venezuela ............................................. 130

6-7 Diets by size class (_ 40 mm SL) of three piranha species from the Cinaruco
and Capanaparo river drainages of the low Llanos, Orinoco River basin,
V enezuela .............................................................................. 133






x








Fiure

6-8 Comparison of the proportion of plant material in the diets of carnivorous
and herbivorous piranha species ( 80 mm SL) from the low Llanos to those from upper Orinoco River drainages in terms of percent adjusted
volume (%Va), percent dominance (%D), and percent frequency of
occurrence (% O ) ..................................................................... 138

6-9 Diets by size class ( t40 mm SL) of Serrasalmus manueli comparing low
Llanos (Cinaruco drainage) and upper Orinoco populations ..................... 141

6-10 Scatter diagram showing relationship between mean intestine length/standard length and percent volume of plant material in diet for
selected serrasalmine fish ( >80 mm SL) ........................................... 145

6-11 Scatter diagram showing relationship between intestine length and standard length for the three most common piranha species in samples from the upper
Orinoco River basin of Venezuela ................................................... 146

6-12 Scatter diagram showing relationship between intestine length and standard length for Serrasalmus manueli comparing upper Orinoco and Llanos
p opulations ............................................................................. 146

7-1 Bar graph comparing dry mass composition of small whole fish, scales and
fin s ...................................................................................... 150

8-1 Proposed hypothetical model showing the dietary responses of carnivorous
versus herbivorous piranha species to changes in various habitat parameters
and food resources ........................................ 171

8-2 Diets and intestine length mapped onto the proposed phylogeny of
Machado-Alhison (1985) for genera of the subfamily Serrasalminae ........... 179






















xi















Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy

TROPHIC ECOLOGY OF PIRANHAS (CHARACIDAE: SERRASALMINAE) FROM SAVANNA AND FOREST REGIONS IN THE ORINOCO RIVER BASIN OF VENEZUELA by

Leo G. Nico

December, 1991



Chairman: Dr. Horst 0. Schwassmann
Major Department: Zoology

This study emphasizes interspecific and intraspecific comparisons of the trophic

ecology of piranhas (Characidae: Serrasalminae) from two vegetatively distinct regions in the Orinoco River basin of Venezuela: (1) the upper Orinoco in the Federal Amazon Territory, an area dominated by dense tropical forests, and (2) the low Llanos of Apure State, a region characterized by immense open savannas. Eleven piranha species were taken from the two regions studied. Since 1979, ten species have been collected from the low Llanos of Apure State, whereas my 1989-1991 samples indicate that at least eight species occur in the upper Orinoco. Seven species were widely distributed and inhabited both regions. The high similarity in species composition between the two regions suggests that there are really no distinct savanna versus forest piranha assemblages.

All piranhas exhibit changes in diet with age. The smallest juveniles, < 20 mm standard length (SL), prey mainly on microcrustaceans and small aquatic insects. Older juveniles of most species, between 20 and 80 mm SL, commonly eat fins. Fin eating by xii










young piranhas is common in both the low Llanos and the upper Orinoco. Chemical analysis indicated that fins are similar to scales in energy and protein content, but less than that of small whole fish. Orinoco piranhas 80 mm SL fall into two general dietary categories: species that are primarily carnivorous and others that are largely herbivorous. The seven carnivorous piranhas (Pygocentrus caribe, Serrasalmus altuvei, S. manueli, S. rhombeus, S. elongatus, S. irritans, and S. medinai) feed heavily on fish or fish fins. Adults of the four herbivorous species (Serrasalmus cf. eigenmanni, Pygopristis denticulatus, and two Pristobrycon spp.) are seed predators, biting seeds and hard fruits into small fragments before ingesting them. Serrasalmus manueli was one of the few carnivorous species that occasionally took seeds or fruit in mass. Overall, relative intestine length differed among serrasalmine species and was closely correlated with diet. Seedeating piranhas tended to have long intestines, similar to those of highly herbivorous Myleus, Mylossoma, and Metynnis species, but I found no significant difference in relative intestine lengths between forest and savanna populations of S. manueli even though diets differed.

Both carnivorous and herbivorous species are somewhat flexible in their use of

food resources. I found that upper Orinoco piranhas, at both the group and species levels, exploit plant material more than piranhas from the low Llanos. Many piranhas, especially those that are largely herbivorous, shift their diets in response to spatial as well as temporal variation in the availability of fish prey versus plant food. Even though savanna and forest regions have a similar piranha species makeup, herbivorous species are much more common in forested regions. Nevertheless, even though seeds and fruits are a locally abundant resource, assemblages of forest piranhas were typically dominated by one or two large, highly carnivorous species (S. rhombeus, S. manueli, or both).







xiil














CHAPTER 1
INTRODUCTION


Introduction to Piranhas


Piranhas (Characidae: Serrasalminae) are neotropical freshwater fishes found in the major Atlantic drainages of South America, from 100 North latitude in the Orinoco River basin of Venezuela and Colombia, through the Amazon basin, and south in the La PlataParaguay-Parana basin to about 350 South latitude. Called caribes in Venezuela, they comprise a monophyletic group of at least 30 species in the genera Serrasalmus, Pygocentrus, Pristobrycon and Pygopristis (Fig. 1-1) (Machado-Allison 1983, 1985, Fink 1988). Piranhas possess many unique morphological traits that distinguish them from other serrasalmines (Machado-Allison 1985), but they are most easily recognized by their unusual and impressive dentition. They have a single row of sharp, somewhat triangular teeth in both jaws; the teeth are tightly packed, partially interlocking, and are typically used for rapid puncture and shearing.

Examples of other serrasalmine fishes are species of Mylossoma, Myleus, and

Metynnis (silver dollars, pdmpanos, palometas), the scale-eating characin Catoprion mento, and the nearly one-meter long Piaractus brachypomus (morocoto) and Colossoma macropomwnum (cachama or tambaquO. In contrast to the piranhas, the dental morphologies of other serrasalmine fishes are variable. Most species have combinations of relatively broad and strong molariform and incisive teeth, often with more than one row of teeth in the upper jaw. Serrasalmine fishes are laterally compressed and most are fairly deepbodied; however, maximum adult size, body shape, and color patterns vary among species. Piranhas range from medium-sized fishes such as Serrasalmus irritans, some 20 cm from

1







2





Colossoma Piaractus Mytossoma Myleus

Mylesinus A Utiarichthys

Acnodon


Metynnis B Catoprion

P ygop rist is Pygocentrus PRNA

Pristobrycon Serrasalmus.




Fig. 1-1. Hypothesized phylogenetic relationships among genera of the subfamily
Serrasalmninae as proposed by Machado-Allison (redrawn from MachadoAllison 1985).







3

tip of snout to base of tail (Standard Length, SL) to large species such as Serrasalmus rhombeus, which grow to well over 35 cm SL. The general body form ranges from sharpsnouted and elongate, Serrasalmus elongatus, to blunt-headed and robust species such as the red-bellied piranhas Pygocentrus caribe of the Orinoco and P. nattereri of the Amazon.

Of the approximately thirty species of piranhas, at least twelve occur in the Orinoco basin where, as in many other areas of tropical South America, they are exploited for subsistence fisheries and also commercially. Piranhas occur in rivers and floodplains of both open savannas and densely forested regions and often make up a high percentage of fish biomass and numbers of individuals (Mago-Leccia 1970, Taphom and Lilyestrom 1984). Thus, they play a major role in the food web of many lowland aquatic communities. Contrary to common belief that they are strictly carnivorous, piranhas and their close relatives exploit a broad spectrum of food resources including arthropods, fishes and other vertebrates, fish fins and scales, carrion, seeds, fruits, leaves, and flowers (Goulding 1980, Sazima 1983, Sazima and Guimardes 19S7, Nico and Taphorn 1988, Winemiller 1989a, Sazima and Machado 1990). Serrasalmine fishes living in tropical savannas encounter substantially different habitat conditions in comparison to those populations occupying forested regions. Thus, comparative studies of piranha diets and trophic ecology can provide insights into their responses and adaptations to the selective forces of different environments

Purpose of Present Study


Tropical South America possesses the most diverse freshwater fish fauna of any continent (Bt5hlke et al. 1978). Considering both described and undescribed taxa, Lundberg et al. (1987) estimated that the Orinoco River basin alone probably contains almost 1,000 fish species, more species than are found in all the freshwater systems of temperate North America. Unfortunately, the extremely diverse faunas and floras of many







4

tropical environments are seriously threatened. Because of expanding human populations and increased development, natural habitats are being destroyed or degraded at a rapid pace. Forests are being cleared for agriculture, ranching, timber, and minerals; rivers and their floodplains are being modified by dams, levees, and pollution. Aquatic and terrestrial systems in the lowland tropics are intricately interwoven, the changes to each inevitably affecting the other. The profound and likely irreversible changes now occurring throughout tropical America make it increasingly important to understand more about the interrelationships between tropical environments and their diverse fauna and flora. Such an understanding is necessary for successful conservation of habitats, species, and genetic stocks.

The science of ecology attempts to understand the complex interrelationships

between an organism and its physical and biotic environment. Studies in trophic: ecology are a way to investigate such interrelationships, and often perrnit analysis at several levels or scales, Obviously, what an animal eats is limited by the kinds and availability of food resources in its local surroundings. Valid interpretations of feeding patterns, however, also require consideration of past envirom-nental conditions, inasmuch as the probability of an animal taking a particular type of prey depends on its array of interrelated morphological and behavioral characters that result from its particular phylogenetic history. Trophic studies provide insights into the biology of organisms, because food, unlike many other resources or niche parameters, can be measured, analyzed, and compared in a large number of ways using a variety of techniques. Evidence for the importance and practicality of research on trophic ecology is provided by the tremendous volume of literature on the subject (for review of fishes see Ross 1986). Accordingly, the study of diets and food resources has contributed to the development of many ecological concepts, including resource partitioning, niche theory, optimality theory, energetics, food webs, and predatorprey relationships.







5

The aim of this study is to increase our knowledge of the ecology and natural

history of piranhas and a few of their close relatives. I have attempted to document and explain similarities and differences in trophic ecology within and among closely related species by comparing populations from two floristically distinct regions of the Orinoco River Basin of Venezuela: (1) the upper Orinoco, an area dominated by dense forests, and

(2) the low Lianos of Apure State, a region characterized by immense open savannas.

Piranhas are widely distributed geographically and very abundant in many lowland tropical habitats, but we know relatively little about their ecology, behavior, and natural history. Goulding (1980) found many fishes in the Amiazonian forest ecosystems, including several piranhas, to be herbivorous or omnivorous and to depend heavily on flooded forests for food resources. Influenced by Goulding's findings., Donald Taphorn and I began, in late 1983, to study the trophic ecology and natural history of piranhas and other fishes in savanna ecosystems of the Venezuelan Llanos (Nico and Taphorn 1988, Nico 1990). Although my initial research on piranhas focused on savanna regions in the Orinoco Basin, I also made visits to southern Venezuela and the Rio Casiquiare in 1985, and to MaraJ6 Island in the lower Amazon of Brazil in 1986. Subsequently, between May 1988 and March 1991, I participated in five expeditions to the upper Orinoco basin and its forests to broaden my investigation of the feeding ecology of Orinoco piranhas as related to their habitat.

Waters of the low Llanos are typically high in fish and invertebrate biomass, and many sites support large numbers of carnivores (Mago-Leccia 1970, Taphorn and Lilyestrom 1984, Machado-Allison 1987, Saunders and Lewis 1988, Rodriguez and Lewis 1990). However, large woody plants are uncommon, and in conjunction with water stress caused by the yearly dry periods, production of seeds and fruits is highly seasonal (Sarmiento 1984). As a result, availability of plant materials, especially fruits and large seeds, as food for savanna fishes is low, markedly seasonal, and very localized (personal observations). On the other hand, the few phenological studies of wet forests in lowland







6

areas of tropical South America (Terborgh 1983, Goulding et at. 1988, Janson and Ernmons 1990), or information gleaned from botanical exploration of the upper Orinoco (B. Stergios, personal communication), suggest that such habitats make a wide variety and abundance of fruits and seeds available to fishes during most of the year (Goulding 1980, Gouilding et al. 1988). Even though species diversity is often high in the upper Orinoco, our collections made with a variety of fishing gear indicate that fish biomass in tropical forest regions is generally lower than in the low Lianos.

If present ecological conditions are important, environment should strongly influence both species composition and trophic ecology of piranha assemblages in particular regions. Accordingly, comparisons of piranhas from the more heavily forested upper Orinoco basin with those from the open savannas or low Llanos were made to address the following questions: (1) Do the same species of piranhas occur in both savanna and forested regions? (2) Do diets differ, and, if so, are fish from populations in forested habitats significantly more herbivorous than their saivanna counterparts? (3) Do ontogenetic shifts in diet occur and, if so, how do they compare among species and do they correlate with regional environments? (4) Because gut length is often an indicator of natural diet in vertebrates (i.e., longer in herbivores), is intestinal length of piranhas and other serrasalmine fishes correlated with diet? (5) What are the nutritional benefits associated with different diets or food preferences (e.g., scale- or fin-eating versus flesheating)? (6) How do diets of piranhas compare with other serrasalmine species? (7) What is the relationship between piranha ecology and serrasalmidne phylogeny?

The comparative approach is useful in helping us understand aspects of the

evolution and adaptations of closely related species (Clutton-Brock and Harvey 1984, Huey and Bennett 1986). Recent comparative studies in tropical vertebrate ecology have focused on birds (Schluter 1988), mammals (Terborgh 1983), and reptiles and amphibians (Duellman 1990). An objective in many comparative studies is discovery of evolutionary trends in morphological and behavioral adaptations to different environments, thereby







7

making it possible to recognize how particular characters arise under the influence of contrasting selective forces (Clutton-Brock and Harvey 1984). Furthermore, comparisons across a broad biogeographical scale offer what Wiens et al. (1986) suggested as perhaps the best opportunity to understand a species' limits or responses to different environmental conditions, revealing patterns that suggest something of its adaptive abilities or evolutionary potential.


Literature Review



The following is a brief review of the literature relating to piranha feeding behavior and trophic ecology. A summary of field studies investigating piranha feeding and diets is given in Table 1 -1. Unless otherwise stated, scientific names are as used in the original literature. All references to Serrasalmus nattereri should be Pygocentrus nattereri.

Early naturalists and explorers were the first to report on piranhas, and most accounts, such as those by Alexander von Humboldt, Henry Bates, and Theodore Roosevelt, were primarily devoted to describing attacks by piranhas on animals and humans, or relating the destruction done by piranhas to fishing gear (Bates [1863] 1975:202, Roosevelt 1914). Hum-boldt, who traveled extensively in South America between 1799 and 1804, wrote the following passage while on the Orinoco River:


On the morning of the 3rd of April our Indians caught with a hook the fish
known in the country by the name of caribe* [*Caribe in the Spanish
language signifies cannibal, or caribito, because no other fish has such a
thirst for blood. It attacks bathers and swimmers, from whom it often bites
away considerable pieces of flesh. The Indians dread extremely these
caribes; and several of them showed us the scars of deep wounds in the calf
of the leg and in the thigh, made by these little animals. They swim at the
bottom of rivers; but if a few drops of blood be shed on the water, they rise
by thousands to the surface, so that if a person be only slightly bitten, it is difficult for him to get out of the water without receiving a severer wound.
Humboldt ([1816-1831] 1971:166-167)







8

Eigenmann (1915), Eigenmann and Allen (1942), and Myers (1972) have reviewed many of the earlier stories about piranhas. Although published anecdotal information brought notoriety to this group of South American fishes, early accounts did not significantly contribute to our knowledge of piranha biology and natural history, and many stories simply aided to perpetuate myths about piranha ferocity.

There have been a moderate number of studies that have addressed the natural diets of piranhas, (Table 1-1). Most of these have focused on only one or a few of the most common and widespread species, from a single locality or region. The diets of several of the more uncommon species have never been described. Most studies of piranha diets have been of fishes inhabiting artificially altered environments. Because a few of the more common piranha species seem to flourish in man-made lakes, several studies focused on populations inhabiting reservoirs or impoundments. Work on piranhas has also been done in watersheds modified to some extent by cattle ranching, agriculture, and by construction of roadways. Few investigations have been carried out in Pristine habitats.

Several of the earliest efforts to characterize piranha diets were carried out in the

Jaguaribe River basin, a coastal drainage located in northeastern Brazil. The first was that of Menezes and Menezes (1946). Along with information on several other species, they presented a simple listing of food items, primarily fish remains and insects, found in the stomachs of 138 specimens of a single piranha species taken in 1944 from the Lima Campos Reservoir in Ceard State. First identified by Menezes and Menezes as Serrasalmo immaculatus, Braga (1954) later indicated the species was Serrasalmus rhombeus. Braga also studied Lima Campos piranhas. He recorded the frequency of occurrence and volume of stomach contents of a large sample of S. rhombeus (n = 2,222; 100-290 mmn total length) during a 12-month study, 1952-1953 (Braga 1954). Of the 1,713 individuals containing food, predominant food items were freshwater shrimp (Palaemonidae) and fish, 65 and 28 percent of the total food volume, respectively. Braga later published results from other studies on piranhas in a single volume (Braga 1975), providing diet information



















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on S. nattereri from three other reservoirs of the Jaguaribe basin. In that work, Braga concluded that piranhas were carnivorous, preferring to feed on other fishes, although they also prey on other vertebrates (i.e., birds and amphibians), some invertebrates, and only occasionally on plant material, such as seeds, parts of leaves, and algae.

Bonetto et al. (1967) reported on the feeding habits of two piranhas, Serrasalmus spilopleura (n = 104) and S. nattereri (n = 21), taken from the middle Parand River and its floodplain in Argentina. Both species fed predominantly on fish, but prey were not identified to lower taxa. Stomachs of many of the individuals examined contained small amounts of plant material, for example, roots and leaves of the aquatic plant Salvinia sp. and roots of Eichhornia sp. (water hyacinth); however, these items were thought to have been taken accidentally during capture of their principle prey.

Lowe-McConnell (1964) studied the ecology of fishes in the Rupununi savanna of the Essequibo River basin, British Guiana (present day Guyana). Although not focusing on fish diets, she briefly mentioned that the stomachs of fishes trapped in drying pools, including the piranhas Serrasalmus nattereri, S. rhombeus, and Pygopristis denticulatus, contained only mud and bottom debris; however, these same fishes had large amounts of body fat. From her work in the Essequibo River drainage, Lowe-McConnell concluded that the dry season was a period when fishes exhibited reduced feeding and high diet overlap.
Roberts (1970) was the first to report on the more unusual feeding practices of piranhas when he found large amounts of fins and some scales in the stomachs of seven Serrasalmus elongatus from several sites in the Amazon River basin. He also discussed scale-eating by the serrasalmine Catoprion mento. Saul (1975) collected two piranha species during his study of habitat and food preferences of fishes at a site along the Aguarico River, a tributary of the Napo River in the western Amazon Basin, Ecuador. He found the stomachs of Serrasalmus nattereri (n = 6) to contain fish remains and insects;







13

those of S. marginatu (n = 4) held fish and fish remains. Both species were found primarily in floodplain lakes or side channels, as opposed to the main river.

The relationship between piranha feeding patterns and environment had not been

investigated in any detail, however, until Goulding (1980) studied the diets of medium and large-sized adult fishes, including seven piranha species, from in and around the Machado River, a clearwater tributary of the turbid-water Madeira River in Amazonia Brazil, a region of seasonally inundated forests. He found that large Serrasalmus rhombeus (n = 254), the most common piranha taken, were primarily pisciv ores that often bit chunks of flesh out of large fish. Of added interest, fruits and seeds made up an estimated 10 percent of the total volume of food eaten by S. rhombeus. Adult S. elongatus (n = 85) collected by Goulding were similar to the juveniles examined by Roberts in that they had fed heavily on fins and scales. Goulding reported that five of the seven species fed heavily on seeds, which they masticated before swallowing. These five piranhas, which were relatively uncommon in samples, included Serrasalmus serrulatus (n = 36), Serrasal.'Mus cf. striolatus (n = 9), and three unidentified Serrasalmus species (n = 5?). Goulding concluded that Amazonian fishes had evolved a close interrelationship with lowland forests, and that many fishes depended on flooded forests for food in the form of fruit, seeds, and other allochthonous materials. In addition to being seed predators, Goulding (1983) later indicated that piranhas sometimes took seeds whole, and suggested that these fish also acted in dispersal of seeds.

After Goulding completed his work in the Madeira River basin, he was joined by Carvaiho and Ferreira (Goulding et al. 1988) in a study on the natural history of Amazonian fishes in habitats associated with the main channel of the lower Rio Negro. Of approximately 450 species taken in the Rio Negro, six were piranhas. They did not discuss piranha diets in much detail, but reported that fin and scale eating by adult piranhas seemed to be common. Their collections of juvenile piranhas from the Rio Negro are yet to







14

be analyzed. In the published proceedings of a symposium Ledo et al. (1989) reported on the morphology, reproduction, and diet of Serrasalmus altuvei from the Rio Negro.

Sazima and his colleagues have explored the behavior of piranhas and related species, particularly in reference to fin and scale-eating, through laboratory work with captive fishes and underwater observations of free-living fishes in the Pantanal region, western Brazil (Sazima 1983, 1986, 1988; Sazima and Zamprogno 1985, Sazima and Pombal 1988, Sazima and Machado 1990). Sazima and Guimardes (1987) recognized Pygocentrus nattereri and Serrasalmus spilopleura as scavengers, feeding on dead and sometimes decaying fishes, birds, and mammals. They suggested that deaths of humans attributed to piranhas might often be the result of scavenging on victims already dead from drowning or other causes. Sazima and Machado (1990) presented data from their underwater observations on the behavior of three species, S. marginatus, S. spilopleura, and P. nattereri, with emphasis on their predatory tactics, feeding behavior, and social interactions while foraging.

Ferreira (1984b) studied the food and feeding habits of the principal fish species inhabiting the Curudi-Una River Reservoir, in the Amazon Basin near Santar6m, Brazil. Ferreira found that the diet of Serrasalmus rhombeus, taken from five localities in the reservoir, showed slight differences among stations, feeding mainly on fish at four sites, and on aquatic insects (i.e., ephemeroptera) at a fifth locality. In total, 250 specimens were examined (ranging from 50 to 320 mm SL) of which 196 piranhas contained food.

Northcote et al. (1986, 1987) reported fin feeding by Serrasalmus spilopleura from the Americana Reservoir, an impoundment on the Atibaia River in southeastern Brazil. Analysis of prey fishes with damaged fins showed that S. spilopleura usually nip the lower lobe of fins, indicating that attacks are made from below and behind prey fishes. They also suggested that S. splilopleura was the main, if not the only, fin-feeder in the reservoir fish community. Mota et al. (1982) studied the seasonal variation in the intensity of feeding, as measured by stomach fullness, of S. spilopleura from the Bariri Reservoir in Sdo Paulo







15

State, Brazil. They reported that heaviest feeding took place during the summer months with a corresponding heavy build up of body fat by autumn.

Several recent works dealing with piranhas in the Venezuelan Llanos have

documented diet shifts during ontogeny (Machado-Allison and Garcia 1986, Nico and Taphorn 1988, and Winemiller 1989a). All found that early juveniles ate principally zooplankton, while older individuals were predominantly piscivores. In addition to discussing ontogenetic changes in dental morphologies, Machado-Allison and Garcia (1986) examined 134 specimens, mostly juveniles, of three species (Pygocentrus caribe Pristobrycon striolatus, and Serrasalmus rhombeus) taken from the Camaguin lagoon, a large wetland between the Portuguesa and Apure rivers, Guarico State. Predominant food items, in terms of frequency of occurrence, of young piranhas were microcrustaceans, aquatic insects, fins, and scales. In addition, they found small seeds (i.e., Cyperaceae) in the stomachs of 33 of 134 specimens, but did not provide information on volume and numbers of seeds eaten. Nico and Taphorn (1988) examined the diets of seven piranha species from streams and flooded savannas in the western Llanos of the Orinoco River Basin. Their work suggested that savanna piranhas do not depend on fruits and seeds as had been reported by Goulding (1980) for piranhas in flooded tropical rain forests. Nico and Taphom found that juveniles and sub-adults of six of seven piranhas from a single locality fed heavily on fins. Winemiller (1989a) studied the fish community of Cario Maraca, a seasonal stream in the Apure River drainage that meanders through a region of wooded savannas used for cattle ranching and cropland in Portuguesa State. His findings on four piranha species (P. caribe, S. irritans, S. rhombeus, and S. medinai), mostly juveniles and sub-adults, supported the earlier work of Nico and Taphorn.

For the most part, piranhas have been found to be daytime feeders, usually most active during twilight periods (Lowe-McConnell 1964, Goulding 1980, Barthem 1987, Nico 1990, personal observations). Barthem (1987) reported on activity patterns of several vdrzea lake fishes from near Manaus, Brazil. His results, based onanalysis of gilinet







16

catches, suggest an early morning peak of activity in Pygocentrus nattereri, Serrasalmus elongatus, and S. rhombeus, and a late afternoon peak for the latter two species. Nico (1990) found that young Pygocentrus notatus ( = P. caribe) had a peak feeding activity in the morning, whereas adults seemed to be more active near dusk.

Intestine length of a few piranha species has been measured by Braga (1954),

Luengo (1965), Bonetto et al. (1967), and Jdgu and dos Santos (1988). Braga reported that the digestive tract of Serrasalmus rhombeus averaged 1.4 times the standard length. Luengo (1965), relating intestine length to natural diet, reported that the highly carnivorous Serrasalmus nattereri ( = Pygocentrus caribe) taken in the Venezuelan Llanos had a short intestine compared with that of Prochilodus reticulatus ( = Prochilodus mariae?), a prochilodid fish that feeds primarily on organic mud and detritus. Martfnez (1976:67) studied the anatomy of what was identified as Serrasalmus nattereri ( = Pygocentrus caribe) and reported 10 to 12 intestinal caeca originating near and slightly past the pylorus. In a taxonomic treatment, J6gu and dos Santos (1988) provided information on intestine length and number of pyloric caeca for several piranha species from the Rio Tocantins of Brazil, but they did not suggest dietary correlations.


Organization of Dissertation


The content and sequence of the chapters reflect the major components of my study. Chapter 2 provides an overview of the Orinoco River basin and describes the environment of the two study regions. Chapter 3 identifies the study sites and details field and laboratory methods used. Chapter 4 compares the species composition of piranha assemblages between the two regions and among the different drainages. Chapter 5 presents results from long-term studies on the trophic ecology and natural history of savanna populations of piranhas from a site in the Apure River drainage. Chapter 6 focuses on the trophic ecology of populations of serrasalmine fishes from six drainages in







17

the upper Orinoco River Basin, a region characterized by extensive forests that undergo seasonal flooding. In addition, my findings from the upper Orinoco are compared to results from my studies of savanna populations, including data on a few savanna species not reported in previous studies. Chapter 7 then gives results of an analysis of the nutritive values of various food items commonly taken by piranhas. Finally, Chapter 8 summarizes the major findings of the study, and attempts to interpret and synthesize the results in terms of relevant mechanistic, ecological, and evolutionary issues.















CHAPTER 2
THE ENVIRONMENTAL SETTING


In this chapter I give an overview of the Orinoco River basin and describe the two regions dealt with in the present study: (1) the open savannas or low Llanos of Apure State, and (2) the upper Orinoco in the Venezuelan Federal Territory of Amazonas, an area dominated by forests. Little is known about the geological and ecological history of tropical lowlands in South America (Whitmore and Prance 1987). Because historical events undoubtedly influenced present-day ecological patterns, I briefly review several hypotheses concerning the basin's and the river's formation, as well as climatic and vegetation changes that purportedly took place in northern South America during the recent past.


The Orinoco River Basin


The Orinoco River, although dwarfed by the Amazon, is a major tropical river. The basin is located in northern South America between 2' and 10' N latitude, and empties into the Atlantic Ocean (Fig. 2-1). The Orinoco's mean annual discharge is about 35,800 m3/sec from a drainage area of approximately 1, 100,000 km2, located in Venezuela (70%) and Colombia (30%) (Lewis 1988). Compared to the Mississippi River. the Orinoco has more than twice the annual discharge, yet drains an area of only one-third the size. The basin is geologically and ecologically diverse, having large mountain ranges and broad low-lying plains, with habitats ranging from inu-nense open grasslands to lush tropical forests.



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The headwaters of the Orinoco are traditionally considered to be in southern

Venezuela where it receives water from both the western slopes of the Guyana Shield and from extensive lowland areas dominated by deciduous or evergreen tropical forest. In contrast, most tributaries in the northern and western parts of the basin originate in the Andes and adjoining coastal mountains and then flow through the Lianos, a vast alluvial plain supporting tropical savanna vegetation. The main channel of the Orinoco forms an unusual U-shaped pattern, the river winding around the western borders of the Guyana Shield. From its source the Orinoco flows several hundred kilometers west-northwest until it is met by the Atabapo and Guaviare rivers; here the river makes an abrupt turn to the north. Along its northward segment the Orinoco forms the border between Colombia and Venezuela.

At about 5'30'N latitude the river courses through several series of treacherous cataracts near Puerto Ayacucho, the most prominent being the Atures Rapids where the river drops 17.5 m over a distance of 9.3 km (CODESUR 1979). The Attires Rapids and the other cataracts are spread along a reach of nearly 100 km, marking the boundary between the upper and lower sections of the Orinoco. Farther downstream the Orinoco is joined from the west by the Meta, Cinaruco, Capanaparo, and Apure rivers as it gradually swings to the east. Finally, below the confluences with the Caura and Caroni rivers the Orinoco arrives at its large delta. Here the huge main river is subdivided into a multitude of smaller channels that empty into the Atlantic Ocean near the island of Trinidad. The main causeway of the Orinoco, from its origin in the Sierra Parima in the Guyana Shield to its mouth, is estimted to be 2,140 km long (DISCOLAR 1983). High-order tributaries draining highland areas of the Andes and the Guyana Shield are characterized by large numbers of waterfalls, rapids, and fast-flowing waters. However, the larger streams and rivers common to lowland areas typically have slight gradients. The upper Orinoco, at the







21

community of La Esmeralda, nearly 1,800 km by river from the sea, is only 135 m above sea level, an average drop of less than 1 m for every 10 km of river.

In summary, large rivers of lowland forests that feed the upper Orinoco from the south include the Mavaca and Atabapo rivers. Big-river tributaries originating in the Guyana Shield and feeding into the upper Orinoco include the Ocamo, Padamo, Cunucunuma, Ventuari, and Sipapo; those flowing into the lower Orinoco include the Caura and Caroni rivers. Large tributaries of the Orinoco that originate on or near the Andean slopes are the Inirida, Guaviare, Vichada, Tomo, Meta, Cinaruco, Capanaparo, Arauca, and Apure rivers. About 31 percent of the upper Orinoco volume is continually diverted into the Amazon basin by way of the Brazo Casiquiare, a natural canal (CODESUR 1979).

In addition to a diverse flora and topography, the Orinoco River basin is a mosaic of water types. Alfred Russel Wallace ([1853] 1972) was one of the first to mention the striking differences in water colors among the various South American waters using the terms whitewater, blackwater, and clearwater rivers. In a later and more detailed analysis, Sioli (1975, 1984) summarized differences among these three water types based on differences in water color, amount of suspended matter, and chemical properties. Whitewater streams are turbid because of inorganic sediments, of milk-coffee color (cafe con leche), relatively rich in nutrients, and of near neutral pH. Black-water streams are transparent but reddish brown, the color of tea due to humic acids (the color appears black where water runs deep), very poor in nutrients and very acidic. Clearwater streams are also transparent, often greenish in color, typically poor in nutrients, and have a pH that can range from slightly acidic to slightly alkaline.

In the Orinoco River basin, whitewater and blackwater habitats predominate. Clear waters are more typical of small carlos and the upland reaches of certain rivers. However, the classification of rivers by water color is not always easy to apply and thus the usefulness Sioli's classification scheme is somewhat limited. Many rivers are a mixture of







22


two or more of the basic water types; some change seasonally as flows from a diverse array of smaller tributaries rise and fall. For example, during high water the Guayapo River of the Sipapo drainage changes from a clearwater river in its upper and middle reaches to a blackwater river in its lower segments, due to increased input of tannin-stained waters from adjacent flooded forests. To a large extent, the hydrochemistry of the Orinoco tributaries is controlled by the geomnorphological and floristic character of their watersheds. In general, rivers of the Andes and Lianos are high in suspended sediments, whereas streams originating in the weathered Guayana highlands and the forests of the upper Orinoco transport low sediment loads. Nevertheless, exceptions to the above-mentioned hydrochemical pattern can be found in all regions as a result of local conditions.



History of the Basin


The details and precise timing of geological events 1 evolvedd in the formation of the Orinoco River basin are not well understood. The oldest land form in the basin is the Guyana Shield, ancient mountains composed of Precambrian material that underwent additional uplift and exposure during the Tertiary (Whitmore and Prance 1987). Because they have been exposed for many millions of years, these highlands have been heavily worn and dramatically shaped by erosion. The mountains of the Andes were created later, uplifted as a result of plate tectonic events during the Miocene-Pliocene, 2-8 million years ago (Whitmore and Prance 1987:7). The Llanos are thought to be the most recent major topographical feature in the basin. During Quaternary periods of raised sea-level (interglacials) the Llanos plains were the bed of a large interior sea. Thus, similar to many lowland areas in South America, these central plains are primarily composed of Quaternary sediments that niantle Tertiary and older sediments, with recent additions of alluvial river deposits carried down from the surrounding mountains during the Pleistocene (Beek and Bramdo 1968:86, Walter 1973: 72-73, Cole 1986).







23

An ancient Orinoco River is thought to have flowed to the northwest, emptying into the Caribbean before the Miocene uplift of the Andes near or through the present day Maracaibo Lake Basin. In addition to geologic evidence, this idea of a northward flow has received added support from comparisons of fossil and living fishes found in northern Colombia and Venezuela (Lundberg et al. 1986, 1988). According to the proposed scenario, the river slowly shifted to the east some time between the Late Cretaceous and early Oligocene, finally assuming its present course by the Oligocene epoch, about 30 million years ago (Lundberg et al. 1988). However, it is still uncertain how the river's movements affected or coincided with the fon-nation and eventual draining of the sea that covered the interior lowlands at about the same time periods (Taphom 1990).

The Orinoco and Amazon rivers are connected today by the Casiquiare canal, a natural waterway flowing southward from the upper Orinoco into the upper Rio Negro, permitting interchange of fishes between the two basins. However, the Orinoco and Amazon basins may have had an even closer association in the past, partly based on studies in western Brazil. The Amazon once flowed westward to the Pacific before the major rise of the Andes in the Miocene (Goulding 1980, Putzer 1984). After the Andes uplift blocked its westward flow, a huge lake, or more likely, a series of large lakes and wetlands, were formed covering much of the lowland areas in the basin (Frailey et al. 1988). Eastward flow was prevented at the time by higher elevations joining the Brazilian and Guyana shields. Before the Amazon had completely carved its way east between the two shields, the proposed Pleistocene/Holocene lake or lakes had theil prime outlet north into the Orinoco. Indeed, tectonic events may have resulted in shifting the primary outlet several times between the north and east (Frailey et al. 1988).







24

The Low Llanos


The Lianos (Fig. 2-2) are a vast plain of up to 400 kmn width along the north bank of the Orinoco, stretching from near the delta mouth westward for over 1,000 km through Venezuela, far into Colombia (Walter 1973). It occupies about 500,000 km2. is essentially unbroken by major forests, and is the largest continuous savanna in the neotropics north of the equator (Sarmiento 1984). A combination of factors, for instance soil type and rainfall patterns, prevent the establishment of forest in large parts of the Llanos. Dry season fires, of mostly human origin, are also important in limiting the growth of woody vegetation.

Several systems have been used to divide the Llanos into different categories using combinations of physical and biological features. In most cases, a distinction is made between the low Llanos and high or upper Lianos, based on elevation and extent of flooding during the rainy season (Walter 1973: 73, Cole 1986). The low Llanos are characterized by open grass savannas with fairly level terrain that undergo frequent or long term flooding during the rainy season. According to Cole (1986:92), savanna grasslands cover some 150,000 km2 of the low Llanos in the Orinoco basin. Apure State, in western Venezuela, encompasses a large portion of the low Llanos. Here the terrain is relatively flat, with elevations of 100 mn or less above sea level. In Apure, the landscape is dominated by herbaceous cover, mainly bunch grasses and sedges, with occasional shrubs and small trees (Sarrniento 1984, Cole 1986). Most trees, including palms, exist in small isolated groups (matas) or in gallery forest situations fringing the rivers and larger streams (Sarmiento 1984, Cole 1986). These gallery forests range from narrow bands, only a few trees wide, to fairly extensive stands, in some places many hundreds of meters wide, as seen existing along reaches of the lower Cinaruco and Capanaparo rivers.

The low Llanos of Apure State (Fig. 2-3) comprise a vast open floodplain

containing a diversity of aquatic habitats (Mago-Leccia 1970). All undergo pronounced seasonal changes. Because of its low elevation and flat physical relief, most of the








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'-4

o-'- /


0











26












CAI







1, 4











4-4
+





14 4,-q
















0





































O.L 0i






27

landscape floods during the rainy season, whereas surface water during the dry season is usually limited to a few large permanent lagoons, large streams, and rivers. As the dry season progresses, the savanna vegetation turns yellow and the earth becomes hard and is fissured with cracks from the intense heat of the sun. Rivers and streams in the low Llanos are of low gradient, with many wide meanders and anastomoses. The Apure River and many of its tributaries are whitewater in character, with a relatively high sediment load and high conductance (Saunders and Lewis 1988). In contrast, the Capanaparo and Cinaruco are essentially blackwater rivers, with moderate sediment loads. In addition to stream channels, the landscape of the low Llanos is dotted with shallow marshes (esteros) that hold water after floods or rain. Lagoons (lagunas) form in deeper depressions, some created from abandoned stream meanders, and are more permanent aquatic habitats. Human population density is low and most of the low Llanos is used for cattle ranching. Since the early 1970's extensive networks of low earthen dikes, called modules (mdulos), have been constructed, surrounding large areas of the floodplain savanna. These modules lessen the extreme effects of seasonal changes within their boundaries by controlling flooding and by holding water in lower areas, available to cattle year round. The hundreds of borrow pits (prestamos) excavated during the construction of these dikes, as well as from building of roads, collect water and serve as permanent and semi-permanent artificial lagoons. Typically less than 25 m wide, some prestamos stretch unbroken for several kilometers.
During high water, adjacent rivers and streams in the Llanos are often connected by sheet flooding of the savanna or by filling of small interconnecting channels. Thus, fish are generally able to move across the entire floodplain. However, where dikes or roadways are present, run-off patterns have changed and local fish movements are somewhat restricted (Taphorn and Lilyestrom 1984, Nico and Taphorn 1988).

Many of the wetlands in the Llanos contain large amounts of organic material and become highly productive during the rainy season (Mago-Leccia 1970, Saunders and






28

Lewis 1988). During high water, the flooded savanna habitats are important to fish as breeding and feeding areas. Aquatic vegetation flourishes and emergent and floating plants may cover large portions of the surface of both permanent and temporary water bodies. Large mats of water hyacinth (Eichhornia species) are especially abundant in many of the lagoons, prestamos, and some of the streams. Partially inundated grasses and sedges commonly grow in the shallows of streams, prestamos, and other standing waters. Other common aquatic and semi-aquatic plants of the low Llanos include Ludwigia, Benjarnania, and Pontederia. Some common aquatic plants with floating leaves are Salvinia, Lemna, and Pistia.

The Upper Orinoco


The upper Orinoco drainage is situated in the Federal Territory of Amazonas

(Fig. 2-4) in southern Venezuela, a vast area covering 178,095 km2 (CODESUR 1979). Main features of the heavily forested landscape are flat alluvial plains, large mountain valleys, and massive granitic hills (lajas) (CODESUR 1979, Huber and Wurdack 1984). About 70 percent of the territory is drained by the Orinoco, with the remainder flowing into the Rio Negro of the Amazon basin (CODESUR 1979). Together with the adjacent state of Bolivar, this southern section of the country is often referred to collectively as Venezuelan Guyana because the Precambrian Shield dominates the topography. Little developed and with few inhabitants, the great majority of intact forests in Venezuela occur in this southern region. Steyermark (1982) estimated that forests covered 82 percent of the region, or about 146,000 km2. Due to forest clearing, the total coverage is probably slightly less today. Because forests of the upper Orinoco are continuous with those of the northern Amazon Basin, the region is part of the largest area of humid forests within the neotropics (Whitmore and Prance 1987).








29














50








40

























0 0




670 660 650 640





Fig. 2-4. Approximate distribution of lowland forests (shaded area) in Federal Amazon
Territory of Venezuela.







30



The flat lowlands or peneplains of southern Venezuela are domidnated by wet tropical forests (Figs. 2-2 and 2-4). The altitude of these lowland regions in the upper Orinoco range from 100 to 500 m, with most less than 200 m (Huber and Wurdack 1984). Similar to the situation described for Amazonian lowlands (Prance 1979, Kubitski 1989), many lowland forests in the upper Orinoco are inundated by the annual high water, with some sites being permanently waterlogged. Aerial photos of the lowlands reveal a history of streams meandering across their adjacent floodplains. Large and small streams, cutoffs, and oxbows abound in many of the drainages (e.g., Mavaca River) and, similar to the low Llanos, interconnections with adjacent drainages within the upper Orinoco are common during high water. However, aquatic vegetation in the region is much more sparse and localized in comparison to the low Llanos. Although a few backwaters are choked with submergent and emergent vegetation, most floodplain lakes in the upper Orinoco have few or no aquatic plants. The reasons for such scarcity are likelIy related to high shade, unconsolidated bottoms, and few available nutrients in the water or substrate. In flowing waters there are often small bands of flooded grasses along bank edges of inner bends. The fish fauna of the upper Orinoco is the least known in all of Venezuela, largely because of the inaccessibility of the region. With very few roads, modes of transportation within the area are limited almost exclusively to small and medium-sized boats and small planes.


Savannas and Forests during the Quaternary


Both tropical forest and tropical non-forest vegetation originated in the Cretaceous and Tertiary, about 100 million years ago, periods when world climates were apparently rather stable and tropical conditions much more widespread (Whitmore and Prance 1987). However, during the last two million years there have been periodic and dramatic fluctuations in the distribution of savannas versus forest environments in northern South







31

America that are associated with climatic oscillations (Prance 1982, Whitmore and Prance 1987). Although lowland regions remained essentially tropical, during major glaciations the equatorial lowland regions experienced dryer and hotter climates (but see Colinvaux 1976). As a result, savanna and open-land environments expanded, whereas humid forests contracted. During these dry periods, forests were often reduced to combinations of variably-sized isolated refuges and fingers of gallery forests along major rivers. Indeed, new data on Pleistocene mammals indicate that savanna habitat may have expanded to such an extent as to form a continuous band connecting the Orinoco Llanos with the pampas of Argentina by way of the western Amazon basin (Rancy 1991). The last major glacial event causing a cold, dry Pleistocene climatic phase occurred 13,000-18,000 years ago.

Much controversy exists about the extent and precise location of forests during the Pleistocene dry periods. Haffer (1987:12) presented a map outlining possible distribution of both relatively humid areas and tropical forests, forest "refugia", surviving in northern South America during that period of savanna expansion. His map delineates three major regions of hurnid forests in the Orinoco basin: several sections in the Andes; a block near the southern tip of Venezuela; and a long broad belt (100-200 krn wide) south of the main stem Orinoco, extending from near the mouth of the Meta River eastward through the Guianas.

In contrast to glacial periods, interglacial or pluvial periods were wetter and relatively cooler, contributing to the expansion of humid forests and contraction of savannas. Isolated savannas curTently found in the upper Orinoco are thought to be savanna refugia that survived the cooler and wetter phases. The present climatic condition is wet and warm (i.e., as opposed to dry and hot), and humid forests are at or near their maximum extent, whereas the extent of natural savannas and dry forests is restricted (Whitmore and Prance 1987:63).







32

Present Climate and Seasonality


Regional topography and the fact that the entire Orinoco Basin lies immediately

north of the equator are important factors controlling climate and the timing of precipitation (Walter et al. 1975). There is a trend toward increased rainfall from north to south. Nevertheless, rainfall patterns can be quite variable from year to year in a single locality, as well as among different localities within any particular region.

The Lianos have consistently high temperatures and fairly distinct wet and dry

periods. The rainy season is associated with the inner-tropical convergence zone (Walter et al. 1975), and lasts from seven to nine months, usually from late April to October or November (Fig. 2-5). Little or no rain falls during the two or three driest months, when the inner-tropical convergence zone is in the southern hemisphere. Total rainfall in the Llanos ranges from 1200 to 1800 mnm per year (Taphorn 1990), with savanna grasslands common to the low Llanos typically receiving 1300-1400 mm (Cole 1986:97). The recording station at San Fernando de Apure, located in the center of the low Lianos, reported a mean annual precipitation of 1416 mm, based on 2 6 years of records (Walter et al. 1975); mean monthly temperatures for the locality varied between 26.6 and 29.2 TC (Cole 1986:97). However, daily temperatures can fluctuate widely.

Although the two regions have a fairly similar range of air temperatures, the upper Orinoco is much more humid than the Llanos. Average annual rainfall is 3,250 mm/yr, with very humid areas receiving well over 4,000 mm (CODESUR 1979). Although the amount of rainfall varies seasonally, the dry season in the upper Orinoco is not as pronounced as in the Llanos (Fig. 2-5). Few areas of record receive less than 75 mm in any given month during the dry season (CODESUR 1979). Nevertheless, the alternation of low and high water seasons is distinct. Highest precipitation occurs between May and September and the lowest between December and March (CODESUR 1979). Monthly mean temperatures range from 26 to 28.5 TC (CODESUR 1979). Both the low Llanos of







33

Apure State and the lowland forests of the upper Orinoco undergo extensive flooding during the wetter part of the year by a combination of rising river water and local rains.







34











400
-'-- Upper Orinoco
Low Llanos 300

E

S 200



100



0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month



Fig. 2-5. Monthly rainfall recorded at representative sites in Orinoco River basin, Venezuela. (1) Upper Orinoco: monthly average 1971-1977 from Santa Maria
de Los Guaicas, mouth of Ocamo River, Federal Territory of Amazonas, and (2)
Low Llanos: for year 1972 from Caflo Caicara area, Apure River drainage,
Apure State. Sources: CODESUR (1979) and Taphom and Lilyestrom (1984),
respectively.














CHAPTER 3

METHODS


Fl Sapng


In the field I tried to collect as many individuals, sizes, and species of serrasalm-ine fishes as possible from each region and drainage, but I did not attempt to measure fish biomass. Sampling of fishes was done in all major habitats using appropriate combinations of collecting gear and fishing tactics so as to obtain the most information in a short period of time. Although piranhas were taken in greatest numbers during the day, especially near twilight, night collections were also made in the two major regions studied. For sampling piranhas, I depended mainly on various combinations of seines, gill nets, cast nets, and hook and line. Harpoons, spear gun, midnnow traps, trotlines, and commercial (5% rotenone) and natural (barbasco) fish toxicants were used only rarely; these capture methods contributed little to the total sample of serrasalmine fishes taken. In the field, most fishes collected were preserved immediately in 10-20% formialin; in the laboratory, preserved specimens (those less than about 200 mm SL) were transfered to 70% ethanol or 35% isopropanol. A few young piranhas were kept alive and maintained in aquaria.

Each type of sampling gear targeted a certain size range of fishes. For collecting

young piranhas and other small fishes, I used small nylon seines (6x2 and 5x2 m, 6.4 mm. mesh), nylon and monofilament cast nets ranging from 1.8 to 3 mn diameter (2 to 2.5 cm mesh), and hand nets (3 mm mesh); these were normally limited to use in shallow areas (<1.5 m deep). Small seines and hand nets were the most effective equipment for sampling in areas with dense aquatic vegetation. In instances where vegetation made it difficult to



35







36

effectively puff the seine forward, a seine was set stationary, and one or more "kickers" drove fishes from the vegetation into the net.

Nylon bag seines (6x2 m, with 2x2 rn bag, 6.4 mm mesh) or large beach seines (10x2 m, 6.4 mm mesh) were used in more open shallow water habitats. These nets sampled for a broad range of fish sizes, but because few areas had clean substrates, large seines were usually limited to open beaches along rivers or streams, and lagoons, where there was little submerged debris.

Nylon and monofilament gill nets with float lines were used to sample selectively for medium and large-sized fishes, including adult and subadult piranhas. Gin net sizes were 20x2 rn (20 cm stretch mesh), lOx5 m. (5 cm mesh), 50x2 rn (with two 25-m long panels of 5 and 7 cm mesh, respectively), and lOOx2 m. (6 cm mesh). For taking piranhas, gill nets were set in areas with little or no current, used in conjunction with seines, and in deeper water (>1.5 m) where use of seines was impractical. Set gill nets were monitored and all fish removed every 0.5 to 6 hours, depending on tliine of day and local fish abundance. Because piranhas can damage gill nets, nets set in areas with high piranha densities were checked more frequently.

All piranha species occurring in the Orinoco River basin take baited hooks (personal observation). Hook-and-line fishing was done mostly with natural bait, using hand lines and occasionally rod and reel. Different sizes and types of commercial hooks were used to sample for fishes of different sizes. Type of bait employed was noted so as to not be mistakenly recorded later as part of their natural diet. In general, sampling by hook and line yielded the same piranha species, and proportions of individuals, as those caught by gill net.

Overall, piranha species that were common in any one area were taken by two or more types of sampling gear. No one capture technique seemed to be selective for a particular piranha species, or group of species. Seines, gill nets, cast nets, and hook and






37

line were all occasionally effective in capturing species considered uncommon in a particular drainage or region.

To reduce the risk of missing uncommon or rare species in upper Orinoco

drainages, where most sampling was limited to relatively short periods, I supplemented my own samples with collections of others. In the field, I recorded the catch of hired fishermen and Indians, including the daily hook-and-line collections of camp workers.


Field Site Locations and Sampling Periods


Nine drainages of the Orinoco River basin in Venezuela were sampled during the present study, three in the low Llanos and six in the upper Orinoco (Fig. 3-1).


Low Llanos or Savanna Sites


Three major drainages were studied in the low Llanos of Apure State: the Apure, Cinaruco, and Capanaparo rivers (Fig. 3-2). Principal habitats sampled were rivers, streams, natural and artificial lagoons and pools, and flooded savanna. The Apure drainage was the only site where long-term research on piranhas was carried out.


Apure Drainage. Almost all fieldwork was done in the Caio Caicara watershed of the Apure drainage in and around the Fernando Corrales research station and ranch of the Universidad de Los Llanos (UNELLEZ) (07'25'50"N, 69'35'30"W). This area is bordered by Carlo Caicara, its tributary Calo Maporal, and a smaller stream, Caflo Guaritico. I made periodic samples in the Caio Caicara study area during December 1983; January, March, May, July, September, and November 1984; and March, April, and May 1985; these were followed by samples taken during August 1988, March, April, and December 1989, and January, March, and May 1990. I also examined material taken











38










0 0 0
C\j 0 LO
0


0
0
0
o (D







C\j C\j
(0
0
m Q


>
i:
(D 11-1 (0 (D 00


cr 0 ca
C)
0 Cd
0 cr z on 04
(D Lli 0
(D E =
CL ca
0



U) 04 LO
0 0 0
co co
W z (D
<






V) 0 >
0 r
.
LL)
o
o LLJ C\j 2
0
f
0 -1 0
N (\j (D
>
4.4
0
cn

co


0
0 CC) C"i











39



tD







Cot












un





cn cn


0 CA

0



in
-M











cn cn
0 0










0- 0 ..
cd



0 01
4

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40

between 1979 and 1984, which included monthly samples of a one-year biomass study of the area in 1982-1983 (see Taphorn and Lilyestrom 1984). A total of about two hundred fish collections were made in the Apure River drainage in carlos Caicara and Maporal and their adjacent floodplains from 1979 to 1990.


Cinaruco and Capanaparo drainages. I examined collections made by others from the lower Cinaruco and Capanaparo rivers and their floodplains. Most sites sampled were within 50 km of the north-to-south road joining San Fernando de Apure with Puerto Paez, a route roughly following 67030' W longitude. Samples were taken in January 1982, December 1986, January 1987, and March and April 1989. The 1989 collections were the result of a fish inventory of the two drainages made by D. C. Taphom and A. Barbarino using seines, cast nets, and hook and line. Overall, sites collected were the main channels and near-shore areas of the two rivers, as well as Laguna Larga of the Cinaruco River, and Caflo La Pica and Laguna Brava of the Capanaparo drainage.


Upper Orinoco or Forest Sites


Six major drainages in the upper Orinoco, Amazon Territory of Venezuela, were sampled for analysis of piranha populations from forested regions (Fig. 3-3). These included the Sipapo, Atabapo, Ventuari, Matacuni, Ocamo, and Mavaca drainages, as well as the main channel of the Orinoco River. I collected fishes and evaluated habitats during five expeditions, between early 1989 and 1991, as part of a resource inventory of southern Venezuela in association with the mineral consortium CVG-TECMIN (Corporaci6n Venezolana Guyana Tecnica Minera). Data on serrasalmine fishes from the region are based on intensive sampling of many sites over relatively short periods of time. Each expedition lasted between 25 and 40 field days and covered a different drainage or set of







41



60- + +/

Venezuela



50




N

4*- +






+











0 100
KILOMETERS


670 6 6" 650 640



Fig. 3-3. Map of 1988-1991 sampling sites in upper Orinoco, Federal Territory of
Amazonas, Venezuela Solid circles represent localities sampled by the
author; solid squares represent areas collected by others (specimens from all sites deposited at MCNG and examined by the author). Circles and squares
may represent more than one sampling site.







42

drainages. Work in any one drainage was usually limited to one part of the year, either during the high or low water period.

Lowland habitats sampled in the upper Orinoco were channel borders and beaches of rivers, streams, side channels, old meanders and other back waters, including isolated floodplain lakes, as well as inundated forest. Elevations ranged from 90 to about 240 m above sea level. Collection sites and sampling dates were as follows: (1) Guayapo and Sipapo rivers, from 12 May to 7 June, 1989; (2) lower Ventuari River, including its tributaries the Yureba, Pari, Asisa, Guapuchi ( = Picure), Marueta rivers and the carlos CucuriW, Moriche and Tabi-Tabi, from 17 September to 16 October, 1989; (3) Atabapo River, including its tributaries the Atacavi and Temi rivers and the caflos Patacame, Cuchakrn, Bocachico, and Chimita, from 23 October to 17 November, 1989; (4) Ocamo, Putaco, Padamo, and Matacuni rivers, and the carlos Jayuwapuei, Jenita, Maveti, and Yaraca-bawei, including the upper Orinoco River main channel above its confluence with the Ventuari, from 16 January to 16 February, 1990; and (5) Mavaca River, its tributary Cario Mavaquita ( = Caflo Hauyapiwei), and the upper Orinoco main channel, from 18 January to 20 February, 1991. A total of 200 fish collections representing 180 individual sites was made in this region, resulting in over 18,000 specimens, of which 500 were serrasalmine fishes.


Evaluation of Habitats


A variety of habitat parameters was recorded whenever possible for most collection sites. Qualitative and quantitative estimates were as follows: (1) season (wet, dry, or transitional); (2) water type (clear, black, white, or combination); (3) water level (isolated pools, continuous in bank, bank full, or flood condition); (4) watershed topography (level, moderately rolling, rolling, mountains); (5) stream gradient (flat, slight, moderate, or >30 degrees); (6) land use (natural, cattle, agricultural, or developed); (7) major terrestrial







43

habitat (grassland, savanna, gallery forest, or forest); (8) dominant riparian vegetation (none, grasses/forbes, shrubs/trees, narrow forest border, or forest); (9) water depths at site and capture depths (very shallow [0-5 cm], shallow [5-20 cm], moderate [20-50 cm], deep [50-100 cm], very deep [ 100-150 cm], extremely deep [>150 cm]); (10) water velocities, as measured with a mechanical flowmeter (General Oceanics) or using a floating stick or cork, were classified into six categories (zero [<0.02 m/sec], very slow [0.02-0.10 m/sec], slow [0.10-0.25 m/sec], moderate [0.25-0.75 m/sec], fast [0.75-1.25 m/sec], and torrential [>1.25 m/sec]); (11) water temperature; (12) water pH measured with a Hach pH Pocket Pal meter or a Hach colorimetric (color disc) wide range pH test kit (Model 17-N);

(13) water color and turbidity (very-clear, clear-tannin, clear-green, slightly-turbid, moderately turbid, or very turbid); (14) water clarity as measured with a 20-cm diameter Secchi disk; (15) estimated maximum and average water width; (16) degree of shading (full sun, partial shade, temporary full shade, permanent full shade).

Substrate types and types of aquatic or instream cover for each collecting site were recorded by estimating their proportion of the total surface area: (0)=none/few; (1)<10%;

(2)10-50%; and (3)>50%. Substrate types recognized were: silt/mud; sand; gravel; rubble; boulder; bedrock/claypan; vegetation; litter; and detritus/decomposed organics. Fish cover categories recognized were: floating aquatic vegetation; emergent vegetation; submergent vegetation; litter on bottom; overhanging vegetation; undercuts; bank cover; brush/roots; rocks; logs; and artificial structures (e.g., culverts, bridge piers).


Identification and Nomenclature of Piranhas


At least 12 species of piranha occur in the Orinoco River basin (personal

observation). As with most groups of South American freshwater fishes, there has been a great deal of confusion surrounding the classification and nomenclature of the subfamily Serrasalminae, due to a combination of factors. Some species exhibit marked changes in







44

body shape with growth. Individuals are also fairly variable in terms of body pigmentation and color patterns; such differences can be associated with age, size, or sexual condition, and may also be environmentally induced. To further complicate piranha taxonomy, the complete geographic distribution of most species is unknown. Moreover, because little if any comparative material was available to previous taxonomists, most earlier descriptions were incomplete, and thus inadequate for making accurate identifications. Fink (1988) reported that fewer than half of the about 60 nominal species of piranhas were valid. Nevertheless, sampling in previously uncollected regions has resulted in the discovery of a few new species (personal observation). Except for difficulties in identifying some of the smallest specimens (less than 25 mm. SL), I believe I have successfully sorted out the different species encountered in this study. Preserved specimens examined are deposited in the Museo de Ciencias Naturales (MCNG), UNELLEZ, Guanare, Venezuela. Voucher material has also been donated by MCNG under an official cooperative agreement to the Florida Museum of Natural History (UF), Gainesville, Florida. Institutional acronyms are from Leviton et al. (1985).

Because of the taxonomic confusion, piranhas have often been misidentified in the literature. Drs. William Fink (UMMZ) and Antonio Machado-Allison (MBUCV) are currently revising the piranhas of Venezuela; I have relied on both for identifications of certain voucher specimens. They have also made available their unpublished key to Venezuelan piranhas. Taphomn (1990) prepared keys to the characiform fishes of the Apure drainage, and also listed probable generic and specific synonyms of serrasalmrine fishes. His nomenclature for piranhas follows that of Fink and Machado-Allison. Abbreviations used for piranhas and other serrasalmine fishes in illustrations and tables are given in Table 3-1. In the following section species names used in the present report are listed together with names used by me and colleagues for the same species in recent publications:







45

(1) Serrasalmus altuvei Ramirez 1965: Serrasalmus altuvei in Nico and Taphorn (1988); color illustrations in Nico and Taphorn (1986:33), photos reproduced in Schulte (1988:119).

(2) Serrasalmus cf. eigenmanni Norman 1928: Serrasalmus cf eigenmanni may involve a species complex (W. Fink, personal communication): however, I distinguished only one species in my samples. This species, to my knowledge, has not been previously referenced in publications on Venezuelan piranhas. The piranha Serrasalmus nalseni described and figured by Fernmndez-Y6pez (1969) is a possible synonym, but I have not seen the type series. All previous references to Serrasalmus eigenmanni from the Orinoco probably refer to other species (see Serrasalmus irritans below).

(3) Serrasalmus elongatus Kner 1860: Serrasalmus cf. elongatus in Taphorn and Lilyestrom (1984), Nico and Taphomrn (1988); color illustrations in Nico and Taphomrn (1986), photos reproduced in Schulte (1988:1, 119); photos as S. pingke in Roman (1983:56).

(4) Serrasalmus irritans Peters 1877: S. eigenmanni in Taphomrn and Lilyestrom (1983); S. irritans in Nico and Taphomrn (1988) and Winemiller (1989a, 1989b); color illustrations as Serrasalmus eigenmanni in Nico and Taphorn (1986:31, 33), same photos reproduced in Schulte (1988:120), photos as S. eigenmanni in Rom,.n (1983:57).

(5) Serrasalmus manueli Femndez-Y6pez and Ramnfrez 1967: This species has rarely been referenced in the literature since its original description. I am unaware of misidentifications. There is no published information on its biology or natural history.

(6) Serrasalmus medinai Ramfrez 1965: Serrasalmus caribe in Nico and Taphomrn (1988); incorrectly spelled as S. medini in Winemiller (1989a, 1989b); color illustrations as Pristobrycon sp. in Nico and Taphorn (1986:31, 33, 41), photos reproduced as Serrasalmus (Pristobrycon) sp. in Schulte (1988:119), and as Serrasalmus (Pristobrycon) "iridescent" (incorrect locality given) in Schulte (1988:128); photos as S. rhombeus in Romdn (1983:31,60).







46











Table 3-1. List of abbreviations used in figures and tables for piranhas and other serrasah-nine fishes.

Piranhas: Other Serrasahnine Fishes:

PC Pygocenftw caribe Cm Catoprion mento
Psp Pristobrycon sp. Mag Metynnis argenteus
Pst Pristobrycon sololatus Mya Myleus asterias
Pyp Pygoprislis denticulatus Mys Myleus schomburgkii
Sa Serrasalmus altuvei Myt Myleus torquatus
Seg Serrasalmus cf eigenmanni Md Mylossoma duriventfis
Sel Serrasalmus elongatus
Sir Serrasalmus irfitans
Sm Serrasalmus manueli
Smd Serrasalmus medinai
Sr Serrasalmus rhombus






47

(7) Serrasalmus rhombeus (Linnaeus) 1766: Serrasalmus rhombeus in Nico and

Taphom (1988) and Winemiller (1989a, 1989b); and color illustration in Nico and Taphorn (1986:40-41).
(8) Pygocentrus caribe Valenciennes 1849: Pygocentrus notatus in Taphorn and Lilyestrom (1984), Nico and Taphorn (1988), Winemiller (1989a, 1989b), Nico (1990); color illustrations are given as P. notatus in Nico and Taphomrn (1986:31, 40, 41), photos reproduced as Serrasalmus (Pygocentrus) notatus in Schulte (1988:109, 110), as Serrasalmus niger in Schulte (1988: 111), and as Serrasalmus nattereri (incorrect locality given) in Schulte (1988:12-13).
(9) Pristobrycon striolatus (Steindachner) 1908: Pristobrycon striolatus in Nico and Taphom (1988); color illustrations as Pristobrycon striatus in Nico and Taphorn (1986:31, 41), and as Pygocentrus striolatus in Nico and Taphorn (1986:33), photo reproduced in Schulte (1988:120). Machado-Allison et al. (1989) concluded that Pygopristis antoni Ferndndez-Y6pez, 1965 is a junior synonym of P. striolatus.

(10) Pristobrycon sp.: This species is in the process of being described as new by W. Fink and A. Machado-Allison.

(11) Pygopristis denticulatus Muller and Troschel 1844: photograph as Serrasalmus (Pygopristis) antoni in Roman (1983:51).


Faunal Comparisons


The Coefficient of Biogeographic Resemblance (CBR) proposed by Duellman (1990) was used to compare the composition of piranha assemblages between the two regions studied and among the different drainages. This qualitative index of similarity has been reinvented a number of times, consequently it is known by several names including the Faunal Resemblance Factor, the Sorenson Index, and the Dice Coefficient (Boesch 1977, Romesburg 1984, Magurran 1988, Duellman 1990). This index is one of the more







48

commonly used measures for comparing species presence-absence data (Krebs 1989), and is calculated as:

CBR = 2C/ (Ni + N2),

where C is the number of species common to two areas, NI is the number of species in the first area, and N2 is the number of species in the second area. The resulting values range from 0, if there are no species in common, to 1, if both areas share the same number and kinds of species. This measure is simple, is not affected by relative numbers of individuals, and thus is best used when there are no reliable quantitative data on abundance of species (Magurran 1988, Krebs 1989). Binary similarity measures are not totally independent of sample size (Wolda 198 1, Krebs 1989). However, comparisons when maximum number of possible species is low give results less affected by sample size differences than those dealing with many species (see Krebs 1989). CIBR is very similar to the Jaccard Coefficient (Boesch 1977, Romesburg 1984, Duellman 1990); it doubly weights shared positive attributes (i.e., joint presences), and is preferred over the Jaccard Coefficient if the entities vary widely in their number of positive attributes (Boesch 1977:22).

To make presence-absence data more reliable, I supplemented my data with

information from collections deposited at MCNG and UF. I also reviewed the literature for records of species occurrence. A Spearman rank correlation test was used to test for an association between species composition and drainage area size, and between faunal similarities and distances among drainages. The similarity or resemblance matrix generated from the CBR equation was used as a basis for clustering drainages, employing the unweighted pair-group method using mathematical averages, or UPGMA.







49





In order to analyze diets and document ontogenetic shifts in feeding, sampled fishes were divided into five size classes: Group 1) 10-19 mmn SL small juveniles; Group 11) 2039 mm SL; Group HII) 40-79 mmn SL; Group IV) 80-159 num SL; and Group V) 160 mm SL. Several species were not represented by all size classes.

During the study, more than 2,000 serrasalmine fishes were captured; total number of specimens examined for stomach contents was 1,538 from the low Lianos and 393 from the upper Orinoco. Standard length (SL) of each specimen was measured to the nearest mm. Although a few of the largest fish were dissected and examined in the field, most specimens were preserved after capture and dissected later in the laboratory to determine stomach contents. I examined stomach contents and recorded frequency of occurrence

(0), number (N), and dominance by bulk (D) for each food item. I also recorded volume

(V) of food items found in stomachs of fishes taken in the field after 1986. Small food organisms were counted using a Ward counting wheel under 25X magnification. Volume was determined by water displacement using appropriately- sized graduated cylinders. Volumes of smaller items were calculated by measuring dimensions with Vernier calipers or by examidnation under a dissecting microscope and comparison with known volumes. An estimate of relative stomach fullness was made using scores ranging from 0 (empty) to

3 (if full, or almost full) (Thomerson and Wooldridge 1970, Nico and Taphomn 1988).

For specimens collected in the Apure River drainage before 1986, I estimated

volume using a point system, referred to as adjusted volume (Va), and derived from D and stomach fullness (Nico and Taphorn 1988). That is, only the dominant food categories of a given stomach were included and each was assigned the fullness points (1-3) for that stomach. If two food items in a single stomach were of about equal volume, each received half the fullness value. Thus, %Va = total fullness points for each food category as a percentage of all fullness points, and can be shown as:







50



%10Va Y, Fj /YTi,) x 100,
n n
where Fi is the fullness points for stomachs whose dominant food item is F; Ti is total fullness points for all stomachs; and n is the number of stomachs examined of a species or size class.

I attempted to identify food items to the lowest taxonomnic level, whenever possible. For comparing piranha diets, I recognized eleven general food categories: (1) masticated seeds crushed or fragmented seeds together with the hard parts (mainly endocarp)that surround the seed; (2) other plant material mostly leaves, root fragments, fleshy fruits, and flowers; (3) decapods crabs and shrimp; (4) microcrustaceans copepods, cladocerans, ostracods and conchostracans; (5) aquatic insects various families, including larvae and adults; (6) other invertebrates mostly arthropods, including terrestrial forms, but also aquatic nematodes and snails; (7) small whole fish at least two-thirds of total body; (8) fish flesh pieces of flesh bitten from fish; (9) fish fins fins not taken with or attached to pieces of flesh; (10) fish scales scales not taken with or attached to flesh; and

(11) other detritus, sand, nonfish vertebrates, and unidentifiable items.

I compared and contrasted diets within and among the different species and size groups by calculating estimates of diet breadth and overlap based on percent food volume or adjusted volume. Because I did not quantitatively measure the relative availability of food resources in the field, I chose two widely used indices of breadth and overlap that do not take into account the relative abundance of the various food items in the natural environment.

Diet breadth, or width, measures the diversity and evenness of resource use. Diet breadth was computed for each species' size class using Levins' index of niche width (Levins 1968, Krebs 1989):







51

Diet breadth (B) = 1/ jp2
n

where Pi is the proportion of food category i in the diet. B ranges from 1, when one resource state is used exclusively, to n (the total number of food categories recognized), when all resource states are used in equal proportion. This measure is the reciprocal of Simpson's index of diversity (Krebs 1989).

Ii used the Schoener Overlap Index (Schoener 1970) to estimate the similarity in diets between and within species. This particular index is also known as the Renkonen Index, the Percent or Proportional Similarity Index, Percentage Overlap, and Czekanowski's Index (Krebs 1989); the Bray-Curtis Coefficient gives the same results as the above index if its scores are standardized (Boesch 1977:26, Bloom. 198 1). The Schoener Overlap Index is calculated as:



Overlap = 1 0.5( 1 x pi I (minimum pxi, pyi),
n



where pxi is the proportion of food category i in the diet of species x, pyi is the proportion of food category i in the diet of species y, and n is the number of food categories. The Schoener Index gives values from 0 to 1 (or 0 to 100%) indicating no overlap to complete similarity in the proportion of food categories used by the two groups compared.

There are many indices available for estimating niche or diet width and overlap, but as yet there is no general consensus as to which of the many indices is best (Huribert 1978, Abrams 1980, Wallace 1981). Recent reviews of frequently used indices include Ludwig and Reynolds (1988) and Krebs (1989). All measures of breadth and overlap are biased in some way, the bias usually being reduced with increasing sample size (Schluter 1988, Krebs 1989). It has also been shown that measures of breadth and overlap are sensitive to the number of resource categories used. Although lumping resource states can inflate niche







52

overlap values (Greene and Jaksic 1983), bias increases as the number of resource categories used increases or is large (Ricklefs and Lau 1980, Smith and Zaret 1982, Krebs 1989). Overlap and breadth indices also give somewhat different results depending on the methods used to tabulate dietary components, for example, percentages based on total food volume, weight, frequency of occurrence, or food item number (Wallace 198 1). An additional problem implicit in all overlap and breadth measurements is that the investigator may recognize resource categories that animals do not. For instance, Goulding et al. (1988:52) suggested that Arnazonian frugivorous fishes "select their preferred fruits and seeds at what taxonomically are referred to as genera" rather than at the species level. Conversely, organisms may distinguish resources lumped together by human observers (Ludwig and Reynolds 1988, Krebs 1989). Finally, most overlap and width indices are based on the relative use of different resources, without accounting for their relative availabilities. However, resource availability is difficult to assess and therefore rarely measured. Those indices that do incorporate some estimate of food availability into their equations are generally less simple to interpret and more variable between sites (Schluter 1988). Abrams (1980) and Wallace (198 1) recommended the Schoener Index as the best of the measures of niche overlap when available resources to the organism have not been quantified. Krebs (1989:304-306), referencing Wolda (1981), regarded this measure as one of the better quantitative similarity coefficients available, showing that it is relatively little affected by sample size and number of species (i.e., resources states).

Because percentage of occurrence and percentage of total number of food items tend to over-emphasize the importance of small food items, I used proportions based on total food volume for calculating diet widths and overlaps. Using food volume introduces the possible bias that a large prey item in a single large piranha might overshadow all other items when pooling stomach contents data. However, this problem is overcome to a large extent by dividing fish into different size classes and treating each size class as a separate "trophic unit" (sensu Stoner and Livingston 1984).







53

In my analysis of diets, the similarity or resemblance matrix generated from the Schoener Index was used as a basis to cluster species using the unweighted pair-group method using mathematical averages, or UPGMA. I used 2 x 2 contingency table X2 tests (one-tailed) and Mann-Whitney U-tests to test the prediction that forest populations fed more on plant material than their savanna counterparts.


Nutrient Content Analysis of Food Items



In order to compare nutrient values, analyses were carried out to determine ash, crude protein, total fat, carbohydrate, and energy contents of different food items. Three types of food items were examined: small whole fish, fish fins, and fish scales. I also searched the literature for information on the nutrient value of other types of general food items, for example insects and various types of plant material. Prey fishes used for analysis were taken from the Apure River drainage, Venezuela, using cast nets and seines during the dry season in December 1989 and March 1990. Tissues from members of two unrelated families of fishes were tested: (1) Curimatidae, represented by Curimatella immaculata, Cyphocharax spilurus, and Steindachnerina argentea; and (2) Cichlidae, Aequidens pulcher and Cichlasoma orinocense. These species are common in the Orinoco River basin and are frequently preyed upon by juvenile and adult piranhas.

In total, 135 small cichlids (SL range 39-77 mm) and 96 curimatids (SL range 4578 mm) were used for nutrient content determinations. Fish were placed on ice immediately after capture, transported to the laboratory at the Universidad de Los Llanos Occidentales (UNELLEZ) in Guanare, Venezuela, and refrigerated until analysis was conducted. Body scales were removed from partially frozen specimens with a small fish scaler, and no attempt was made to clean off the body's outer mucous layer. Only caudal and dorsal fins were used for fin samples; these were removed by clipping with scissors above the fin base to avoid scales. Two or three entire cichlid and curimatid specimens







54

were used for tests as small whole fish. All subsequent nutrient analyses were carried out at UNELLEZ under the direction of the biochemist Dr. Margioly de Morales. Samples were oven-dried to constant weight at 60 T to prevent lipids in the body tissues from volatilizing. After drying, samples were ground in a Willey mill and stored in desiccators. Unless otherwise stated, methods of analysis used follow AOAC (1980) guidelines. Results are expressed as percentages of dry weight, rather than as percentages of ash-free dry weight (i.e., on organic matter basis), for ease of comparison to previously published data. Ali measurements were duplicated; the differences between replicate subsamples of a particular food item were generally less than 1%. Ash contents were determined by combustion of samples of dried body tissue at 550 T for 3 hours (Pierce et al. 1980). Total fat content was determined by extracting lipids for four hours with diethyl ether. Crude protein was determined by the Kjeldahl method for nitrogen, where crude protein is total nitrogen concentration multiplied by 6.25. Carbohydrates were deten-nined as the sum of crude fiber and nitrogen-free extract; total carbohydrates are the sum of both values. Energy content was measured using a Parr bomb calorimeter and expressed as 0 per g; this can be converted to kilocalories per g by dividing by 4.184.


Intestine Length


Length of the intestinal tract (IL) was determined by removing the entire

gastrointestinal tract, placing the extended intestine (without stretching) on a flat surface, and measuring the distance from the pylorus to the anus (Ribble and Smith 1983). Fecal material was left in the intestine during measurement. Relative intestine length for each fish was calculated by dividing IL by standard length (SQ. An analysis of covariance (ANCOVA) was carried out in order to compare the regression lines of IL versus SL among species. A Spearman rank correlation test was used to test for an association between relative intestine length and the percent volume of plant material among the






55

different species. My data indicated allometric changes in intestine length. In order to reduce variation and make comparisons more valid, only specimens > 80 mm SL were used in correlation analysis.


Field and Aquarium Observations


I made qualitative and quantitative observations on the feeding behaviors of wildcaught juvenile and subadult piranhas maintained live in aquaria or large outdoor concrete tanks (L. Nico, unpublished data). Species represented from low Llanos populations were Pygocentrus caribe, Serrasalmus elongatus, S. irritans, S. medinai, S. rhombeus, and Pristobrycon striolatus; those from upper Orinoco sites were Pygopristis denticulatus and Serrasalmus manueli. In the field, most observations of piranha feeding behavior were done from shore or from boats while fishing, these qualitative observations totaled over one hundred hours. I also made brief underwater observations on the feeding behavior of several species totaling about five hours. Underwater observations were made using mask and snorkel in clearwater and blackwater streams in the states of Bolivar, Guarico, and Monagas. Species observed were juveniles or subadults of Serrasalmus irritans, S. medinai, S. rhombeus, and Pygocentrus caribe.


Statistical Analyses


All nonparametric tests were run using the computer software program Basic

Statistical Subroutines by DYNACOMP (1983) following Siegel (1956) and Siegel and Castellan (1988). Statistical tests of ANCOVA were done using the SuperANOVA program on a Macintosh SE/30 computer. For cluster analysis, I used the computer program NTSYS-pc (Numerical Taxonomy and Multivariate Analysis System) version 1.5 by Rohlf (1988). Cluster analysis has been shown to be a useful and reliable multivariate







56

procedure for identifying feeding patterns in assemblages of fishes (Stoner and Livingston1984, Henderson and Walker 1986) and other vertebrates (Jaksfc and Medel 1990). The method has also been used extensively to describe fish distribution patterns (Hocutt and Wiley 1986). Basically, the UPGMA clustering technique generates a hierarchical tree, or dendrogram, grouping together those samples or objects that are most similar. UPGMA is widely applied because it can be used with a variety of resemblance coefficients and also because it forms clusters in a more conservative manner than many other clustering methods (Gauch 1982:199, Romesburg 1984, James and McCulloch 1990:147). As a measure of secondary validity, an additional clustering technique, complete linkage (farthest neighbor), was used to assess whether resulting clusters were more-or-less real rather than mathematical artifacts (Gauch 1982, Romesburg 1984).















CHAPTER 4
COMPOSITION OF PIRANHA ASSEMBLAGES In this chapter I compare the species composition of piranha assemblages from the low Llanos to those from the upper Orinoco. I also examine and compare species composition and richness among the nine drainages sampled, and present possible habitat correlates. Little has been published on the distribution of Orinoco River fishes, with the upper Orinoco being that part of the basin least explored ichthyologically. Because sampling effort was not equal among all the drainages, I supplementedmy data with information from museum collections and published records. Although additional collecting will likely add a few species to faunal lists for several of the drainages, the data presented represent a first attempt at understanding piranha distribution patterns and habitat preferences.

Figure 4-1 is a schematic representation showing the relative distances among drainages in relation to their confluence with the main channel of the Orinoco River. Table 4-1 is based on my samples supplemented by museum material, and shows the species composition by region and drainage. A total of eleven piranha species were taken from the two regions studied. Since 1979, ten species have been collected from the low Llanos of Apure State, whereas my 1989-1991 samples indicate that at least eight species occur in the upper Orinoco of the Amazon Territory of Venezuela. Seven species were widely distributed and inhabited both regions. The Coefficient of Biogeographic Resemblance (CBR) value comparing piranha species composition between the low Llanos and the upper Orinoco was 0.78.

Piranha assemblages in five of the six upper Orinoco drainages were numerically dominated by either S. rhombus or S. manueli, or both. The exception was the Mavaca


57






58






Ocamo Mavaca
Matacuni 1000 km





Ventuari AtabapoQ Sipapo -500 km




Cinaruco Capanaparo Apure
0 km ORINOCO RIVER




Fig. 4-1. Schematic representation showing relative distances among the nine sampled
drainages and their approximate location along Orinoco River main channel.
Arrow indicates division between upper and lower Orinoco.









59









CL4 CIO U W)


un




cn cn


>


z
u

00 &OD
a4 04 CIA











a4 u u 04





a4 a., CLO a4 0-( a,





U U a4 U 0.4 CL4
46




Z3
iz "I "ts ;t

4 lo vi


to qj
co C11 C-n







60

River, where Serrasalmus cf. eigenmanni was the most common piranha collected. Pygocentrus caribe is the predominant piranha throughout most of the Llanos, and was abundant in samples from the Apure River drainage although absent or uncommon in the Cinaruco and Capanaparo. Pygocentrus caribe was rare in the upper Orinoco. Serrasalmus irritans and S. medinai were locally common in the low Llanos, but neither was taken in the upper Orinoco. Serrasalmus manueli, although absent from much of the Llanos, was commonly taken along with S. rhombeus in the Cinaruco River. Pristobrycon striolatus, although widespread, was never common in any one drainage.

Species occurred in one to seven of the nine drainages sampled (Table 4-1); most were found in several (mean = 4.1) drainages, with Serrasalmus rhombeus and Pristobrycon striolatus (taken in seven drainages) being the most widespread. Several species were absent from two middle drainages, the Sipapo and Atabapo rivers. Two species were limited to single drainages. In the Orinoco River basin, Pristobrycon sp. is known only from the Atabapo drainage. Serrasalmus medinai was represented only in Apure River samples (although it is found in other Orinoco tributaries that fringe the Llanos, drainages not included in this study).

The number of piranha species per drainage ranged from 1 to 8 (mean = 5.0) (Table 4-1). Sipapo drainage samples yielded only one piranha species (Serrasalmus manueh), whereas all other drainages were inhabited by three or more species. The Apure had the highest number of species (eight), but it was also the largest and best sampled drainage. There was a significant correlation between numbers of piranha species and size of drainage area (Spearman rank correlation, rs = 0.67, one-tailed P < .05, n = 9; Table 42, Fig. 4-2).

Species composition of piranha assemblages across drainages was highly variable; CBR values ranged from 0 (i.e., no species in common) to 0.83 (Table 4-2). Adjacent drainages often shared many of the same species (Table 4-3), but waterways that had many species in common (i.e., high CBR) were not always those drainages that were







61

geographically close (Fig. 4-3, Table 4-2). For instance, the Mavaca and Cinaruco were somewhat similar in terms of species composition (CBR = 0.73), yet the two drainages are far apart geographically. Similarly, the Apure drainage had four species in common with the Ocamo, even though these two rivers are separated by roughly 1000 km of waterway (Fig. 4-1). As expected, there was a significant negative correlation between species composition resemblance (i.e., CBR) and the distance between adjacent drainages (rs =

- 0.66, one-tailed P <.05, n = 8; Table 4-2, Fig. 4-3). However, the relationship was not significant at the 0.05 level when plotting all possible combinations of drainage-pair distances against their CBR values (rs = 0.23, one-tailed, .10 > P > .05, n = 36; Table 42, Fig. 4-4).

Figure 4-5 summarizes results of a UPGMA cluster analysis showing affinities

among the nine drainages based on CBR similarity values given in Table 4-3. In addition to similarity in species composition, most resulting groups of drainages were related by either geographic proximity, characteristics of the drainage (e.g., water type), or some combination of these two factors. The first major cluster consisted of the three savanna drainages (Capanaparo, Cinaruco, and Apure) and one upper Orinoco tributary (Ventuari). The Capanaparo and Cinaruco are adjacent drainages and both were classified as blackwater, but each receives high input from clearwater streams. The Apure River is a whitewater river with many small blackwater and clearwater tributaries. The Ventuari also is mainly a whitewater river although it has several large blackwater and clearwater tributaries. The second major cluster was formed by three drainages in the upper Orinoco. This cluster consisted of the Matacuni, Ocamo, and Mavaca; all are whitewater rivers and geographically close. The remaining two drainages, the Sipapo and Atabapo, did not cluster with any of the other drainages. They were blackwater rivers with relatively few piranha species. Clustering based on the farthest neighbor strategy resulted in drainage groupings identical to that of the UPGMA method.







62




Table 4-2. Distance between drainages and Coefficient of Biogeographic Resemblance (in parenthesis) among nine sampled drainages in the Orinoco River basin. Distances measured in kilometers between drainage mouths by way of Orinoco River main channel. CBR values range from 0 (no species in common) to 1 (complete similarity in species composition)


River Drainages

Low Llanos Upper Orinoco

Apu Cap Cin Sip Ata Ven Mat Oca Mav


Drainage area
(km2 x 103) 167 35 25 13 9.4 40.5 10.1 9.8 5.3

Number of 8 7 6 1 4 6 3 5 5
piranha species

Apure 110 160 400 530 610 945 965 1000
(0.80) (0.57) (0) (0.33) (0.57) (0.36) (0.62) (0.62) Capanaparo 50 290 420 500 835 855 890
(0.77) (0.25) (0.55) (0.77) (0.20) (0.50) (0.50) Cinaruco 240 370 450 785 805 840
(0.29) (0.60) (0.83) (0.44) (0.55) (0.73) Sipapo 130 210 545 565 600
(0.40) (0.29) (0) (0) (0) Atabapo 80 415 435 470
(0.60) (0) (0.22) (0.44)

Ventuari 335 355 590
(0.44) (0.73) (0.73)

Matacuni 20 55
(0.75) (0.75)

Ocamo 35
(0.80)

Mavaca






63













10
(D
CYU

Apu
g Cap

, 6 Cin oVen
S0 ooca
o May
. 4 OAta
CZ
OMat
2- = Low Llanos
0o O = Upper Orinoco
Sip
0 .......i.. I I ...... I 1 1
3.0 3.5 4.0 4.5 5.0 5.5 6.0

Log drainage area (km 2)


Fig. 4-2. Scatter diagram showing relationship between number of piranha species per
drainage and log of the drainage area size (km2) for nine sampled drainages in
Orinoco River basin, Venezuela. Drainage abbreviations are: Apu = Apure, Ata = Atabapo, Cap = Capanaparo, Cin = Cinaruco, Mat = Matacuni, May =
Mavaca, Oca = Ocamo, and Sip = Sipapo.







64




Table 4-3. Number of shared piranha species and Coefficient of Biogeographic Resemblance (CBR) (in parenthesis) among nine sampled drainages in the Orinoco River basin. CBR values range from 0 (no species in common) to 1 (complete similarity in species composition).

River Drainages

Low Llanos Upper Orinoco


Apu Cap Cin Sip Ata Ven Mat Oca Mav Number of
piranha species 8 7 6 1 4 6 3 5 5


Apure 6 4 0 1 4 2 4 4
(0.80) (0.57) (0) (0.33) (0.57) (0.36) (0.62) (0.62) Capanaparo 5 1 2 5 1 3 3
(0.77) (0.25) (0.55) (0.77) (0.20) (0.50) (0.50) Cinaruco 1 2 5 2 3 4
(0.29) (0.60) (0.83) (0.44) (0.55) (0.73) Sipapo 1 1 0 0 0
(0.40) (0.29) (0) (0) (0) Atabapo 2 0 0 1
(0.60) (0) (0.22) (0.44)

Ventuari 2 4 4
(0.44) (0.73) (0.73)

Matacuni 3 3
(0.75) (0.75)

Ocarno 4
(0.80)

Mavaca







65











1.0
cr

0.8 00 0
0
C
E 0.6 0



4- 0.4 00
0
C- 0

0.2
0
0
0.0 ,
0 100 200 300 400

Distance between adjacent drainages (kin)


Fig. 4-3. Scatter diagram showing similarity in piranha species composition between
adjacent sampled drainages versus distance between adjacent drainages.
Similarity measure was Duellman's (1990) Coefficient of Biogeographic
Resemblance.







66










1.0


0 0.8E *

U 0.60
( ~0.62 0 .0
0 .








vausaditnesaefo 0.0l 4- 2 .







67







0 0.5 1.0
I Water Types Dominant
Vegetation

APURE W (B,C) S


CAPANAPARO B (C) S

CINARUCO B (C) S

VENTUARI W (B,C) F MATACUNI W F

OCAMO W(B) F

MAVACA W (B) F

SIPAPO B (C) F


ATABAPO B F
I I I I
0 0.5 1.0
Coefficient of Biogeographic Resemblance




Fig. 4-5. Dendrogram from cluster analysis depicting similarities among nine sampled
drainages of Orinoco River basin based on piranha species composition. Major and minor (in parenthesis) water types, W = whitewater, B = blackwater, and C = clearwater; Dominant regional flora, S = savanna (low Llanos), and F = forest
(upper Orinoco). Similarity values are from Table 4-3. Clustering technique was UPGMA, and similarity measure was Duellman's (1990) Coefficient of
Biogeographic Resemblance.







68



A summary of species occurrence by habitat type is given in Table 4-4. Most species were found in a variety of environmental conditions, but relative abundances differed among sites. Serrasalmus rhombeus and S. manueli were frequently taken in riverine habitats; other piranhas were more common in floodplain habitats (e.g., lagoons or old meanders) and in caflos with slow currents. In those cases where piranhas were found in large streams or rivers, they commonly congregated in adjoining slackwaters near the interface between fast-flowing and still waters, for example near the mouths of sloughs or deep carios.

Most piranhas were found in two or all of the three major water types (Table 4-4), but greatest numbers occurred in whitewater habitats. Three species (i.e., Serrasalmus manueli, Pygopristis denticulatus, and Pristobrycon sp.) were usually associated with lowpH, blackwater habitats. Nevertheless, most species seem to tolerate a wide range of temperatures and pH, as shown by wild-caught juveniles of both S. manueli and P. denticulatus that have survived nine months (to date) in aquarium water with pH as high as

8.5. Water temperatures at sample sites ranged from 24.5 to 38 'C, and pH 4.5 to 7.2; water transparency ranged from very turbid (10 cm as measured with a Secchi disk), to very clear (>3 m).

Where piranhas occur, two or more species are commonly taken together. In the low Llanos, juveniles and subadults of as many as five species (i.e., Pygocentrus caribe, Serrasalmus altuvei, S. irritans, S. medinai, and S. elongatus) were occasionally taken in single seine hauls in floodplain pools of the Apure drainage. In the upper Orinoco, adults of as many as four species of piranha (e.g., Serrasalmus rhombeus, S. cf. eigenmanni, Pygocentrus caribe, and Pristobrycon striolatus) were caught together in gill nets set during evening twilight. Sites of highest species richness were characterized by a large amount of instream cover or other protection, including mats of aquatic vegetation, adjacent flooded forest, or deep water. Small juvenile piranhas (<40 mm SL) were only found in







69

microhabitats where there was high cover provided by herbaceous plants. In the Llanos, small piranhas relied on water hyacinth or flooded grasses for shelter and as a foraging place. In the upper Orinoco, young juveniles were limited to a few sites where there were mats of flooded grasses (e.g., stream edges) or shallow waters with dense growths of submergent plants, such as beds of the aquatic plant Elodea.











70






cq C14 C14

to






mm
tA C14 C14 tn
I
r
cq C14



COS tn
cq kn
r
tm. A



















x






x x





C6






04
C




X X X


co
4.3








LZ tu C-0

Aw



z















CHAPTER 5
TROPHIC ECOLOGY OF SAVANNA PIRANHAS: THE APURE DRAINAGE


This chapter focuses on the diets of piranhas from the area around the Fernando Corrales ranch and research station of the University of the Western Llanos (UNELLEZ), located in the Caflo Caicara region, Apure River drainage, in the low Llanos (Fig. 5-1). I give this drainage separate treatment because it is the only site where long-term sampling (1979-1990) has been carried out (Taphorn and Lilyestrom 1984, Nico and Taphorn 1984, 1985, 1988, Nico 1990, Taphorn 1990). The existing data base on piranhas from the Calo Caicara region is the most complete of any single locality or drainage in the Orinoco basin. The seven species examined were Pygocentrus caribe, Serrasalmus altuvei, S. medinai, S. elongatus, S. irritans, S. rhombeus, and Pristobrycon striolatus (Fig. 5-2). I also report on the diet of the serrasalmine Catoprion mento, a close relative of the piranhas.


Study Area


The study area is located in the low Llanos of Apure State (07025'50"N,

69035'30"W) about 80 km W of the town of Mantecal (Fig. 5-1). Several permanent streams border the 12,600-ha ranch, catlos Caicara, Maporal, and Guaritico. These lowgradient streams have mostly silty bottoms, and are bordered by narrow gallery forests. The ranch is maintained primarily for grazing of cattle and encompasses open flat savanna with a very gradual sloping terrain west to east. Most of the savanna floodplain of the ranch is surrounded by a 2.5 m high earthen dike constructed to control flooding during the rainy season and hold water during the drier part of the year. During the rains most of the


71









72























20
w GO




4-1
0
0










4-4
0

0










C)


+-0
C)



> w 4.
0
0 0
0


0
0




























Fig. 5-2. General body form and major fin markings of seven piranha species (55-70 mmn
SL) and Catoprion mento (Cm) from Cafto Caicara study area, Apure Drainage,
in the low Lianos of Venezuela: Pc = Pygocentrus caribe; Pst =Pristobrycon
striolatus; Smd = Serrasalmus medinai; Sr = Serrasalmus rhombeus,
Sa =Serrasalmus altuvei, Sir =Serrasalmus irritans, and Sel = Serrasalmus
elongatus.





74



0

PC 0
Pst




Smd Sr




Sa 311




Sel cm







75

savanna becomes flooded, with low areas covered by as much as 2 m of water. Lower areas and deeper borrow pits contain water throughout the year, but most permanent water sites are reduced to less than 1 m depth during the dry season. The fish species composition of borrow pits resembles that of natural lagoon habitats. Large free-floating mats of vegetation, primarily Eichhornia crassipes and E. azurea, are common in streams and savanna pools. During high water, fishes can move between the streams and the interior of the diked areas through culverts or low sections of the dike, but this interchange has been greatly reduced as dike stability has been achieved. During the late dry season (January to early April), the streams have little or no flow and are often reduced to isolated pools. Rainy season flow is continuous with depths to 5 m or more. Width ranges from 3 to 12 m during low water to over 30 m during peak flooding. Although the Apure River itself is white water in character, streams of the study area are essentially blackwater habitats with low transparency. The flooded savanna pools are white water habitats, usually very turbid (< 10 cm Secchi disk), but the larger poolIs often become quite clear (> 1 m Secchi disk) late in the rainy season.



Species Accounts


In this section, I describe the general morphology, local distribution and habitat, and the diets of the piranha species found in the Cafto Caicara study area. Information on the smallest size class of piranhas, juveniles less than 20 mm SL, were pooled; all were tentatively identified as Pygocentrus caribe. Figure 5-3 is a summary of the diets by size class (Group HI and larger) of the seven piranhas and Catoprion mento from the Caflo Caicara area.
































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Pygocentrus caribe (Valenciennes 1849)

Pygocenrus caribe was the most abundant piranha in the Carlo Caicara area,

occurring in both flooded savanna and flowing waters. This blunt-headed, heavy-bodied species (Fig. 5-2) reaches approximately 300 mm SL. Stomach contents of 516 P. caribe in the four larger size classes are given in Table 5-1 and Figure 5-3. Unlike most other piranha species, fish fins and scales were of minor importance in stomachs of juveniles. Group II fish fed most heavily on aquatic insects, followed by microcrustaceans, but for Group 1II fish flesh was the most important food item, followed by plant material (primarily vascular plant debris) and aquatic insects. Larger P. caribe of groups IV and V took mostly fish flesh and whole small fish.
Thirty-two species of prey fishes (mostly characins) were identified from stomachs of Groups IV and V P. caribe (Table 5-2). There were also several instances of cannibalism by adults on small juveniles. In addition to fish, larger juveniles and adults sometimes ate other vertebrates, perhaps as carrion. Different stomachs contained a chunk of flesh from a small caiman (Caiman crocodilus), skin of a lizard (probably Ameiva), and a small adult leptodactylid frog. Three individuals taken together had stomachs full of feathers, flesh, and bone fragments of a white-faced whistling duck (Dendrocygna viduata). Mammals were not found in P. caribe from the study area, but I have found flesh and fur of small rodents in specimens from nearby localities.


Serrasalmus irritans Peters 1877

Serrasalmus irritans was very common, usually second only to P. caribe in

numbers of individuals at most sampling sites. My sample consisted of 271 specimens (Table 5-3 and Fig. 5-3). It has a moderately pointed snout (Fig. 5-2) and is seldom longer than 160 mm SL. My study shows that juvenile S. irritans (Groups II and III) specialized on fins of other fishes. Stomachs of the young of this piranha were typically packed exclusively with fins, mostly from fish smaller or similar in size to the predator.










79





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80






Table 5-2. List of vertebrate prey taxa identified from the stomach contents of the four most common piranhas from the Cafto Caicara area, Apure River drainage, in the low Llanos of Venezuela.


Species Vertebrate Pre y
(fiNuency of occurrence)


Pygocentrus cailbe Fish (whole or flesh): Characidae Aphyocharax erythrurus (6), Astyanax
bimaculatus (1), Astyanax sp. (3), Charax sp. (2), Cheirodon pulcher (1), Ctenobrycon spiturus (22), Gymnocorymbus thayeri
(15), Hemigrammus ntarginatus (5), Hemigrammus sp. (5), Moenkhausia dichroura (2), Odontostilbe pulcher (7), Poptella orbicularis (6), Pygocentrus caribe (6), and Roeboides affinis (1), Roeboides dayi (8), Roeboides sp. (3), Serrasalmus eigenmanni (1), Serrasalmus sp. (1), Triportheus sp. (1); Curimatidae Curintata Pxtae (10), curitnatids (14); Lebiasinidae Pyrrhulina cf. lugubris (2); characoid (8); Cichlidae Microgeophagus ramirezi (2), Gymnotidae Gymnow carapo 1); Stemopygidae Sternopygus macrurus (1), and Eigentnannia spp. (10); Hypopomidae Hypopornus sp. (1); Auchenipteridae Entoffwcorus garneroi (1) and Parauchenipterus galealus (1); Pimelodidae Pimelodella sp.(I); Caffichthyidae Hoplosternum littorale (1); Rivuhdae (1). Fins of Hypophthalmidae Hypophthalms cf. edentatus (1); Characidae Triportheus sp. (1). Reptiles: Flesh of Caiman crocodiles (1); flesh of lizard, probably Ameiva (1).
Amphibians: Small adult leptodactylid frog. Birds: Feathers and flesh of white-faced whistling duck (Dendrocygna viduata) (3).

Serrasalmus irdtans Fish (whole or flesh): Characidae Ctenobrycon spilurus (1),
Odontostilbe pulcher (2), Hemigrammus sp.(l), small juvenile Pygocentrus caribe (1); Curimatidae Curinwta n7etae (1), curimatid
(1); characoid (4); gymnotoid (1); Cichlidae Microgeophagus randrezi (1), cichlid (1). Fins of adult Pygocentrus caribe (2).

Serrasalmus metgnai Fish (whole or flesh): Characidae Aphyocharax erythrurus (1),
Hemigrammus nwrginatus (2), Hemigrammus sp. (1), and Odontostilbepulcher (2), characid (2); Curimatidae Curinwta ffwtae
(2), curitnatid (1); Cichlidae Microgeophagus rapdrezi (1); gymnotoid (1); catfish (1); Fins from Loricariidae (1).

Serrasalnws rhombus Fish (whole or flesh): Characidae Astyanax bitnaculatus and Charax
sp.(l), characid (1); characoid (1); Doradidae Agamxis? (3); unidentified catfish (1); Fins of Characidae Pygocentrus caribe (1); Erythrinidae? (1).
Amphibians: Small adult frog (1).












81







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It was usually not possible to identify the fins eaten, but the thick red anal fins of Pygocentrus caribe were found in two individuals. Large S. irritans preyed mostly on small whole fish, fish flesh, fins, and occasionally scales. Fishes eaten whole or in pieces by S. irritans are given in Table 5-2. A small juvenile P. caribe was found in the stomach of one individual. No nonfish vertebrate remains were found.


Serrasalmus medinai Valenciennes 1849

Serrasalmus medinai was the third most common piranha in the study area; 124 specimens were analyzed for diet (Table 5-4 and Fig. 5-3). It is a medium-sized piranha, usually less than 160 mm SL with a head shape that is intermediate between the robust P. caribe and species with pointed snouts (Fig. 5-2). Unlike Pygocentrus, but similar to other Serrasalmus, it has a series of ectopterygoid teeth that is easily seen even in small individuals (from about 25 mm SL). It is primarily a fin-eater when small (20-79 mm SL). The largest individuals (Group IV) fed chiefly on fish flesh, fins and scales, and small whole fish. Prey fish identified from the stomachs of S. medinai are given in Table 5-2. The only fin identified was from an armored catfish. Shrimp and crabs were also eaten.


Serrasalmus rhombeus (Linnaeus) 1766

Serrasalmus rhombeus was uncommon in flooded savanna of the Caflo Caicara

study area, although on several occasions adults were taken in large numbers by hook and line at night in Carlo Maporal. Juvenile Serrasalmus rhombeus have a somewhat elongate body and sharp snout (Fig. 5-2). They resemble S. irritans in body form, but are slightly more robust. Adults have heavy rhomboidal bodies. The body and fins of large individuals, some well over 300 mm SL, are black or blue-black, and the iris is often deep red. I examined the stomach contents of 51 S. rhombeus from the Caio Caicara area (Table 5-5 and Fig. 5-3).











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Juvenile S. rhombeus in size classes iH-IV specialized on fish fins. Aquatic insects, mostly plecopterans, were packed in the guts of several specimens from Carlo Guaritico. The ten largest S. rhombeus (Group V) had taken almost equal volumes of whole small fish, chunks of fish flesh, and fish fins. Fishes identified from the stomachs of larger S. rhombeus are given in Table 5- 2. Three large S. rhombeus collected at night in Calo Maporal contained entire or partial individuals of small 20-30 mm SL doradid catfishes. One individual had eaten a small adult frog.


Serrasalmus elongatus Kner 1860

Serrasalmus elongatus was rare to uncommon in my samples in the study area. It is a pikelike piranha (Fig. 5-2), having the most elongate body, relative to body depth, of all piranhas. I examined 42 individuals, including a few from the small size class (Group II) from other locations in the Apure River drainage (Table 5-6 and Fig. 5-3). Stomachs of three small juveniles (20-39 mm SL) were packed with fins of other small fishes, and one also contained a nematode (possibly a parasite). Stomachs of large specimens contained fish fins and many scales. In addition, small whole fish and chunks of fish flesh were taken by the largest S. elongatus.


Serrasalmus altuvei Ramirez 1965

Serrasalmus altuvei was rare in the Caflo Caicara area, and was found in both streams and floodplain pools. It is a medium-sized piranha; maximum length in my samples was less than 200 mm SL, with a deep narrow body and a slender pointed snout (Fig. 5-2). It has a silver body and a broad, black terminal band on its unpaired fins, none of my specimens from the Apure drainage had any red on the body. I examined the stomachs of ten of 17 individuals collected in Caflo Maporal and the flooded savanna











86






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(Table 5-7 and Fig. 5-3). Fish fins, scales, flesh and small whole fish were found in the two size classes (il and IV) represented in our samples.


Pristobvcon striolatus (Steindachner) 1908
Pristobrycon striolatus was rare in the Cario Caicara study area, and was collected only on several occasions from Cailo Maporal. It is a medium-sized species (Fig. 5-2), less than 200 mm SL; the largest specimen taken from the Calo Caicara region was 156 mm. Adults sometimes had a red-orange chest and occasionally a pattern of orange vertical bars along the sides. Pristobrycon striolatus has a rather blunt snout, but smaller and weaker jaws and jaw musculature than Pygocentrus caribe. The body is deep and strongly compressed. Small juveniles are similar to young Serrasalmus rhombeus but are slightly stouter, lack ectopterygoid teeth, and have little if any side spotting. The largest individual collected in the study area was 159 mm SL. I examined the stomach contents of 16 of the 38 specimens collected. Food items by size class are given in Table 5-8 and Figure 5-3. Specimens in Group II fed mostly on fish fins as did the one Group III specimen examined. Three adults from Group IV contained fish flesh, a few scales, shrimp fragments, an adult aquatic beetle, an aquatic hemipteran and unidentified insect fragments.


Catoprion mento (Cuvier) 1819

Catoprion mento was common in many of the streams and savanna pools. It is a small, deep-bodied species (Fig. 5-2) that is closely related to piranhas. Although maximum size is around 120 mm SL, in the Apure drainage most specimens sampled were under 80 mm SL, and none was greater than 100 nm. The teeth of C. mento are somewhat everted and its long lower jaw swings open to more than 180 degrees, making it well suited for scraping scales off other fish. The stomachs of all 104 specimens examined contained fish scales (ranging up to 23 mm in diameter) (Table 5-9 and Fig. 5-3). Plant material, primarily comprising vascular debris and root wads, and occasionally filamentous




Full Text
96
O
r
25
-r~
50
~T~
75
r
L.
0
25 50 75
Percent diet similarity
100
1
General
Piscvoros
H
JV 10-19 J_ Aquatic Insects/
PC 20-39 _T Microcrustaceans
PC 40-79 _
SR 80-159
PC 80-159
SEL 80-159
SIR 80-159
SMD 80-159
SA 80-159
PST 80-159
PC >160
SA 40-79
SR >160 _J
SR 20-39
SR 40-79
SIR 40-79
SMD 40-79
SMD 20-39
PST 20-39
SEL 20-39
PST 40-79
- Fin Eaters
SIR 20-39
SEL 40-79
SEL >160 J
CM 20-39
CM 40-79
CM 80-159 J
- Scale Eaters
100
Fig. 5-5. Dendrogram from cluster analysis depicting similarities among diets of piranhas
and related species (by size class) from the Cao Caicara area of the low Llanos,
Apure River drainage, Orinoco River basin, Venezuela. Similarity values are
from Table 5-11, dendrogram UPGMA-generated using overlap index of
Schoener (1970). Size ranges are in mm Standard Length. Species
abbreviations are as follows: PC = Pygocentrus caribe; PST = Pristobrycon
striolatus; SMD = Serrasalmus medinai; SR = Serrasalmus rhombeus, SA =
Serrasalmus altuvei, SIR = Serrasalmus irritaos, SEL = Serrasalmus elongatus,
and CM = Catoprion mento\ JV = small juveniles.


185
MCNG 9101 (2-1). 1981: MCNG 11015 (2-2); UF 31858 (1-0); UF 77722 (1-0). 1984:
MCNG 11361 (8-4); MCNG 11350 (1-1) 1988: MCNG 21242 (2-2). Cao Caicara:
1990: MCNG 23382 (3-3). Other.-1979: MCNG 1193 (1-1); MCNG 9683 (2-2); MCNG
12588 (1-1).
Capanaparo River drainage: 1989: MCNG 20229 (1-0).
Serrasalmus cf. eigenmanni
Llanos
Cinaruco River drainage: 1989: MCNG 21380 (1-1); MCNG 20156 (2 2).
Upper Orinoco
Ventuari River drainage: 1989: MCNG 22116 (1-1).
Ocamo River drainage: 1990: MCNG 22415 (1-1); MCNG 22410 (1-1); MCNG
22260 (8-8); MCNG 22287 (1-1); MCNG 22289 (1-1); MCNG 22290 (2-2); MCNG
22250 (3-3); MCNG 22406 (4-4).
Matacuni River drainage: 1990: MCNG 22125 (5-5); MCNG 22129 (9 9).
Orinoco main stem: 1990: MCNG 21850 (1-1).
Mavaca River drainage: 1991: MCNG 25409 (4-4); MCNG 25361 (2-2); MCNG
25364 (4-4); MCNG 25337 (3-3).
Other
Caura River drainage: 1989: MCNG 21047 (3-3); ;MCNG 21593 (3-3); MCNG
21929 (6-6).
Serrasalmus irritans
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 7685 (4-4); MCNG
8409 (1-1); MCNG 9443 (2-2). 1980: MCNG 4439 (1-1); MCNG 5901 (13-13). 1981:


50
(=1 ;= 1
%Va =( jFil Yji ) x 100,
/I /I
where F/ is the fullness points for stomachs whose dominant food item is F\ Ti is total
fullness points for all stomachs; and n is the number of stomachs examined of a species or
size class.
I attempted to identify food items to the lowest taxonomic level, whenever possible.
For comparing piranha diets, I recognized eleven general food categories: (1) masticated
seeds crushed or fragmented seeds together with the hard parts (mainly endocarp)that
surround the seed; (2) other plant material mostly leaves, root fragments, fleshy fruits,
and flowers; (3) decapods crabs and shrimp; (4) microcrustaceans copepods,
cladocerans, ostracods and conchostracans; (5) aquatic insects various families, including
larvae and adults; (6) other invertebrates mostly arthropods, including terrestrial forms,
but also aquatic nematodes and snails; (7) small whole fish at least two-thirds of total
body; (8) fish flesh pieces of flesh bitten from fish; (9) fish fins fins not taken with or
attached to pieces of flesh; (10) fish scales scales not taken with or attached to flesh; and
(11) other detritus, sand, nonfish vertebrates, and unidentifiable items.
I compared and contrasted diets within and among the different species and size
groups by calculating estimates of diet breadth and overlap based on percent food volume
or adjusted volume. Because I did not quantitatively measure the relative availability of
food resources in the field, I chose two widely used indices of breadth and overlap that do
not take into account the relative abundance of the various food items in the natural
environment.
Diet breadth, or width, measures the diversity and evenness of resource use. Diet
breadth was computed for each species' size class using Levins' index of niche width
(Levins 1968, Krebs 1989):


41
Fig. 3-3. Map of 1988-1991 sampling sites in upper Orinoco, Federal Territory of
Amazonas, Venezuela Solid circles represent localities sampled by the
author; solid squares represent areas collected by others (specimens from all
sites deposited at MCNG and examined by the author). Circles and squares
may represent more than one sampling site.


142
SERRASALMUS MANUELI
S.L. (mm)
40-79
80-159
>160
LLANOS
UPPER ORINOCO
o = 5 (3.90)
n = 22 (1.96)
n = 18(1.83)
n = 18 (1.45)
n = 42 (1.99)
Masticated Seeds
Other Plant Material
Decapoda
Aquatic Insects
Other Invertebrates
Small Whole Fish
Fish Flesh
Fish Fins
Fish Scales
Other


156
geological history, and the physical and biological characteristics of the individual
drainages. A combination of all these factors has probably helped to shape the distribution
patterns observed for Orinoco piranhas.
Several recent studies in different parts of the Orinoco River basin have examined
patterns of fish distribution and species composition. Based on long-term collecting, much
of it in the Apure River drainage. Taphorn (1990) felt that altitude (lowland versus
montane) and water type (i.e., clear and black versus white) were the two basic
environmental parameters governing fish species distribution. He found that many species
(47 of 103 characiform fishes) living in black waters seemed to be restricted to that type of
habitat, whereas relatively few species were limited to just white waters (15 of 77
characiform species). In a study of fish communities from 20 floodplain lakes in the lower
Orinoco, Rodriguez and Lewis (1990) found that differences in species composition
between lakes might be best explained in terms of variation in small-scale factors (e.g.,
water type, lake morphology, and vegetation), and that apparent differences among regions
might be averaged out and disappear if many sites (i.e., habitats) from each region were
included in a comparison. Chemoff et al. (1991) rejected both ecological segregation and
the possibility of sampling artifact and concluded that historical events, or vicariance, better
explained the seemingly disjunct distribution patterns seen with some Orinoco fish species.
I examined and compared piranha distribution patterns among regions and
drainages to reveal any associations existing between species composition and habitat. My
interest in habitat-dependent piranha distribution revolved around their relationship to
piranha trophic ecology. Although piranhas exhibit a fair amount of flexibility in what they
eat, my study documents the fact that Orinoco piranhas, in terms of adult diets,
nevertheless fall into two general categories: species that are largely carnivorous, and
others that axe primarily herbivorous (Table. 8-1). Given this apparent dichotomy in
feeding preferences, a close association between piranha distribution patterns and habitat
type might be predicted. Herbivorous species should.be much more common in the


200
Ferreira, E. J. G. 1984a. A ictiofauna da represa hidreltrica de Curu-Una, Santarm,
Par. I Lista e distribuipo das espcies. Amazoniana 8(3):351-363.
Ferreira, E. J. G. 1984b. A ictiofauna da represa hidreltrica de Curu-Una, Santarm,
Par. II Alimenta§ao e hbitos alimentares das principis espcies. Amazoniana
9(1):1-16.
Fink, W. L. 1988. Evolutionary biology of piranhas. Pages 13-14 in G. H. Dalrymple,
W. F. Loftus, and F. S. Bernardino, Jr., editors. Wildlife in the Everglades and
Latin American wetlands Proceedings of the First Everglades National Park
Symposium, Florida international University, Miami.
Fittkau, E. J., U. Irmler, W. J. Junk, F. Reiss, and G W. Schmidt. 1975. Productivity,
biomass, and population dynamics in Amazonian water bodies. Pages 289-311 in
F. B. Golley and E. Medina, editors. Tropical ecological systems, trends in
terrestrial and aquatic research. Springer, New York.
Fox, L. R., and P. A. Morrow. 1981. Specialization: species property or local
phenomenon? Science 211:887-893.
Frailey, C. D., E. L. Lavina, A. Raney, J. P. de Souza-Filho. 1988. A proposed
Pleistocene/Holocene lake in the Amazon basin and its significance to Amazonian
geology and biogeography. Acta Amaznica 18:119-143.
Futuyma, D. J. 1986. Evolutionary biology. Sinauer Associates. Sunderland,
Massachusetts, 600 pp.
Gauch, H. G. 1982. Multivariate analysis in community ecology. Cambridge University
Press, Cambridge, 298 pp.
Gry, J. 1972. Poissons characoides de Guyanes II. Famiile des Serrasalmidae.
Zoologische Verhandelingen Leiden 122:134-248.
Gilbert, C. R. 1980. Zoogeographic factors in relation to biological monitoring of fish.
Pages 309-355 in C. H. Holcutt and J. R. Stauffer, Jr., editors. Biological
monitoring in fish. D. C. Heath and Company, Lexington, Massachusetts.
Gottsberger, G. 1978. Seed dispersal by fish in the inundated regions of Humait,
Amazonia. Biotropica 10:170-183.
Goulding, M. 1980. The fishes and the forest: explorations in Amazonian natural history.
University of California Press, Los Angeles, 280 pp.
Goulding, M. 1983. The role of fishes in seed dispersal and plant distribution in
Amazonian floodplain ecosystems. Sonderbd. Naturwiss. Ver. Hamburg 7:271-
283.
Goulding, M., M. L. Carvalho, and E. G. Ferreira. 1988. Rio Negro, rich life in poor
water. SPB Academic Publishing, The Hague, The Netherlands, 200 pp.
Greene, H. W., and F. M. Jaksic. 1983. Food-niche relationships among sympatric
predators: effects of level of prey identification. Oikos 40:151-154.


192
Table B-2. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and 5. rhombeus (n =
70).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
574.649
574.649
0.288
0.5924
SL
1
1923573.822
1923573.822
964.479
0.0001
Species x SL
1
6466.875
6466.875
3.242
0.0741*
Residual
126
251296.649
1994.418
^Conclude that slopes of regression lines are not different at 0.05 level of significance,
therefore eliminate interaction effect (see Table B-3) to see if y-intercept is the same..
Table B-3. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and S. rhombeus (n =
70) eliminating interactive effect (i.e., adjusting for differences in SL).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
68775.973
68775.973
33.886*
0.0001*
SL
1
1922891.270
1922891.270
947.408
0.0001
Residual
127
257763.523
2029.634
* Adjusting for differences in SL, reject null hypothesis and conclude that y-intercepts are
different, therefore the IL of the two species differ significantly (F = 33.89, P = 0.0001).


80
Table 5-2. List of vertebrate prey taxa identified from the stomach contents of the four
most common piranhas from the Cao Caicara area, Apure River drainage, in the low
Llanos of Venezuela.
Species
Vertebrate Prey
(frequency of occurrence)
Pygocentrus caribe
Fish (whole or flesh): Characidae Aphyocharax erythrurus (6), Astyanax
bimaculatus (1), Astyanax sp. (3), Charax sp. (2), Cheirodon
pulcher (1), Ctenobrycon spilurus (22), Gymnocorymbus thayeri
(15), Hemigrammus marginatus (5), Hemigrammus sp. (5),
Moenkhausia dichroura (2), Odontostilbe pulcher (7), Poptella
orbicularis (6), Pygocentrus caribe (6), and Roeboides qffinis (1),
Roeboides dayi (8), Roeboides sp. (3), Serrasalmus eigenmanni (1),
Serrasalmus sp. (1), Triportheus sp. (1); Curimatidae Curimata
metae (10), curimatids (14); Lebiasinidae Pyrrhulina cf. lugubris (2);
characoid (8); Cichlidae Microgeophagus ramirezi (2), Gyranotidae -
Gymnotus carapo 1); Stemopygidae Sternopygus macrurus (1), and
Eigenmannia spp. (10); Hypopomidae Hypopomus sp. (1);
Auchenipteridae Entomocorus gameroi (1) and Parauchenipterus
galeatus (1); Pimelodidae Pimelodella sp.(l); Callichthyidae -
Hoplosternum ¡inrale (1); Rivuiidae (1). Fins of Hypophthalmidae -
Hypophthalmus cf. edentatus (1); Characidae Triportheus sp. (1).
Reptiles: Flesh of Caiman crocodilus < 1); flesh of lizard, probably
Ameiva (1).
Amphibians: Small adult leptodactyiid frog.
Birds: Feathers and flesh of white-faced whistling duck (Dendrocygna
viduata) (3).
Serrasalmus irritans
Fish (whole or flesh): Characidae Ctenobrycon spilurus (1),
Odontostilbe pulcher (2), Hemigrammus sp.(l), small juvenile
Pygocentrus caribe (1); Curimatidae Curimata metae (1), curimad
(1); characoid (4); gymnotoid (1); Cichlidae Micro geophagus
ramirezi (1), cichlid (1). Fins of adult Pygocentrus caribe (2).
Serrasalmus medinai
Fish (whole or flesh): Characidae Aphyocharax erythrurus (1),
Hemigrammus marginatus (2), Hemigrammus sp. (1), and
Odontostilbe pulcher (2), characid (2); Curimatidae Curimata metae
(2), curimatid (1); Cichlidae Microgeophagus ramirezi (1);
gymnotoid (1); catifish (1); Fins from Loricariidae (1).
Serrasalmus rhombeus
Fish (whole or flesh): Characidae Astyanax bimaculatus and Charax
sp.(l), characid (1); characoid (1); Doradidae Agamyxis'l (3);
unidentified catfish (1); Fins of Characidae Pygocentrus caribe (/);
Erythrinidae? (1).
Amphibians: Small adult frog (1).


Table 6-8continued.
Species and
Size Range (SL, mm)
SA
80-159
SA
>160
MYA
80-159
MYA
>160
MYS
80-159
MYS
>160
MYT
80-159
MYT
>160
CM
80-159
SM
10-19
SM
20-39
PST
10-19
PST
20-39
PYP
10-19
PYP
20-39
SR 40-79
27
20
0
0
0
0
5.3
0.2
0
0
20
20
20
0
0
SR 80-159
47.45
44.65
5.15
5.05
5.6
6.45
18.95
9.35
14.3
0.7
31
8.95
32.05
0.7
2.9
SR >160
14.15
8.65
1.95
1.85
4.4
8.05
8.65
5.95
4.8
0
3.8
3.75
7.1
0
2.3
SM 40-79
36.14
30.24
1.54
1.46
2.31
2.34
6.84
2.64
1.49
0
28.7
8.3
29.06
0
2.1
SM 80-159
11.26
16.55
12.65
13.15
13.11
7.05
17.15
13.55
10.31
0.01
4.1
4.06
4.46
0
2.3
SM >160
9.15
14.25
24.75
17.35
16.2
19.85
16.85
26.05
10.7
0
1.4
1.45
1.85
0
2.4
SEG 40-79
63.1
75
0
0
0
0
5.3
0
0
0
100
8.3
55.3
0
0
SEG 80-159
19
12.1
11.9
3.1
1.75
49.2
9.8
55.7
4.85
0.4
7.6
8.3
22.1
0.4
1.9
SEG >160
18.15
11.15
11.05
2.25
0
47.25
11.15
54.55
9.5
0
1.6
1.4
1.4
0
0
PC 80-159
18.15
10.95
0.1
0
0
0.95
7.95
3.05
2.6
0
8.3
8.3
8.7
0
0.5
PC >160
23.35
22.55
9.45
9.35
11.9
6.25
25.55
14.15
24.8
0
0.7
0.7
0.7
0
1.6
PST 80-159
14
12.35
16.55
7.85
6.7
53.65
10.95
57.15
5.6
0
6.7
6.7
7.1
0
2.3
PST ¡>160
0.5
5
15.5
6.7
4.55
51.7
5
55.4
4.95
0
0
0
0
0
1.6
PSP >160
2
2.2
11.4
2.6
0.45
48.7
2.2
52.8
2.15
0
0
0
0.4
0
1.0
PYP >160
1.8
1.6
11
2.2
0
48.3
1.6
52.2
1.6
0
0
0
0.4
0
0.6


178
the conclusions drawn here fare when they are re-evaluated in light of a well understood
phytogeny of the piranhas.


193
Table B-4. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and 5. cf. eigenmanni
(n = 32).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
6822.825
6822.825
3.024
0.0856
SL
1
547308.446
547308.446
242.538
0.0001
Species x SL
1
48373.729
48373.729
21.437*
0.0001*
Residual
88
198579.446
2256.585
^Conclude that slopes of regression lines are different, and that the IL/SL ratio of S. cf.
eigenmanni is significantly greater.(F = 21.44, P = 0.0001).
Table B-5. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus rhombeus (n = 70) and S. cf. eigenmanni
(n = 32).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
4463.807
4463.807
1.886
0.1727
SL
1
506164.993
506164.993
213.908
0.0001
Species x SL
1
61742.334
61742.334
26.093*
0.0001*
Residual
98
231895.339
2366.279
^Conclude that slopes of regression lines are different, and that the IL/SL ratio of S. cf.
eigenmanni is significantly greater.(F = 26.09, P = 0.0001).


130
"O
co
03
b
3 ~\
2-
1 ~
0
ill
s -y
pi
h4
i X
I:: -
:y*y
?:
1P
|p
rip
i
i
i
Si 7
lp
i
lp
i
10-19 mm

20-39 mm

40-79 mm
z
80-159 mm

>160 mm
S. rhombeus S. maiueli S. eigenmanni S. atuvei P. caribe P. strioiaus Prist, sp. P. denticulatus
Species
Fig. 6-6. Diet breadths estimated for eight piranha species, by size class, from the upper
Orinoco River basin, Venezuela. Diet breadth calculated using formula of
Levins (1968). Most species not represented in all size classes. Size ranges are
standard length (mm).


Table 1-1. Summary of principal field studies investigating piranha feeding and diets in order of publication date. All studies based on
analysis of stomach contents unless otherwise indicated. Most measured size as standard length in mm, if not, size given as total length
(TL) or weight in grams (g). Scientific names are as used in original literature unless marked with asterisk (*) (also see nomenclatural
changes discussed in Chapter 3).
Basin
Site or
Study Period and
Species
No. Examined
Comments
Source
(State, Country)
Habitat
Duration
(Size range)
1. Jaguaribe
(Cear, Brazil)
Lima Campos
Reservoir
1944, May to
October
1) Serrasalmo immaculatus
(^Serrasalmus rhombeus)
n= 138
(wt: 10-215 g)
Diet consisted mainly of fish
remains
Menezes and
Menezes (1946)
2. Jaguaribe
(Cear, Brazil)
Lima Campos
Reservoir
12-month study,
1952-1953
1) Serrasalmus rhombeus
n = 2,222
(100-290 TL)
Fed mainly on shrimp and fish
Braga (1954)
3. Essequibo
and Amazon
(Guyana)
Rupununi
Savanna, savanna
pools
Intermittent 1957,
1958, and 1961
(~2 months total)
1) Serrasalmus nattereri,
2) S. rhombeus
3) S. gymnogenys
4) Pygopristis denticulatus
Number examined
not given
Reduced feeding found during dry
season
Lowe-
McConnell
(1964)
4. Paran
(Argentina)
Middle Paran
rivers, lagoons (?)
Intermittent
1962 to 1966
1) Serrasalmus spilopleura
2) S. nattered
n = 104 (3-657 g)
n = 21 (10-200 g)
Diet of mostly fish
Bonetto et al.
(1967)
5. Amazon
(Par, Brazil)
Three sites: Lago
Jacup, no data on
other two
1967 (?)
1) Serrasalmus elongatus
n = 7 (89-152)
All contained fins, some scales;
fins major item in all but two
Roberts (1970)
6. -Jaguaribe
(Cear, Brazil)
Three reservoirs:
Roque de Macdo,
Cruzeiro do Sul,
Assis Machado
Intermittent 1970-
1972: Nov. 1970,
May 1972, other
date?
1) Serrasalmus nattered
n = 500
(125-370 TL)
Fed mainly on fish (small
characins)
Braga (1975)
7. Napo-Amazon
(Ecuador)
Rio Aguarico
floodplain lakes,
side channels
Intermittent
1967 and 1968
(~3 1/2 months)
1) Serrasalmus nattered
2) S. marginatus
n = 6 (30-321)
n = 4 (45-224)
1) fish remains and insects
2) fish remains
Saul (1975)


TABLE OF CONTENTS
page
ACKNOWLEDGEMENTS ii
LIST OF TABLES vii
LIST OF FIGURES ix
ABSTRACT xii
CHAPTERS
1 INTRODUCTION 1
Introduction to Piranhas 1
Purpose of Present Study 3
Literature Review 7
Organization of Dissertation 16
2 ENVIRONMENTAL SETTING 18
The Orinoco River Basin 18
History of the Basin 22
The Low Llanos 24
The Upper Orinoco 28
Savannas and Forests During the Quaternary 30
Present Climate and Seasonality 32
3 METHODS 35
Field Sampling 35
Field Site Locations and Sampling Periods 37
Evaluation of Habitats 42
Identification and Nomenclature of Piranhas 43
Faunal Comparisons 47
Analysis of Diets 49
Nutrient Content Analysis of Food Items 53
Intestine Length 54
Field and Aquarium Observations 55
Statistical Analyses 55
4 COMPOSITION OF PIRANHA ASSEMBLAGES 57
v


64
Table 4-3. Number of shared piranha species and Coefficient of Biogeographic
Resemblance (CBR) (in parenthesis) among nine sampled drainages in the Orinoco River
basin. CBR values range from 0 (no species in common) to 1 (complete similarity in
species composition).
River Drainages
Low Llanos
Upper Orinoco
Apu Cap
Cin
Sip
Ata
Ven
Mat
Oca
Mav
Number of
piranha species
8 7
6
1
4
6
3
5
5
Apure
6
4
0
1
4
2
4
4
(0.80)
(0.57)
(0)
(0.33)
(0.57)
(0.36)
(0.62)
(0.62)
Capanaparo
5
1
2
5
1
3
3
(0.77)
(0.25)
(0.55)
(0.77)
(0.20)
(0.50)
(0.50)
Cinaruco
1
2
5
2
3
4
(0.29)
(0.60)
(0.83)
(0.44)
(0.55)
(0.73)
Sipapo
1
1
0
0
0
(0.40)
(0.29)
(0)
(0)
(0)
Atabapo
2
0
0
1
(0.60)
(0)
(0.22)
(0.44)
Ventuari
2
4
4
(0.44)
(0.73)
(0.73)
Matacuni
3
3
(0.75)
(0.75)
Ocamo
4
(0.80)
Mavaca


UPPER ORINOCO
LLANOS
S.L. (mm)
SERRASALMUS PRISTOBRYCON PYGOPRISTIS
MANUELI STRIOLATUS DENTICULATUS
PYGOCENTRUS
CARIBE
n = 114(2.11)

Other Plant Material
I
Other Invertebrates
Microcrustaceans
Fish Fins
\ \ V
/ / /
\ N \
Aquatic Insects
Other


29
Fig. 2-4. Approximate distribution of lowland forests (shaded area) in Federal Amazon
Territory of Venezuela.


Colossoma
A
B
Fig. 1-
Piaractus
Mylossoma
Myleus
Mylesinus
Utiarichthys
Acnodon
Metynnis
Catoprion
Pygopristis
Pygocentrus
Pristobrycon
Serrasalmus
- PIRANHAS
1. Hypothesized phylogenetic relationships among genera of the subfamily
Serrasalminae as proposed by Machado-Allison (redrawn from Machado-
Allison 1985).


Fig. 6-11. Scatter diagram showing relationship between intestine length (IL) and standard
length (SL) for the three most common piranhas in samples from the upper
Orinoco River basin of Venezuela. Regression lines are as follows: S. manueli
IL = -64.09 + 1.86SL (r2 = 0.908, n = 60), S. rhombeus IL = -76.07 +
1.66SL (r2 = 0.857, n = 70), S. cf. eigenmanni EL = -137.88 + 3.44SL (r2 =
0.733, n = 32). Lines fitted by the above linear regression equations, r =
Pearson correlation coefficient. See Appendix B for ANCOVA analyses.
Fig. 6-12. Scatter diagram showing relationship between intestine length (IL) and standard
length (SL) for Serrasalmus manueli comparing upper Orinoco and Llanos
populations. Regression lines are as follows: Upper Orinoco EL = -64.09 +
1.86SL (r2 = 0.908, n = 60), Llanos IL = -94.32 + 2.00SL (r2=0.864, n =
20). Line fitted by the above linear regression equation, r = Pearson
correlation coefficient See Appendix B for ANCOVA analyses.


28
Lewis 1988). During high water, the flooded savanna habitats are important to fish as
breeding and feeding areas. Aquatic vegetation flourishes and emergent and floating plants
may cover large portions of the surface of both permanent and temporary water bodies.
Large mats of water hyacinth [Eichhornia species) are especially abundant in many of the
lagoons, prestamos, and some of the streams. Partially inundated grasses and sedges
commonly grow in the shallows of streams, prestamos, and other standing waters. Other
common aquatic and semi-aquatic plants of the low Llanos include Ludwigia, Benjamania,
and Pontederia. Some common aquatic plants with floating leaves are Salvinia, Lemna,
and Pistia.
The Upper Orinoco
The upper Orinoco drainage is situated in the Federal Territory of Amazonas
(Fig. 2-4) in southern Venezuela, a vast area covering 178,095 km2 (CODESUR 1979).
Main features of the heavily forested landscape are flat alluvial plains, large mountain
valleys, and massive granitic hills [lajas) (CODESUR 1979, Huber and Wurdack 1984).
About 70 percent of the territory is drained by the Orinoco, with the remainder flowing into
the Rio Negro of the Amazon basin (CODESUR 1979). Together with the adjacent state of
Bolivar, this southern section of the country is often referred to collectively as Venezuelan
Guyana because the Precambrian Shield dominates the topography. Little developed and
with few inhabitants, the great majority of intact forests in Venezuela occur in this southern
region. Steyermark (1982) estimated that forests covered 82 percent of the region, or about
146,000 km2. Due to forest clearing, the total coverage is probably slightly less today.
Because forests of the upper Orinoco are continuous with those of the northern Amazon
Basin, the region is part of the largest area of humid forests within the neotropics
(Whitmore and Prance 1987).


184
Cinaruco River drainage: 1987: MCNG 17157 (4-0?); 1989: MCNG 20018 (2-2);
MCNG 20110 (1-1).
Capanaparo River drainage: 1989: MCNG 21885 (4-4); MCNG 17776 (3-3); UF
84183 (1-1).
Upper Orinoco
Venturari River drainage: 1981: MCNG 7874 (2-0);
Atabapo River drainage: 1989 MCNG 21881 (1-1);
Mavaca River drainage: 1991: LN 91-19 (33-9); LN 91-45 (47-15).
Serrasalmus altuvei
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 9147 (1-1). 1981:
MCNG 3619 (4-4). 1984: MCNG 10713 (5-5). 1985: MCNG 12470 (1-0). Cao
Maporal.-1981: MCNG 9356 (1-0); MCNG 11018.(1-0): UF 31859 (2-0). 1983:
MCNG 10075 (2-0). 1988: MCNG 21241 (1-1).
Upper Orinoco
Matacuni River drainage: 1990: MCNG 22126 (3-0); MCNG 22417 (1 1).
Mavaca River drainage: 1991: MCNG 25336 (7-7); MCNG 25410 (1-1).
Serrasalmus elongatus
Llanos
Apure River drainage: UNELLEZ module.-1980: MCNG 5902 (2-1). 1981:
MCNG 2044 (1-1); MCNG 4560 (1-1); MCNG 4736 (1-1). 1984: MCNG 10711 (9-8).
1985: MCNG 11382 (13-13); MCNG 11539 (2-2). 1989: MCNG 23139 (1-1); MCNG
23156 (1-1); MCNG 23179 (1-1); MCNG 23164 (7-7); MCNG 23386 (1-1); MCNG
23169 (9-9). 1990: MCNG 23384 (2-2). Cao Maporal.- 1980: MCNG 6067 (3-2);


Fig. 6-9. Diets by size class (>40 mm SL) of Serrasalmus manueli comparing Llanos
(Cinaruco River drainage) and upper Orinoco populations. Size of segments
represents percentage of volume of each prey type; n = number of stomachs
examined; numbers in parentheses represent diet breadth using formula of Levins
(1968).


CHAPTERS page
5 TROPHIC ECOLOGY OF SAVANNA PIRANHAS: THE APURE
DRAINAGE 71
Study Area 71
Species Accounts 75
Comparison of Diets 91
6 TROPHIC ECOLOGY OF PIRANHAS FROM THE UPPER
ORINOCO 97
Species Accounts 100
Summary of Upper Orinoco Trophic Patterns 123
Comparison with Savanna Populatons 131
Ecomorphological Correlates: Intestine Length and Diet 143
7 NUTRIENT VALUES OF PIRANHA PREY 148
Animal Matter 148
Plant Matter 153
8 DISCUSSION AND CONCLUSIONS 155
Composition of Piranha Assemblages 155
Trophic Patterns 163
Ecomorphological Correlates 175
A Phylogenetic Perspective 177
APPENDICES
A MATERIAL EXAMINED 181
B DATA ANALYSIS 191
LITERATURE CITED 198
BIOGRAPHICAL SKETCH 209
vi


68
A summary of species occurrence by habitat type is given in Table 4-4. Most
species were found in a variety of environmental conditions, but relative abundances
differed among sites. Serrasalmus rhombeus and S. manueli were frequently taken in
riverine habitats; other piranhas were more common in floodplain habitats (e.g., lagoons or
old meanders) and in caos with slow currents. In those cases where piranhas were found
in large streams or rivers, they commonly congregated in adjoining slackwaters near the
interface between fast-flowing and still waters, for example near the mouths of sloughs or
deep caos.
Most piranhas were found in two or all of the three major water types (Table 4-4),
but greatest numbers occurred in whitewater habitats. Three species (i.e., Serrasalmus
manueli, Pygopristis denticulatus, and Pristobrycon sp.) were usually associated with low-
pH, blackwater habitats Nevertheless, most species seem to tolerate a wide range of
temperatures and pH, as shown by wild-caught juveniles of both S. manueli and P.
denticulatus that have survived nine months (to date) in aquarium water with pH as high as
8.5. Water temperatures at sample sites ranged from 24.5 to 38 C, and pH 4.5 to 7.2;
water transparency ranged from very turbid (10 cm as measured with a Secchi disk), to
very clear (>3 m).
Where piranhas occur, two or more species are commonly taken together. In the
low Llanos, juveniles and subadults of as many as five species (i.e., Pygocentrus caribe,
Serrasalmus altuvei, S. irritans, S. medinai, and S. elongatus) were occasionally taken in
single seine hauls in floodplain pools of the Apure drainage. In the upper Orinoco, adults
of as many as four species of piranha (e.g., Serrasalmus rhombeus, S. cf. eigenmanni,
Pygocentrus caribe, and Pristobrycon striolatus) were caught together in gill nets set during
evening twilight. Sites of highest species richness were characterized by a large amount of
instream cover or other protection, including mats of aquatic vegetation, adjacent flooded
forest, or deep water. Small juvenile piranhas (<40 mm SL) were only found in


different species. My data indicated allometric changes in intestine length. In order to
reduce variation and make comparisons more valid, only specimens > 80 mm SL were
used in correlation analysis.
55
Field and Aquarium Observations
I made qualitative and quantitative observations on the feeding behaviors of wild-
caught juvenile and subadult piranhas maintained live in aquaria or large outdoor concrete
tanks (L. Nico, unpublished data). Species represented from low Llanos populations were
Pygocentrus caribe, Serrasalmus elongatus, S. irritans, S. medinai, S. rhombeus, and
Pristobrycon striolatus; those from upper Orinoco sites were Pygopristis denticulatus and
Serrasalmus manueli. In the field, most observations of piranha feeding behavior were
done from shore or from boats while fishing, these qualitative observations totaled over
one hundred hours. I also made brief underwater observations on the feeding behavior of
several species totaling about five hours. Underwater observations were made using mask
and snorkel in Clearwater and blackwater streams in the states of Bolivar, Guarico, and
Monagas. Species observed were juveniles or subadults of Serrasalmus irritans, S.
medinai, S. rhombeus, and Pygocentrus caribe.
Statistical Analyses
All nonparametric tests were run using the computer software program Basic
Statistical Subroutines by DYNACOMP (1983) following Siegel (1956) and Siegel and
Castellan (1988). Statistical tests of ANCOVA were done using the SuperANOVA
program on a Macintosh SE/30 computer. For cluster analysis, I used the computer
program NTSYS-pc (Numerical Taxonomy and Multivariate Analysis System) version 1.5
by Rohlf (1988). Cluster analysis has been shown to be a useful and reliable multivariate


Fig. 6-8. Comparison of the proportion of plant material in the diets of carnivorous and
herbivorous piranha species (> 80 mm SL) from the low Llanos to those from
upper Orinoco River drainages in terms of percent adjusted volume (%Va),
percent dominance (%D), and percent frequency of occurrence (%0).
Carnivorous species abbreviations are: Pc = Pygocentrus caribe; Sa =
Serrasalmus altuvev. Sel = S. elongatus; Sir = S. irritans; Sm = S. manueli: Smd
= S. medinai; and Sr = S. rhombeus. Herbivorous species abbreviations are:
Pst = Pristobrycon striolatus; Psp = Pristobrycon sp.; Pyp = Pygopristis
denticulatus; and Seg = Serrasalmus cf. eigenmanni. Psp was found only in the
upper Orinoco; Sel, Sir, and Smd were found only in the Llanos.


Table 6-4. Food items of Serrasalmus cf. eigenmanni from the upper Orinoco River basin by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %V = percent volume. N =4 8.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
m(40-79)
2
0
%D
%v
%0
IV(80-159)
40
2
%D
%V
%o
V (>160)
6
0
%D
%V
Masticated seeds
-
-
-
78.9
63.2
74.4
83.3
83.3
76.4
Plant material
-
-
-
5.3
-
0.9
-
-
-
Aquatic insects
-
-
-
2.6
-
0.4
-
-
-
Other invertebrates
-
-
-
7.9
2.6
1.1
-
-
-
Fish flesh
-
-
-
15.8
13.2
11.6
33.3
-
12.4
Fish fins
100.0
100.0
100.0
39.5
18.4
7.6
16.7
-
1.6
Fish scales
-
-
-
26.3
-
3.6
33.3
16.7
9.5
Other
-
-
-
2.6
-
0.4
-
-
-


Fig. 2-3. Approximate distribution of open savanna (low Llanos) in Venezuelan state of Apure, Orinoco River basin.
to
ON


163
Based on the fossil record and the proposed phylogenetic relationships among
serrasalmine fishes (Lundberg et al. 1986; Fig. 1-1), no less than a proto-piranha existed
before the start of the Pleistocene. If this "first piranha" entered the Quaternary unchanged,
subsequent radiation might have been in the form of adaptive responses to the dramatic
changes wrought by glacial events. In this scenario, herbivorous piranhas would have
evolved in forested areas and perhaps certain carnivorous forms in savanna regions.
However, given evolutionary stasis (see Lundberg et al. 1986) and the possibility that
piranhas, as we now know them, had already evolved well before the climatic events of the
Pleistocene, piranha lifestyles would still have been dramatically altered by the climatic
cycles, and these fishes would have had to respond behaviorally, if not morphologically, to
large cyclical changes in food resources.
Trophic Patterns
Trophic Groupings
Based mostly on stomach content analysis, I identified six general trophic groups
among the serrasalmine fishes and size classes studied; four of these six feeding guilds
included piranhas. In order to compare the Low Llanos and the upper Orinoco groupings,
I attempt a general assessment in the following pages. Information on minor food items
not included in these discussions can be found in species account sections presented earlier.
1) Piscivores. The adults of at least seven Orinoco piranhas (Serrasalmus and
Pygocentrus; Table 8-1) are largely carnivorous, feeding mainly on fishes by either biting
out pieces of flesh or taking small fish whole. In addition to actively preying on other
fishes, piscivorous piranhas are opportunistic and scavenge on dead or dying fish (as well
as other vertebrates) (see Sazima and Guimaraes 1987, Nico and Taphom 1988).
Goulding (1980) reported that the dominant Amazonian piranha, S. rhombeus, preyed
most heavily on common fishes of about its own size by removing chunks of flesh. I


34
Month
Fig. 2-5. Monthly rainfall recorded at representative sites in Orinoco River basin,
Venezuela. (1) Upper Orinoco: monthly average 1971-1977 from Santa Maria
de Los Guaicas, mouth of Ocamo River, Federal Territory of Amazonas, and (2)
Low Llanos: for year 1972 from Cao Caicara area, Apure River drainage,
Apure State. Sources: CODESUR (1979) and Taphom and Lilyestrom (1984),
respectively.


23
An ancient Orinoco River is thought to have flowed to the northwest, emptying into
the Caribbean before the Miocene uplift of the Andes near or through the present day
Maracaibo Lake Basin. In addition to geologic evidence, this idea of a northward flow has
received added support from comparisons of fossil and living fishes found in northern
Colombia and Venezuela (Lundberg et al. 1986, 1988). According to the proposed
scenario, the river slowly shifted to the east some time between the Late Cretaceous and
early Oligocene, finally assuming its present course by the Oligocene epoch, about 30
million years ago (Lundberg et al. 1988). However, it is still uncertain how the river's
movements affected or coincided with the formation and eventual draining of the sea that
covered the interior lowlands at about the same time periods (Taphom 1990).
The Orinoco and Amazon rivers are connected today by the Casiquiare canal, a
natural waterway flowing southward from the upper Orinoco into the upper Rio Negro,
permitting interchange of fishes between the two basins. However, the Orinoco and
Amazon basins may have had an even closer association in the past, partly based on studies
in western Brazil. The Amazon once flowed westward to the Pacific before the major rise
of the Andes in the Miocene (Goulding 1980, Putzer 1984). After the Andes uplift blocked
its westward flow, a huge lake, or more likely, a series of large lakes and wetlands, were
formed covering much of the lowland areas in the basin (Frailey et al. 1988). Eastward
flow was prevented at the time by higher elevations joining the Brazilian and Guyana
shields. Before the Amazon had completely carved its way east between the two shields,
the proposed Pleistocene/Holocene lake or lakes had their prime outlet north into the
Orinoco. Indeed, tectonic events may have resulted in shifting the primary outlet several
times between the north and east (Frailey et al. 1988).


ACKNOWLEDGEMENTS
I owe a debt of gratitude to many friends and colleagues for their help during the
field work, data analysis, and manuscript preparation. During my development as a
tropical biologist, I greatly benefited from the guidance of several people. Dr. Jamie
Thomerson launched me into the study of neotropical fishes. Dr. Donald Taphom
provided me with the opportunity to do long-term research in the Orinoco River basin. In
1980, he took me to the Llanos where we netted my first piranha while seining the muddy
waters of Cao Maraca. The botanist Dr. Basil Stergios invited me to accompany his 1985
expedition to the upper Rio Negro and the Brazo Casiquiare where I fell in love with the
rivers and humid forests of southern Venezuela. My graduate committee chairman, Dr.
Horst Schwassmann, opened my eyes to the Amazon River; together we crossed part of its
estuary, from Belm to the Dha de Maraj, a journey I shall always remember.
My investigations have prospered from discussions with various members of my
committee as well as from the exchange of ideas with colleagues and friends, in particular
Drs. Donald Taphom, Steve Walsh, and Kirk Winemiller. Dr. Horst Schwassmann, and
other members of my committee Drs. Carter Gilbert, Martha Crump, Frank Nordlie, and
Nigel Smith were always helpful. I thank them for their advice and for reviewing the
tedious draft manuscripts. I am also grateful to Drs. Stephen Walsh, Jamie Thomerson,
Thomas Keevin, and Carmine Lanciani, and to Frank Jordon for their comments on
various sections and drafts of the manuscript.
I thank the following persons for their assistance with collecting fishes in the
Venezuelan Llanos: Andelo Barbarino, Linda Delashmidt, Terry Dye, Guillermo Feo,
Carter Gilbert, Oscar Leon, Craig Olds, Stewart Reid, Eric Sutton, Donald Taphom, and


Table 6-8continued.
Species and
Size Range (SL, mm)
SA
80-159
SA
160
MYA
80-159
MYA
>160
MYS
80-159
MYS
>160
MYT
80-159
MYT
>160
CM
80-159
SM
10-19
SM
20-39
PST
10-19
PST
20-39
PYP
10-19
PYP
20-39
SA 80-159
100
75.6
0.1
0
0.75
0.5
32.3
4.5
29.45
2.5
63.1
10.8
58
2.5
2.6
SA >160
100
12.6
12.5
12.55
6.3
30.3
16.4
22.85
0
75
8.3
55.3
0
1.6
MY A 80-159
100
91.2
89.05
17
21.1
55.6
10.45
0
0
0
0
0
1.6
MYA >160
100
96.95
8.2
21
46.8
10.35
0
0
0
0
0
1.6
MYS 80-159
100
6.05
21.05
45.35
10.9
0.55
0
0.55
0.55
0.6
2.2
MYS >160
100
6.3
53.4
6.25
0
0
0
0.4
0
2.3
MYT 80-159
100
24.9
84.05
0
5.3
5.3
5.3
0
1.6
MYT >160
100
14.25
0
0
0
0.2
0
1.8
CM 80-159
100
8
0
7.95
7.95
8.0
9.5
SM 10-19
100
0
90
44.3
84.8
94.0
SM 20-39
100
8.3
55.3
0
0
PST 10-19
100
52.6
86.5
91.6
PST 20-39
100
44.3
44.6
PYP 10-19
100
88.4
PYP 20-39
100


174
common species (e.g., seeds from rubber trees and palms). Goulding (1980) was able to
identify only a few seeds eaten by Amazonian piranhas. Similarly, because I could not
identify the seeds and most other plant materials in the diets of Orinoco herbivorous species
(i.e., adults), I cannot adequately assess their degree of specialization. Snow (1981)
distinguished between specialized frugivorous birds and unspecialized or opportunist
frugivores. The former typically feed on fruits rich in fats and proteins, whereas the latter
mosdy take fruits that provide mainly carbohydrates and less nutritious overall.
Although serrasalmine species or size classes were assigned to particular trophic
guilds, all exhibited a certain amount of plasticity in their diets. Because most foods do not
supply all the nutrients needed by an animal, a certain level of diet flexibility is probably a
requirement. An assessment of the balance between benefits and costs of piranha particular
modes of feeding and prey choice lies beyond the scope of the present study. Analysis of
energy and nutrient content suggests that certain types of foods are generally more
beneficial than others (e.g., fish flesh and insects over fish fins and scales, fruits and seeds
over leaves), but it ignores the possible costs of foraging, and that proportion of a food
item that is actually assimilated by the consumer. Each of these determinations would
require further study. Comparing aquatic versus terrestrial feeding modes, Liem (1990)
hypothesized that fish, by nature of their being designed for life in the water, have a much
more versatile feeding apparatus (i.e., mouth and jaw structures) than terrestrial
vertebrates. Based on this "built-in versatility", one of Liem's predictions was that fish
should be highly opportunistic in their feeding, thereby exhibiting both high dietary overlap
and extensive prey switching.


186
MCNG 1995 (6-6); MCNG 2046 (28-28); MCNG 2122 (6-6); MCNG 2162 (4-4); MCNG
2189 (3-3); MCNG 2216 (2-2); MCNG 2336 (1-1); MCNG 2359 (9-9); MCNG 2377 (15-
15); MCNG 3645 (1-1); MCNG 3729 (6-6); MCNG 3843 (1-1); MCNG 3889 (1-1);
MCNG 3984 (1-1); MCNG 4092 (3-3); MCNG 4154 (2-2); MCNG 4166 (7-7); MCNG
4199 (4-4); MCNG 4218 (1-1); MCNG 4233 (1-1); MCNG 4308 (4-4); MCNG 4341 (3-
3); MCNG 4543 (1-0); MCNG 4558 (2-2); MCNG 4583 (1-1); MCNG 4688 (2-2);
MCNG 4735 (1-1); MCNG 4776 (1-1); MCNG 4795 (1-1); MCNG 4927 (1-1); MCNG
4974 (20-20); UF 36153 (2-0); UF 77721 (1-0). 1982: MCNG 6325 (1-1). 1984:
MCNG 10712 (50-50); MCNG 11324 (2-2); MCNG 11364 (31-31); MCNG 11366 (1-1);
MCNG 11370 (1-1); LN 84-8 (1-0); DCT 84-68 (4-4). 1985: MCNG 11383 (17-17);
MCNG 11540 (1-0?); MCNG 12471 (6-5). 1989: MCNG 23387 (17-9); MCNG 23134
(6-6); MCNG 23141 (14-7); MCNG 23151 (6-1). 1990: MCNG 23385 (8-8). Cao
Caicara: 1989: LN 89-22 (1-1).
Serrasalmus 'marine I i
Llanos
Cinaruco River drainage: 1982: MCNG 5629 (3-3); 1986: MCNG 17954 (1-1).
1987: MCNG 17156 (8-8). 1989: MCNG 22185 (2-2); MCNG 20180 (2-2); MCNG
21764 (8-8); MCNG 21759 (2-2).
Capanaparo River drainage: 1989: MCNG 20064 (1-1).
Upper Orinoco
Sipapo River drainage: 1989: MCNG 21972 (6-6); LN 89-71 (4-4); LN 89-61
(1-1).
Atabapo River drainage: 1989: MCNG 21957 (6-6); MCNG 21795 (5-5); MCNG
22023 (1-1); MCNG 21889 (2-2); MCNG 21890 (1-1); MCNG 22019 (2-2); MCNG


Table 5-5. Food items of Serrasalmus rhombeus from the Apure River drainage (Cao Caicara area) by size class.
%0 = percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N 51.
Size class (mm, SL)
Number examined
Number empty
Food items
II (20-39)
18
1
%0 %D %Va
Ill (40-79)
15
0
%0 %D %Va
IV (80-159)
8
1
%0 %D %Va
V(>160)
10
1
%0 %D %Va
Plant material
-
-
-
20.0
-
-
42.9
25.0
27.3
11.1
-
-
Microcrustaceans
23.5
15.8
10.9
-
-
-
-
-
-
-
-
-
Aquatic insects
47.1
26.3
32.6
-
-
-
14.3
-
-
11.1
-
-
Other invertebrates
5.9
-
-
-
-
-
28.6
12.5
9.1
33.3
-
-
Small whole fish
-
-
-
6.7
5.9
8.6
-
-
-
44.4
33.3
36.9
Fish flesh
-
-
-
13.3
11.8
8.6
28.6
12.5
18.2
55.6
22.2
21.1
Fish fins
64.7
57.9
56.5
93.3
76.5
80.0
71.4
50.0
45.5
33.3
33.3
31.6
Fish scales
-
-
-
26.7
5.9
2.9
42.9
-
-
22.2
-
-
Other
-
-
-
-
-
-
14.3
-
-
11.1
11.1
10.5
OO
4^


li
Chimita, Atacavi River, with gill net and handlines. The only other specimen known is that
of a single fish taken from a tributary of the blackwater Pasimoni River in the upper Rio
Negro drainage of Venezuela (W. Fink, personal communication). The species is currently
being described as new by W. Fink and A. Machado-Allison, and the five fish reponed on
here will be part of the type series. Pristobrycon sp. is a medium to large-sized piranha
with a rounded snout and a fairly robust body that is covered with irregularly-shaped black
markings (Fig. 6-1). It is known locally as "caribe colorado" (a name sometimes applied to
Pygocentrus caribe) because of the bright red-orange color that marks most of the lower
body and the lower fins. Intensity of body coloration is probably related to breeding
condition. Three of the specimens were females, of which one had the gonads almost
completely developed indicating that spawning takes place near the end of the rainy season.
Curipaco Indians collect adults in the flooded forest by pole fishing using small hooks
baited with earthworms; they maintain that the young of Pristobrycon sp. move from the
flooded forests into streams during low water where they are easily caught with nets or
killed with fish poisons derived from plants (barbasco).
Pristobrycon sp. is a seed predator (Fig. 6-2); stomachs of all five specimens were
packed with unidentified crushed seeds, mostly endocarp plus some exocarp and
mesocarp. Food items were as follows (%0-%D-%V; all Group V); masticated seeds
(100.0-100.0-96.4), plant material (leaf fragment of a palm) (20.0-0-0.4), other
invertebrates (winged insects and fragments of a spider) (60.0-0-1.4), and fish scales (20-
0-1.8). Intestines were very long for piranhas, ranging from 630 to 800 mm; IL/SL ranged
from 2.7 to 4 for the five specimens examined.
Pvgopristis denticulams Muller and Troschel 1845
Pygopristis denticulams (Fig. 6-1) was uncommon in my samples. I collected only
one adult (175 mm SL) from the upper Orinoco, taken from Cao Cuchakn of the
blackwater Atabapo River. I also preserved 80 small juvenile P. denticulatus (15-37 mm


Table 6-3. Food items of Serrasalmiis manned from the upper Orinoco River basin by size class. %0 percent frequency of
occurrence; %D = percent dominance; and %V = percent volume. N = 82.
Size class (mm, SL) 11 (20-39) III (40-79) IV (80-159) V(>160)
Number examined 4 18 18 42
Number empty 0 5 7 16
Food items
%o
%D
%v
%o
%D
%V
%o
%D
%V
%o
%D
%V
Masticated seeds
-
-
-
-
-
-
9.1
-
0.1
30.8
19.2
9.5
Plant material
-
-
-
15.4
7.7
1.5
27.3
18.2
13.1
15.4
11.5
15.1
Decapoda
-
-
-
-
-
-
-
-
-
15.4
3.8
2.9
Aquatic insects
-
-
-
-
-
-
9.1
-
0.01
-
-
-
Other invertebrates
-
-
-
7.7
-
0.8
18.2
18.2
1.0
11.5
7.7
1.2
Fish flesh
-
-
-
38.5
30.8
68.2
45.5
40.9
81.8
69.2
46.2
68.5
Fish fins
100.0
100.0
100.0
28.7
57.7
28.7
27.3
22.7
4.1
3.8
3.8
1.4
Fish scales
-
-
-
7.7
-
0.1
-
-
-
11.5
-
0.3
Other
_
_
_
7.7
3.8
0.8
-
-
-
11.5
7.7
1.0
Note: Stomach contents of a single specimen of Group I size class (10-19 mm SL) consisted of aquatic insects.
o
-j


67
O
r
o
0.5
1.0
Water Types
Dominant
Vegetation
APURE W (B,C) S
CAPANAPARO B (C) s
CINARUCO B (C) S
VENTUARI W (B,C) F
MATACUNI W F
OCAMO W (B) F
M A VACA W (B) F
SI PAPO B (C) F
ATABAPO B F
I I I
0.5 1.0
Coefficient of Biogeographic Resemblance
Fig. 4-5. Dendrogram from cluster analysis depicting similarities among nine sampled
drainages of Orinoco River basin based on piranha species composition. Major
and minor (in parenthesis) water types, W = whitewater, B = blackwater, and C
= Clearwater; Dominant regional flora, S = savanna (low Llanos), and F = forest
(upper Orinoco). Similarity values are from Table 4-3. Clustering technique
was UPGMA, and similarity measure was Duellman's (1990) Coefficient of
Biogeographic Resemblance.


32
Present Climate and Seasonality
Regional topography and the fact that the entire Orinoco Basin lies immediately
north of the equator are important factors controlling climate and the timing of precipitation
(Walter et al. 1975). There is a trend toward increased rainfall from north to south.
Nevertheless, rainfall patterns can be quite variable from year to year in a single locality, as
well as among different localities within any particular region.
The Llanos have consistently high temperatures and fairly distinct wet and dry
periods. The rainy season is associated with the inner-tropical convergence zone (Walter et
al. 1975), and lasts from seven to nine months, usually from late April to October or
November (Fig. 2-5). Little or no rain falls during the two or three driest months, when
the inner-tropical convergence zone is in the southern hemisphere. Total rainfall in the
Llanos ranges from 1200 to 1800 mm per year (Taphom 1990), with savanna grasslands
common to the low Llanos typically receiving 1300-1400 mm (Cole 1986:97). The
recording station at San Fernando de Apure, located in the center of the low Llanos,
reported a mean annual precipitation of 1416 mm, based on 26 years of records (Walter et
al. 1975); mean monthly temperatures for the locality varied between 26.6 and 29.2 C
(Cole 1986:97). However, daily temperatures can fluctuate widely.
Although the two regions have a fairly similar range of air temperatures, the upper
Orinoco is much more humid than the Llanos. Average annual rainfall is 3,250 mm/yr,
with very humid areas receiving well over 4,000 mm (CODESUR 1979). Although the
amount of rainfall varies seasonally, the dry season in the upper Orinoco is not as
pronounced as in the Llanos (Fig. 2-5). Few areas of record receive less than 75 mm in
any given month during the dry season (CODESUR 1979). Nevertheless, the alternation
of low and high water seasons is distinct Elighest precipitation occurs between May and
September and the lowest between December and March (CODESUR 1979). Monthly
mean temperatures range from 26 to 28.5 C (CODESUR 1979). Both the low Llanos of


Fig. 5-3. Diets by size class of seven piranha species and Catoprion ment from Cao Caicara study area, Apure River drainage,
in the low Llanos of Venezuela. Size of segments represents percentage of adjusted volume (Va) of each prey type; n =
number of stomachs examined; numbers in parentheses represent diet breadth using formula of Levins (1968).


LIST OF FIGURES
Figure page
1-1 Hypothesized phylogenetic relationships among genera of the subfamily
Serrasalminae as proposed by Machado-Allison (redrawn from Machado-
Allison 1985) 2
2-1 Map of northern South America showing Orinoco River basin 19
2-2 Major savanna and forest ecosystems in the Orinoco River basin 25
2-3 Approximate distribution of open savanna (low Llanos) in Venezuelan state
of Apure, Orinoco River basin 26
2-4 Approximate distribution of lowland forests in Federal Amazon Territory of
Venezuela 29
2-5 Monthly rainfall recorded at representative sites in Orinoco River basin,
Venezuela. (1) Upper Orinoco: monthly average 1971-1977 from Santa
Maria de Los Guaicas, mouth of Ocamo River, Federal Territory of
Amazonas, and (2) Low Llanos: for year 1972 from Cao Caicara area,
Apure River drainage. Apure State 34
3-1 Map of Venezuela showing nine selected drainages in Orinoco River basin
sampled during present study 38
3-2 Map of Apure State, Venezuela, showing principal low Llanos sampling
locations 39
3-3 Map of 1988-1991 sampling sites in upper Orinoco, Federal Territory of
Amazonas, Venezuela 41
4-1 Schematic representation showing relative distances among the nine
sampled drainages and their approximate location along Orinoco River main
channel 58
4-2 Scatter diagram showing relationship between number of piranha species
per drainage and log of the drainage area size (km2) for nine sampled
drainages in Orinoco River basin, Venezuela 63
4-3 Scatter diagram showing similarity in piranha species composition between
adjacent sampled drainages versus distance between adjacent drainages 65
IX


Figure page
4-4 Scatter diagram showing similarities in piranha species composition
between all possible paired drainages and the distance between paired
drainages 66
4-5 Dendrogram from cluster analysis depicting similarities among nine sampled
drainages of Orinoco River basin based on piranha species composition 67
5-1 Location of Cao Caicara study area, Apure River drainage, in low Llanos
of Apure State, Venezuela 72
5-2 General body form and major fin markings of seven piranha species (55-70
mm SL) and Catoprion ment from Cao Caicara study area, Apure River
drainage, in the low Llanos of Venezuela 73
5-3 Diets by size class of seven piranha species and Catoprion ment from Cao
Caicara study area, Apure River drainage, in the low Llanos of Venezuela 76
5-4 Diet breadths estimated for seven piranha species and Catoprion ment, by
size class, from the Cao Caicara area of the low Llanos, Apure River
drainage, Orinoco River basin, Venezuela 94
5-5 Dendrogram from cluster analysis depicting similarities among diets of
piranha species (by size class) from the Cao Caicara area of the low
Llanos, Apure River drainage, Orinoco River basin, Venezuela 96
6-1 Eight piranha species from the upper Orinoco River basin of Venezuela 98
6-2 Diets by size class (>40 mm SL) of eight piranha species from the upper
Orinoco River basin, Venezuela 101
6-3 Diets of selected small juvenile piranhas (10-19 mm SL) from upper
Orinoco River drainages and the low Llanos, Venezuela 108
6-4 Diets by size class (>80 mm SL) of four common serrasalmine species from
the upper Orinoco River basin: Catoprion ment, Mylens asterias, M.
schomburgkii, and M. torquatus 120
6-5 Dendrogram from cluster analysis depicting similarities among diets of
piranha and related species (by size class) from the upper Orinoco River
basin, Venezuela 127
6-6 Diet breadths estimated for eight piranha species, by size class, from the
upper Orinoco River basin, Venezuela 130
6-7 Diets by size class (>40 mm SL) of three piranha species from the Cinaruco
and Capanaparo river drainages of the low Llanos, Orinoco River basin,
Venezuela 133
x


182
Upper Orinoco
Ventuari River drainage: 1989: MCNG 22054 (38jv-38).
Mavaca River drainage: 1991: MCNG 25335 (1-1); Ocamo River drainage: 1990:
MCNG 22249 (4-4)
Pristobncon sp
Upper Orinoco
Atabapo River drainage: 1989: MCNG 21757 (5-5) (note: these five specimens
will be paratypes and divided among several museums, MCNG 21757 [2-2], MBUCV #
[1-1], and UMMZ # [2-2]).
Pvqocentrus caribe
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 3547 (1-1); MCNG
7686 (1-1); MCNG 8313 (4-4); MCNG 8342 (1-0); MCNG 9421 (2-2). 1980: MCNG
1776 (1-1); MCNG 4440 (1-1); MCNG 5899 (8-7); UF 37063 (2-0). 1981: MCNG 1996
(6-0); MCNG 2036 (5-5); MCNG 2076 (2-2); MCNG 2160 (7-7); MCNG 2166 (7-7);
MCNG 2188 (5-5); MCNG 2215 (1-1); MCNG 2298 (2-2); MCNG 2357 (4-4); MCNG
2379 (25-25); MCNG 2461 (4-4); MCNG 2482 (1-1); MCNG 3693 (2-2); MCNG 3728
(3-3); MCNG 3754 (1-1); MCNG 3842 (3-3); MCNG 3873 (1-1); MCNG 3888 (9-9);
MCNG 4006 (3-3); MCNG 4023 (145-30); MCNG 4049 (13-7,6jv); MCNG 4058 (2-2);
MCNG 4074 (3-1,2jv); MCNG 4119 (7-7); MCNG 4135 (6-6); MCNG 4153 (47-47);
MCNG 4168 (1-1); MCNG 4200 (2-2); MCNG 4217 (2-2); MCNG 4284 (3-3); MCNG
4309 (2-2); MCNG 4491 (1-1); MCNG 4557 (2-2); MCNG 4689 (2-2); MCNG 4715 (1-
1); MCNG 4737 (1-1); MCNG 4757 (2-2); MCNG 4777 (1-1); MCNG 4796 (1-1); 4901
(7-7); MCNG 4925 (5-5); MCNG 5030 (2-2); MCNG 5168 (1-1); MCNG 7881 (57-57?);


183
MCNG 10418 (2-1,ljv); MCNG 10419 (20-19, ljv); DCT 81-157 (2-1); DCT 81-159 (2-2);
DCT 81-160 (20-20); PIMA 18-25 (5-4); PIMA 18-26 (1-1); PIMA 18-27 (6-6); PIMA 18-
30 (3-3); PIMA 18-33 (5-5); PIMA 18-36 (7-7); PIMA 18-37 (1-1); PIMA 18-44 (4-4);
PIMA 18-46 (7-6); PIMA 18-49 (1-1); PIMA 18-78 (1-1); PIMA 18-90 (14-14); PIMA 18-
91 (1-1); uncatalogued student collection (11-10). 1982: MCNG 5075 (1-1); PIMA 18-96
(2-2); PIMA 18-98 (3-3); PIMA 18-99 (4-4). 1983: MCNG 10322 (77-71). 1984:
MCNG 10709 (18-18); MCNG 11325 (72-14); 11367 (4-4?); LN 84-7 (14-14); LN 84-8
(8-8); LN 84-76 (71-55?); DCT 84-13 (7-7). 1988: LN 88-23 (12-12); LN 88-24 (13-13);
LN 88-26 (43-43); LN 88-27 (17-17); LN 88-28 (11-11); LN 88-29 (11-11); LN 88-30
(16-16). 1989: LN 89-171 (5-2); LN 89-170 (6-6); LN 89-173 (1-1); LN 89-176 (9-9).
Other: MCNG 20751 (7-7); MCNG 8790 (1-1?).
Juveniles less than 20 mm SL.tentatively identified as P. caribe. UNELLEZ
module.-1981: MCNG 3949 (59-27jv); MCNG 3956 (21-20jv); MCNG 4006 (2-2);
MCNG 4023 (145-29jv); MCNG 4049 (13-6jv); MCNG 4< ¡74 (3-2jv); MCNG 4075 (1-1);
MCNG 4119 (7-3); MCNG 4135 (5-ljv); MCNG 4258 (1-1); MCNG 7881 (57-24jv);
MCNG 10418 (2-ljv); MCNG 10419 (20-ljv); MCNG 10424 (1-1).
Upper Orinoco
Ventuari River drainage: .1989: MCNG 22974 (2-2); MCNG 22247 (1-1); LN 89-
166 (2-2); LN 89-167 (2-2).
Ocamo River drainage: .1990: MCNG 22269 (2-2); MCNG 22295 (2-2); LN 90-
20 (1 1).
Pvqopristis denticulatm
Llanos
Apure River drainage: 1981: MCNG 3243 (3-1); UF 36177 (1-0).


91
algae, was present in small amounts in many stomachs. Rare items included an aquatic
beetle larva, a cladoceran, and the head of a small characid fish {Aphy ochar ax erythrurus).
Small juvenile piranhas. Group I (10-19 mm SL)
Most piranhas spawn at the onset of the rainy season. Small juveniles inhabit the
flooded grasses and marsh habitats of the flooded savanna. The newly flooded savanna
acts as a prime nursery area for young fish since the flooded herbaceous vegetation
provides protection from predation and produces an abundant supply of invertebrates that
are utilized for food. The 114 stomachs of small juvenile piranhas contained mostly
microcrustaceans and aquatic insects (Table 5-10 ). As size increased within this group
there was a gradual switch from microcrustaceans to small aquatic insects. Primary food
items, in order of importance (high %Va and %D), were: cladocerans, chironomid larvae,
copepods, and ostracods.
Comparison of Diets
Fish (flesh, fins, scales and small whole fish) were the main component of diets of
all seven species of piranhas, both in terms of dominance and adjusted volume (Fig. 5-3).
Only in small juveniles of Group I and juvenile P. caribe less than about 80 mm SL (or
where sample sizes were small, e.g., Group IV P. striolatus) did non-fish items make up a
large proportion. Most juveniles had eaten fish fins. Major exceptions were P. caribe, a
generalist, and C. ment, a highly specialized scale-eater. Fins were usually from fishes
similar in size to the predator. Based on this observation, one may assume juvenile
piranhas were attacking small species or juveniles of other fishes. Whereas fish were the
predominant food resource used by savanna populations, other vertebrates (i.e., mammals,
birds, reptiles, and amphibians) were only of minor importance (Table 5-2).


4
tropical environments are seriously threatened. Because of expanding human populations
and increased development, natural habitats are being destroyed or degraded at a rapid
pace. Forests are being cleared for agriculture, ranching, timber, and minerals; rivers and
their floodplains are being modified by dams, levees, and pollution. Aquatic and terrestrial
systems in the lowland tropics are intricately interwoven, the changes to each inevitably
affecting the other. The profound and likely irreversible changes now occurring
throughout tropical America make it increasingly important to understand more about the
interrelationships between tropical environments and their diverse fauna and flora. Such an
understanding is necessary for successful conservation of habitats, species, and genetic
stocks.
The science of ecology attempts to understand the complex interrelationships
between an organism and its physical and biotic environment. Studies in trophic ecology
are a way to investigate such interrelationships, and often permit analysis at several levels
or scales. Obviously, what an animal eats is limited by the kinds and availability of food
resources in its local surroundings. Valid interpretations of feeding patterns, however, also
require consideration of past environmental conditions, inasmuch as the probability of an
animal taking a particular type of prey depends on its array of interrelated morphological
and behavioral characters that result from its particular phylogenetic history. Trophic
studies provide insights into the biology of organisms, because food, unlike many other
resources or niche parameters, can be measured, analyzed, and compared in a large number
of ways using a variety of techniques. Evidence for the importance and practicality of
research on trophic ecology is provided by the tremendous volume of literature on the
subject (for review of fishes see Ross 1986). Accordingly, the study of diets and food
resources has contributed to the development of many ecological concepts, including
resource partitioning, niche theory, optimality theory, energetics, food webs, and predator-
prey relationships.


177
A Phylogenetic Perspective
In order to synthesize information concerning ecology and evolution, biologists
commonly superimpose ecological or behavioral results onto hypothesized phylogenies
derived from gross morphology or biochemical systematics (Brooks and McLennan 1991).
These types of analyses are preferred because they attempt to establish correlations between
the evolutionary history of organisms and present-day patterns of morphology, behavior,
and ecology. Nevertheless, as Losos (1990) has suggested, meaningful analysis in a
phylogenetic context requires that the group under study has radiated extensively and that
the phylogenetic relationships are relatively well understood. Although piranhas and their
close relatives have undergone moderate radiation, their taxonomy, particularly at the
species level, is still fluid and phylogenetic relationships of serrasalmine fishes are only
partly understood. Using morphological characters, Machado-Allison (1985) provided the
most current analysis of relationships of the subfamily Serrusalminae (Fig. 1-1). His
phytogeny is to genus level only, and its utility for this study is further limited because
most species are in the trophically diverse genus Serrasalmus.
My study provides information on the diets for nine of the 13 serrasalmine genera.
Using data on trophic groupings, I have superimposed my findings onto Machado-
Allison's phytogeny (Fig. 8-2) following the methods of Langtimm and Dewsbury (1991).
It gives a consistency index of 0.5 suggesting that trophic groupings and intestine length
are somewhat consistent with a phytogeny derived from strictly morphological characters.
Because much of the variation in trophic characters within the genus Serrasalmus was due
to the inclusion of Serrasalmus cf. eigenmanni, if this herbivorous species is not included
in the analysis then the consistency index is much higher (i.e., 0.67). Fink (1988)
emphasized the need for future studies on piranha ecology and behavior in addition to
systematic and phylogenetic analyses. Admittedly, my study on serrasalmine trophic
ecology has not answered all the questions. Nevertheless, it will be interesting to see how


CHAPTER 2
THE ENVIRONMENTAL SETTING
In this chapter I give an overview of the Orinoco River basin and describe the two
regions dealt with in the present study: (1) the open savannas or low Llanos of Apure
State, and (2) the upper Orinoco in the Venezuelan Federal Territory of Amazonas, an area
dominated by forests. Little is known about the geological and ecological history of
tropical lowlands in South America (Whitmore and Prance 1987). Because historical
events undoubtedly influenced present-day ecological patterns, I briefly review several
hypotheses concerning the basin's and the river's formation, as well as climatic and
vegetation changes that purportedly took place in northern South America during the recent
past.
The Orinoco River Basin
The Orinoco River, although dwarfed by the Amazon, is a major tropical river. The
basin is located in northern South America between 2 and 10 N latitude, and empties into
the Atlantic Ocean (Fig. 2-1). The Orinoco's mean annual discharge is about 35,800
m3/sec from a drainage area of approximately 1,100,000 km2, located in Venezuela (70%)
and Colombia (30%) (Lewis 1988). Compared to the Mississippi River, the Orinoco has
more than twice the annual discharge, yet drains an area of only one-third the size. The
basin is geologically and ecologically diverse, having large mountain ranges and broad
low-lying plains, with habitats ranging from immense open grasslands to lush tropical
forests.
18


168
had its stomach and intestine full of what were probably palm seeds; about half the seeds
had been masticated and the remainder, about twenty seeds (about 30 mm long) had been
swallowed whole. Machado-Allison and Garcia (1986) reported that juveniles of several
piranha species from a savanna marsh fed on the tiny seeds of sedges (Cyperaceae), but
they did not give number of seeds eaten nor their percentage of the overall volume of food
(Table 1-1).
6) Leaf Eaters. None of the Orinoco piranhas were considered to be folivores, but
small bits of leaves or even flowers were eaten by all species on occasion. Of the
serrasalmine species studied, only Myleus feeds heavily on leaves. Piaractus will also take
leaves in bulk (personal observation). Folivorous serrasalmine fishes seem to restrict
themselves to feeding on live leaves that they clip into small fragments before swallowing.
Similar behaviors have been reported for leaf-eating fishes of the Amazon (Goulding 1980,
Goulding et al. 1988). Goulding et al. (1988) hypothesized that folivory by Amazonian
fishes is limited by the toxic chemicals in the leaves. Their studies suggest no specialized
folivores among herbivorous fishes, but rather that frugivorous fishes become leaf eaters
only when fruits and seeds are scarce, for instance during periods of low water. Most of
the Myleus that I examined were captured during the low water period; therefore, I cannot
rule out such a seasonal shift in diet. Nevertheless, the stomachs of herbivorous piranhas,
netted together with Myleus taken in the upper Orinoco during the drier part of the year,
were full of seeds, suggesting some sort of food resource partitioning.
Ontogenetic Changes in Diet
My study approach has been to emphasize dietary differences among different size
classes as well as among species. The differences found therefore tend to support the
contention of Stoner and Livingston (1984) that ecological studies of fishes should employ
the "ontogenetic trophic unit" concept rather than grouping a taxonomic species as a single
functional ecological unit. Changes in diet with age have been documented for many of the


188
Serrasalmus rhombeiis
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 8267 (1-1); MCNG
8314(3-3). 1981: MCNG 4137 (1-1); MCNG 10420 (1-1); MCNG 10423 (1-1); MCNG
10464(1-1); MCNG 11330 (1-1); MCNG 11331 (1-1); (1-1); DCT 81-157 (3-3). 1984:
MCNG 11345 (1-1); MCNG 11368 (1-1); MCNG 11377 (1-1). 1988: 19070 (1-1); LN
89-12 (1-1). 1989: MCNG 23389 (2-2). Cao Maporal.-1981: MCNG 10168 (1-1);
MCNG 10246 (1-1); MCNG 10288 (7-7); UF 77723 (2-0). 1984: MCNG 11362 (7-6);
MCNG 11348 (1-1); MCNG 11376 (2-2). Other.-1979: MCNG 9752 (13-4). 1984:
MCNG 1927 (1-1); MCNG 11378 (4-4); MCNG 12933 (6-6).
Upper Orinoco
Orinoco main stem: 1989: MCNG 22503 (2-2); LN 89-92 (1-1). 1991: MCNG
25397 (1-1)
Ventuari River drainage: 1989: MCNG 22021 (1-1); MCNG 21970 (1-1); MCNG
21981 (1-1); MCNG 21968 (3-3); LN 89-111 (5-5); MCNG 21926 (1-1); MCNG 22021
(1-1); MCNG 22503 (2-2);
Matacuni River drainage: 1990: MCNG 22507 (3-3); MCNG 22127 (14-14);
Ocamo River drainage: 1990: MCNG 22109 (1-1); MCNG 22102 (1-1); MCNG
22114 (5-5); MCNG 22130 (1-1); MCNG 22131 (1-1); MCNG 22270 (3-3); MCNG
22294 (2-2); MCNG 22411 (1-1); MCNG 22412 (4-4); MCNG 22416 (5-5); MCNG
22420 (1-1); MCNG 22251 (1-1); MCNG 22261 (2-2); MCNG 22923 (1-1); LN 90-12
(5-5); LN 90-14 (6-6); LN 90-19 (1-1); LN 90-21 (1-1); LN 90-22 (1-1); LN 90-26 (2-2);
LN 90-27 (3-3); LN 90-33 (1-1); LN 90-42 (7-7); LN 90-37 (4-4); LN 90-38 (2-2): LN
90-45 (2-2); LN 90-46 (2-2); LN 90-49 (1-1);
Mavaca River drainage: 1991: MCNG 25365 (1-1).


Table 5 8. Food items of Pristorbrycon striolatus from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N 16.
Size class (mm, SL)
Number examined
Number empty
Food items
%o
11 (20-39)
12
1
%D
%Va
%o
m(40-79)
1
0
%D
%Va
IV (80-159)
3
0
%0 %D %Va
Decapoda
-
-
-
-
-
-
66.7
33.3
28.6
Aquatic insects
27.3
18.2
13.3
-
-
-
66.7
-
-
Other invertebrates
3.9
-
-
-
-
-
33.3
33.3
28.6
Fish flesh
18.2
9.1
10.0
-
-
-
33.3
33.3
42.9
Fish fins
81.8
72.7
76.7
100.0
100,0
100.0
-
-
-
Fish scales
-
-
-
-
-
-
33.3
-
-


CHAPTER 6
TROPHIC ECOLOGY OF PIRANHAS FROM THE UPPER ORINOCO
This chapter focuses on the trophic ecology of piranhas and related species from the
upper Orinoco River basin of southern Venezuela, a region characterized by extensive
lowland forests that undergo seasonal flooding. I also provide information on the diets of a
few savanna populations not reported in the previous chapter, and compare feeding patterns
of serrasalmine fishes from savanna with those from forested regions. Finally, I examine
the relationship between intestine length and serrasalmine diets.
There have been few studies of the fishes inhabiting the upper Orinoco River
region. To date, published works have dealt mainly with descriptions of new species or
reports of species distributions as part of broader investigations on South American fish
zoogeography. The research presented here is the first field study of fishes from the
southern region of Venezuela aimed at understanding fish feeding patterns. Although
feeding behaviors among certain piranha species are somewhat similar, the diets of several
species have not been reported previously. The eight species of piranhas examined from
the upper Orinoco are Serrasalmus rhombeus, S. manueli, S. cf. eigenmanni, S. altuvei,
Pygocentrus caribe, Pygopristis denticulatus, Pristobrycon striolatus, and an undescribed
Pristobrycon sp. (Fig. 6*1). I also report on the diets of several other serrasalmine fishes,
focusing primarily on Catoprion ment, Myleus asterias, M. schomburgkii, and M.
torquatus.
97


Table 7-1. Estimates of the lipid, protein, ash, carbohydrate, and caloric contents of fins, scales, and whole fish
for two taxa of typical piranha prey fish. Energy expressed as kJ/g of dry mass, all others given as percent of
dry mass. Where number of replicates exceeds one, values represent mean standard error with number of
replicates in parentheses.
kJ/g
(dry mass)
%
Protein
(dry mass)
%
Ash
(dry mass)
%
Lipids
(dry mass)
%
Carbohydrate
(dry mass)
Cichlidae
Whole fish
14.8 .0.01 (2)
50.7 0.05 (2)
33.3
7.01 0.02 (2)
0.1 0.03 (2)
Scales
9.0.0.01 (2)
43.5 0.05 (2)
48.7
1.1 0.18 (2)
5.7 1 0.00 (2)
Fins
9.2 .0.00.(2)
35.9 0.05 (2)
56.2
3.3 1 0.03 (2)
0.5 1 0.03 (2)
Curimatidae
Whole fish
14.9 .0.00.(2)
52.210.10 (2)
33.7
6.0 1 0.01 (2)
0.8 1 0.03 (2)
Scales
10.2 .0.00.(2)
44.2 0.38 (2)
48.3
0.7 1 0.01 (2)
6.3 1 0.03 (2)
Fins
10.9 .0.00.(2)
34.0 0.60 (2)
57.8
2.1 1 0.03 (2)
2.5 1 0.01 (2)
Combined
Whole fish
14.9 0.03 (4)
51.510.44 (4)
33.5 1 0.20 (2)
6.5 1 0.30 (4)
0.5 1 0.19 (4)
Scales
9.6 0.36 (4)
43.9 1 0.24 (4)
48.5 1 0.20 (2)
0.910.14 (4)
6.010.17 (4)
Fins
10.1 0.48 (4)
34.9 1 0.60 (4)
57.0 1 0.80 (2)
2.7 1 0.37 (4)
1.5 0.58 (4)


17
the upper Orinoco River Basin, a region characterized by extensive forests that undergo
seasonal flooding. In addition, my findings from the upper Orinoco are compared to
results from my studies of savanna populations, including data on a few savanna species
not reported in previous studies. Chapter 7 then gives results of an analysis of the nutritive
values of various food items commonly taken by piranhas. Finally, Chapter 8 summarizes
the major findings of the study, and attempts to interpret and synthesize the results in terms
of relevant mechanistic, ecological, and evolutionary issues.


Coefficient of Resemblance (CBR)
65
1.0i
0.8-
0.6-
0.4
0.2-
o 0
0.0 "I 1 1 T 1 1 1 1
0 100 200 300 400
Distance between adjacent drainages (km)
Fig. 4-3. Scatter diagram showing similarity in piranha species composition between
adjacent sampled drainages versus distance between adjacent drainages.
Similarity measure was Duellman's (1990) Coefficient of Biogeographic
Resemblance.


93
I rarely found evidence of seed-eating by piranhas in the Cao Caicara site, with the
few seeds eaten being very small and probably taken incidentally along with intended prey
items. Although other plant material, such as bits of leaves, grass blades, root wads, tiny
flowers, and filamentous algae, was ingested, these items were usually of minor
importance in terms of dominance and volume. Of hundreds of specimens examined, not
one stomach contained many seeds. Most of the low Llanos, including gallery forests, do
not produce many large fruits or big seeds. By way of comparison, stomachs of the
herbivorous adults of Mylossoma sp. and Metynnis sp., taken in the Cao Caicara study
area, were typically full of filamentous algae, masticated small seeds, and nonwoody
vascular plant debris.
Diets and diet breadth usually changed with age. Diet breadth values were typically
higher for the larger size classes (Fig. 5-3 and 5-4), but C. ment (the highly specialized
scale-eater) had low diet breadth values (1.08 to 1.69) for all size groups. Group III P.
caribe, with 5.92, had the widest breadth.
Table 5-11 is a matrix showing the diet overlap values for piranhas, by size class,
from the Cao Caicara area. Cluster analysis of the Table 5-11 data produced four major
trophic groupings (Fig. 5-5). Cluster I consisted of small juvenile piranhas that fed on
small invertebrates, mostly microcrustaceans and aquatic insects. Cluster II contained
seven species and three different size classes grouped together based on their high degree
of piscivory. These piranhas frequently fed by cutting out chunks of flesh from other fish;
however, diets also included an assortment of small fish taken whole, fish fins, and fish
scales. Cluster HI represented fin-eating piranhas. It included six species, and most were
in size classes that included individuals between 20 and 80 mm SL. The only exception
was adult Serrasalmns elongatus in the >160 mm SL size range. Cluster IV was composed
of scale-eaters and represented by the three size classes of Catoprion ment. As a reflection
of the intraspecific changes or shift in diet with age or size, most species were divided
among two or more of the different cluster groupings.


100
Species Accounts
Figure 6-2 is a summary of the diets by size class of the eight piranha species taken,
in the upper Orinoco. A partial listing of prey items identified from the stomachs of the
common piranhas is given in Table 6-1. In this section I describe the general morphology,
local distribution and habitat, as well as the diets for each of the upper Orinoco piranhas
and several other serrasalmine fishes.
Serrasalmus rhombeus (Linnaeus 1766)
Serrasalmus rhombeus was the most abundant piranha in most samples from the
upper Orinoco River. Greatest numbers were found in whitewaters such as the Ocamo and
Paru rivers where they typically inhabited main channel borders. Serrasalmus rhombeus
(Fig. 6-1) was also the largest piranha species taken, reaching well over 350 mm SL. Like
many piranhas, it varies ontogenetically in both body form and coloration. Juveniles have
a moderately elongate body and pointed snout, whereas adults are robust with a relatively
deep body. Juvenile body color is silver with black spotting, and the caudal fin has a
terminal black band. The body and fins of large adults are darkly pigmented, typically
gray or blue black.
Serrasalmus rhombeus was one of the most carnivorous of the upper Orinoco
piranhas (Fig. 6-2 and Table 6-2). Individuals from 40-159 mm SL (Groups ni-IV) fed
mostly on fish flesh and fins, and the largest specimens examined (>160 mm) had fed
mainly on small fish. Only a few of the prey fish ingested could be identified (Table 6-1).
A large S. rhombeus contained the skeletal remains of an adult toad identified as Bufo
marinas, but overall they rarely preyed upon non-fish vertebrates. Plant material was also
relatively unimportant in their diet, small quantities being found in stomachs of only 11 of
the 83 specimens and accounting for less than 5% of the total food volume. Most or all of
these plant items were probably ingested incidentally .while attacking other prey. Plant


Fig. 6-2. Diets by size class (> 40 mm SL) of eight piranha species from the upper Orinoco River basin, Venezuela. Size of
segments represents percentage of volume (%V) of each prey type; n = number of stomachs examined; numbers in
parentheses represent diet breadth using formula of Levins (1968).


with computer drawing of dendrograms, and Craig Lilyestrom for help with a few of the
graphs and introducing me to the Macintosh computer.
Parts of my research were funded by National Geographic Society grants no. 3811-
88 and 4183-89. The Department of Zoology, University of Florida, provided additional
funds and equipment I thank all those in the Department of Zoology and Florida Museum
of Natural History who gave of their time. I thank George Burgess for use of his library.
The Universidad Nacional de los Llanos Occidentales and Museo de Zoologa (UNELLEZ-
MCNG) gave me lab space and administrative assistance in Venezuela. I am indebted to
many of the UNELLEZ administrators and staff for their help during the last ten years. In
addition, I thank the Venezuelan people, campesinos. Llaneros, and indgenas, for
allowing me do research in their beautiful country.
While conducting this study I came to know many very special people. During my
stay in Venezuela, I enjoyed the warm hospitality and friendship of Luis and Sioux Strebin,
Jose and Sharon Sutera, and Basil and Anita Stergios; along with Terry Dye, Donald
Taphorn, Lucas van Balen and his wife, and Dr. H. Kasem. they brought me through my
bout with falciparum malaria. I express appreciation to Dr. Horst Schwassmann and his
wife Satiko for frequently inviting me into their home during my passages through
Gainesville. I also thank Dr. Carter Gilbert and all my fellow graduate students, especially
Dennis Haney and Dr. Steve Walsh, for their many hospitalities. Finally, I thank my
parents and family for their constant love and support, both at home and during the many
long separations, and I thank Linda for always being there.
IV


203
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computing. John Wiley and Sons, New York, 337 pp.
Luengo, J. A. 1965. La longitud del tubo digestivo de Prochilodiis reticulatus y
Serrasalmus nattereri en relacin con sus hbitos alimentarios (Pisces). Physis
(Buenos Aires) 25(70):371-373.
Lundberg, J. G., J. W. M. Lewis, Jr., J. F. Saunders, III, F. Mago-Leccia. 1987. A
major food web component in the Orinoco River channel: evidence from
planktivorous electric fishes. Science 237:81-83.
Lundberg, J. G., O. J. Linares, M. E. Antonio, and P. Nass. 1988. Phractocephalus
hemiliopterus (Pimelodidae, Siluriformes) from the Upper Miocene Urumaco
formation, Venezuela: a further case of evolutionary stasis and local extinction
among South American fishes. Journal of Vertebrate Paleontology 8(2): 131-138.
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Serrasalminae). Acta Biolgica Venezuelica 12(1): 1' ¡-42.
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40:111-132.


60
River, where Serrasaimus cf. eigenmanni was the most common piranha collected.
Pygocentrus caribe is the predominant piranha throughout most of the Llanos, and was
abundant in samples from the Apure River drainage although absent or uncommon in the
Cinaruco and Capanaparo. Pygocentrus caribe was rare in the upper Orinoco.
Serrasaimus irritans and 5. medinai were locally common in the low Llanos, but neither
was taken in the upper Orinoco. Serrasaimus manueli, although absent from much of the
Llanos, was commonly taken along with S. rhombeus in the Cinaruco River. Pristobrycon
striolatus, although widespread, was never common in any one drainage.
Species occurred in one to seven of the nine drainages sampled (Table 4-1); most
were found in several (mean = 4.1) drainages, with Serrasaimus rhombeus and
Pristobrycon striolatus (taken in seven drainages) being the most widespread. Several
species were absent from two middle drainages, the Sipapo and Atabapo rivers. Two
species were limited to single drainages. In the Orinoco River basin, Pristobrycon sp. is
known only from the Atabapo drainage. Serrasaimus medinai was represented only in
Apure River samples (although it is found in other Orinoco tributaries that fringe the
Llanos, drainages not included in this study).
The number of piranha species per drainage ranged from 1 to 8 (mean = 5.0)
(Table 4-1). Sipapo drainage samples yielded only one piranha species (Serrasaimus
manueli), whereas all other drainages were inhabited by three or more species. The Apure
had the highest number of species (eight), but it was also the largest and best sampled
drainage. There was a significant correlation between numbers of piranha species and size
of drainage area (Spearman rank correlation, rs = 0.67, one-tailed P < .05, n = 9; Table 4-
2, Fig. 4-2).
Species composition of piranha assemblages across drainages was highly variable;
CBR values ranged from 0 (i.e., no species in common) to 0.83 (Table 4-2). Adjacent
drainages often shared many of the same species (Table 4-3), but waterways that had
many species in common (i.e., high CBR) were not always those drainages that were


Table 6-6. Food items of Pristobrycon striolatiis from the upper Orinoco River basin by size class. %0 = percent frequency of
occurrence; %D = percent dominance; and %V = percent volume. N = 43.
Size class (mm, SL)
Number examined
Number empty
Food items
1(19-20)
16
0
%0 %D %V
II (20-39)
22
2
%Q %D %V
IV (80-159)
4
0
%0 %D %V
%o
V(>160)
1
0
%D
%v
Masticated seeds
-
-
-
-
-
-
75.0
60.0
71.8
100.0
100.0
95.0
Plant material
-
-
-
-
-
-
50.0
20.0
5.7
100.0
-
4.5
Microcrustaceans
18.8
-
1.7
-
-
-
-
-
-
-
-
-
Aquatic insects
93.8
93.8
90.0
50.0
50.0
44.3
-
-
-
-
-
-
Other invertebrates
-
-
-
5.0
-
0.4
25.0
-
2.9
-
-
-
Fish flesh
-
-
-
-
-
-
25.0
20.0
12.0
-
-
-
Fish fins
12.5
6.3
8.3
50.0
50.0
55.3
50.0
-
6.7
-
-
-
Fish scales
-
-
-
-
-
-
-
-
-
100.0
-
0.5
Other
_
-
-
-
-
-
25.0
-
1.0
-
-
-


87
(Table 5-7 and Fig. 5-3). Fish fins, scales, flesh and small whole fish were found in the
two size classes (HI and IV) represented in our samples.
Pristobrycon striplatus ( Steindachner) 1908
Pristobrycon striolatus was rare in the Cao Caicara study area, and was collected
only on several occasions from Cao Maporal. It is a medium-sized species (Fig. 5-2),
less than 200 mm SL; the largest specimen taken from the Cao Caicara region was 156
mm. Adults sometimes had a red-orange chest and occasionally a pattern of orange vertical
bars along the sides. Pristobrycon striolatus has a rather blunt snout, but smaller and
weaker jaws and jaw musculature than Pygocentrus caribe. The body is deep and strongly
compressed. Small juveniles are similar to young Serrasalmus rhombeus but are slightly
stouter, lack ectopterygoid teeth, and have little if any side spotting. The largest individual
collected in the study area was 159 mm SL. I examined the stomach contents of 16 of the
38 specimens collected. Food items by size class are given in Table 5-8 and Figure 5-3.
Specimens in Group II fed mostly on fish fins as did the one Group IE specimen
examined. Three adults from Group IV contained fish flesh, a few scales, shrimp
fragments, an adult aquatic beetle, an aquatic hemipteran and unidentified insect fragments.
Catoprion ment (Cuvier) 1819
Catoprion ment was common in many of the streams and savanna pools. It is a
small, deep-bodied species (Fig. 5-2) that is closely related to piranhas. Although
maximum size is around 120 mm SL, in the Apure drainage most specimens sampled were
under 80 mm SL, and none was greater than 100 mm. The teeth of C. ment are
somewhat everted and its long lower jaw swings open to more than 180 degrees, making it
well suited for scraping scales off other fish. The stomachs of all 104 specimens examined
contained fish scales (ranging up to 23 mm in diameter) (Table 5-9 and Fig. 5-3). Plant
material, primarily comprising vascular debris and root wads, and occasionally filamentous


27
landscape floods during the rainy season, whereas surface water during the dry season is
usually limited to a few large permanent lagoons, large streams, and rivers. As the dry
season progresses, the savanna vegetation turns yellow and the earth becomes hard and is
fissured with cracks from the intense heat of the sun. Rivers and streams in the low Llanos
are of low gradient, with many wide meanders and anastomoses. The Apure River and
many of its tributaries are whitewater in character, with a relatively high sediment load and
high conductance (Saunders and Lewis 1988). In contrast, the Capanaparo and Cinaruco
are essentially blackwater rivers, with moderate sediment loads. In addition to stream
channels, the landscape of the low Llanos is dotted with shallow marshes (esteros) that
hold water after floods or rain. Lagoons (lagunas) form in deeper depressions, some
created from abandoned stream meanders, and are more permanent aquatic habitats.
Human population density is low and most of the low Llanos is used for cattle ranching.
Since the early 1970's extensive networks of low earthen dikes, called modules {mdulos),
have been constructed, surrounding large areas of the floodplain savanna. These modules
lessen the extreme effects of seasonal changes within their boundaries by controlling
flooding and by holding water in lower areas, available to cattle year round. The hundreds
of borrow pits {prestamos) excavated during the construction of these dikes, as well as
from building of roads, collect water and serve as permanent and semi-permanent artificial
lagoons. Typically less than 25 m wide, some prestamos stretch unbroken for several
kilometers.
During high water, adjacent rivers and streams in the Llanos are often connected by
sheet flooding of the savanna or by filling of small interconnecting channels. Thus, fish
are generally able to move across the entire floodplain. However, where dikes or
roadways are present, run-off patterns have changed and local fish movements are
somewhat restricted (Taphom and Lilyestrom 1984, Nico and Taphom 1988).
Many of the wetlands in the Llanos contain large amounts of organic material and
become highly productive during the rainy season (Mago-Leccia 1970, Saunders and


LIST OF TABLES
Table page
1-1 Summary of principal field studies investigating piranha feeding and diets in
order of publication date 9
3-1 List of abbreviations used in figures and tables for piranhas and other
serrasalmine fishes 46
4-1 Occurrence of piranha species in samples from nine drainages in the
Orinoco River basin, Venezuela 59
4-2 Distance between drainages and Coefficient of Biogeographic Resemblance
among nine sampled drainages in the Orinoco River basin 62
4-3 Number of shared piranha species and Coefficient of Biogeographic
Resemblance among nine sampled drainages in the Orinoco River basin 64
4-4 Summary of piranha species occurrence by habitat and water type, based on
samples in Orinoco River basin, Venezuela 70
5-1 Food items of Pygocentrus caribe from the Apure River drainage (Cao
Caicara area) by size class 79
5-2 List of vertebrate prey taxa identified from the stomach contents of the four
most common piranhas from the Cao Caicara area, Apure River drainage,
in the low Llanos of Venezuela 80
5-3 Food items of Serrasalmus irritaus from the Apure River drainage (Cao
Caicara area) by size class 81
5-4 Food items of Serrasalmus medinai from the Apure River drainage (Cao
Caicara area) by size class 83
5-5 Food items of Serrasalmus rhombeus from the Apure River drainage (Cao
Caicara area) by size class 84
5-6 Food items of Serrasalmus elongatus from the Apure River drainage (Cao
Caicara area) by size class 86
5-7 Food items of Serrasalmus altuvei from the Apure River drainage (Cao
Caicara area) by size class 88
vii


Kirk Wmemiller. I am particularly grateful to Donald C. Taphom for providing both a
home and work area in Guanare, and for sharing his knowledge of the Venezuelan fish
fauna. He has always been unselfish in the sharing of fish specimens and field data from
his work in the Orinoco Llanos.
Most of my work in the upper Orinoco resulted from participation in expeditions as
part of a natural resource inventory of southern Venezuela, organized and sponsored by
Corporacin Venezolana Guayana Tcnica Minera (CVG-TECMIN). I thank all those
associated with CVG-TECMIN whose assistance made my work possible, for
administrative and logistic support these include Dr. Femando Susach, Victor Fernandez,
and Pedro Mata. For occasional help in the field, I express my sincere appreciation to
several members of the TECMIN technical staff, Angel Fernandez, Luz'Delgado, Andres
Garcia, Guillermo Fuenmayor, Sandra Giner, and Jesus Santiago. I relied heavily on the
fishing skills of my field assistants and camp workers hired by CVG-TECMIN: Fabian
Morillo, Yovani Aragua, Juan Carlos Castillo, Ambrosio Guayamore, Antonio Gaveln,
and Hilario Bolivar. Assistance in the upper Orinoco was also given by Dr. Basil Stergios,
Carlos Rivas, Carlos Templa, and Mike Dawson; many of the Yanomamo Indians
including Chirino, Pablo and Ramn, Cesar Timanaw, Ramn Pokorai; the Curipaco
Indians Carlos Antonio Guaruya, Eliasa Guaruya, and Eruerto Lpez; and many
individuals whose names I did not record. Together with my field assistants, their intimate
knowledge of the fishes, the rivers, and the forests of the upper Orinoco was invaluable to
me.
I thank Drs. William Fink and Antonio Machado-Allison for identification of
voucher specimens of many of the serrasalmine fishes, and for providing me with their
unpublished key to Venezuelan piranhas. I am also obliged to Dr. Donald Taphom for
identification of fish specimens, and to Dr. Basil Stergios, Gerardo Aymard, and Nidia de
Cuellar for identifying plant material. I thank Darryl Harrison for preparing base maps,
Angelina Licata for the fish drawings used in many of my figures, Kevin Schuck for help
iii


105
materials eaten by four Group FV fish consisted of a small leaf, fine roots, and a small
amount of filamentous algae, while five large adults (>160 mm SL) had fed on an
unidentified flower, a leaf fragment, woody twigs, and some small root fibers.
My samples of Serrasalmus rhombeus from the upper Orinoco did not include
individuals less than 40 mm SL. Juveniles found in the low Llanos frequently take fins, as
is probably true also for young S. rhombeus inhabiting the upper Orinoco. IL/SL ranged
from 0.9 for a 158-mm SL fish, to a high of 1.7 for a 233-mm SL adult.
Serrasalmus manueli Femandez-Yepez and Ramirez 1967
Serrasalmus manueli was the most abundant piranha in many of the blackwater
rivers, such as the Atabapo and the Sipapo. It was also found together with S. rhombeus
in a few of the larger whitewater rivers, including the upper Orinoco main stem and the
Ventuari. Serrasalmus manueli (Fig. 6-1) was the second largest piranha found in the
upper Orinoco basin; individuals over 270 mm SL were fairly common, and one specimen
from the Atabapo drainage was 340 mm SL. The shape of the body is similar to S.
rhombeus. Young are relatively elongate and sharp-snouted, whereas large adults have a
fairly deep, thick body, and broad, powerful jaws. The body of S. manueli has many
elongated vertical and irregularly-shaped dark markings, and black coloring is found along
the base of the caudal fin. Large juveniles and adults have a large, black humeral spot, and
the cheek and breast of adults are sometimes red-orange. The body color of S. manueli
changes from silvery to almost black with age as is true also for 5. rhombeus. However,
like many neotropical fish, those inhabiting blackwaters are darker or more heavily
pigmented than individuals taken in turbid whitewaters. Unique among piranhas, the first
few anterior rays of the dorsal fin have filaments that may be greatly elongated in older
juveniles and adults, but most individuals lose this ornamentation to other fin-eating fishes.
The diet of Serrasalmus manueli has never before been reported. Diets of
specimens from the upper Orinoco are given in Figures 6-2 and Table 6-3. Large S.


CHAPTER 1
INTRODUCTION
Introduction to Piranhas
Piranhas (Characidae: Serrasalminae) are neotropical freshwater fishes found in the
major Atlantic drainages of South America, from 10 North latitude in the Orinoco River
basin of Venezuela and Colombia, through the Amazon basin, and south in the La Plata-
Paraguay-Parana basin to about 35 South latitude. Called caribes in Venezuela, they
comprise a monophyletic group of at least 30 species in the genera Serrasalmus,
Pygocentrus, Pristobrycon and Pygopristis (Fig. 1-1) (Machado-Allison 1983, 1985, Fink
1988). Piranhas possess many unique morphological traits that distinguish them from
other serrasalmines (Machado-Allison 1985), but they are most easily recognized by their
unusual and impressive dentition. They have a single row of sharp, somewhat triangular
teeth in both jaws; the teeth are tightly packed, partially interlocking, and are typically used
for rapid puncture and shearing.
Examples of other serrasalmine fishes are species of Mylossoma, Myleus, and
Metynnis (silver dollars, pmpanos, palometas), the scale-eating characin Catoprion ment,
and the nearly one-meter long Piaractus brachypomas (morocoto) and Colossoma
macropomum (cachama or tambaqui). In contrast to the piranhas, the dental morphologies
of other serrasalmine fishes are variable. Most species have combinations of relatively
broad and strong molariform and incisive teeth, often with more than one row of teeth in
the upper jaw. Serrasalmine fishes are laterally compressed and most are fairly deep
bodied; however, maximum adult size, body shape, and color patterns vary among species.
Piranhas range from medium-sized fishes such as Serrasalmus irritans, some 20 cm from
1


157
forested upper Orinoco drainages where plant foods, especially fruits and seeds, are an
abundant and fairly reliable resource; and carnivorous species should predominate in the
grassland savannas of the low Llanos where fish biomass is high but plant food availability
extremely seasonal and therefore a less dependable resource.
Low Llanos versus Upper Orinoco
During this study, eleven piranha species were recorded from the two regions of the
Orinoco River basin: ten from the low Llanos, and eight from the upper Orinoco. Seven
species were found to inhabit both regions. Thus, even though the Llanos and upper
Orinoco have very different vegetation, they are very similar in their overall piranha species
composition. The high similarity in species make-up suggests that, in terms of piranhas,
there are really no distinct savanna versus forest species assemblages. These results at first
seem contrary to the already mentioned possibility that piranhas are distributed based on
their feeding preferences (i.e., carnivorous species in the Llanos and herbivores in the
upper Orinoco). However, a few exceptions to the prevailing species overlap should be
noted. Four of eleven species were limited to one or the other region: Pristobrycon species
is a seed-eating piranha known only from forested blackwater habitats of southern
Venezuela: and Orinoco Serrasalmus elongatus, S. irritans, and S. medinai, all highly
carnivorous, were taken only in the Llanos.
My findings on the relative abundance of species in the two regions suggested
patterns not evident from analysis of presence-absence data alone. Several species are
much more common in one region than the other. These differences were associated, in
part, with differences in food resources. For example, the seed-eating S. cf. eigenmanni
was rare in samples from the Llanos but common in several drainages in the upper Orinoco:
the carnivorous Pygocentrus caribe is abundant throughout much of the Llanos but
uncommon in the upper Orinoco. Overall, herbivorous species were only really common


Table l-l--contnued.
Basin
(State, Country)
Site
Habitat
Study Period and
Duration
Species
No. Examined
(Size range)
Comments
Source
15. Orinoco
(Apure,
Venezuela)
Apure drainage,
savanna streams,
pools, flooded
savanna; cattle
ranch
Intermittent from
1979 to 1986, all
months sampled
1) Pygocentrus caribe*
2) Serrasalmus medinai*
3) S. irritans
4) S. rhombeus
5) S. elongatus
6) S. altuvei
7) Pristobrycon striolatus
Unidentified juveniles
n = 516 (20-280)
n = 124 (31-150)
n = 271 (22-162)
n = 51 (20-235)
n = 42 (23-175)
n = 10 (55-155)
n= 16 (21-159)
n= 114(10-19)
Ontogenetic changes in diet,
smallest fed on microcrustaceans,
most large juveniles ate fins,
adults were mainly piscivores.
Plant material not important in
diet (see Chapter 5)
Nico and
Taphorn (1988)
(see Chapter 5)
16. Amazon
(Amazonas,
Brazil)
lower Rio Negro
beaches, lakes,
swamps, flooded
forest
Intermittent 1979
to 1987
Six piranha species (not
identified)
n = 392 ?
(size range not
given)
Part of larger study, piranhas fed
on fish and plant matter
Goulding et al.
(1988)
17. Orinoco
(Portuguesa,
Venezuela)
Apure drainage
small seasonal
stream; cattle
ranch
~ 12-month
1984
1) Pygocentrus caribe*
2) Serrasalmus medinai*
3) Serrasalmus rhombeus
4) Serrasalmus irritanss
n = 230 (20-200)
n = 68 (20-80)
n = 50(20-200)
n = 76 (20-150)
Piranhas taken 8 of the 12
months, mostly juveniles.
Ontogenetic changes in diet
documented
Winemiller
(1989a)
18. Paran
(Mato Grosso,
Brazil)
Pantanal region
Paraguai drainage
Clearwater pools
and creeks:
Intermittent from
1981 to 1989,
mostly during wet
season
1) Serrasalmus marginatus
2) S. spilopleura
3) Pygocentrus nattereri,
n = 13 (63-146)
n = 26 (64-160)
n = 24 (80-240)
Stomach contents presented and
detailed underwater observations
totalling 314 hours
Sazima and
Machado (1990)
19. Orinoco
(Apure,
Venezuela)
Apure drainage
small seasonal
stream; cattle
ranch
24-hour period,
August 4-5, 1988
wet season
1) Pygocentrus caribe*
n = 123 (40-68)
24-hour diel study of juvenile
feeding; fed mostly on small fish
and aquatic insects, peak feeding
in morning
Nico (1990)


162
Given the complex situation of various water types superimposed onto both
savanna and forested regions, excepdons to any generalizations can be found.
Nevertheless, although additional studies are needed, some general trends are apparent that
are obviously important in understanding the trophic ecology of serrasalmine fishes. On
average, it seems safe to assume that aquatic primary production is greater in the Llanos
than in the upper Orinoco (see Saunders and Lewis 1988), and is greater in white water
than in either blackwater or Clearwater situations (Fittkau et al. 1975, Saunders and Lewis
1988, Goulding et al. 1988). Of course, white waters are much more common in the
Llanos than in the upper Orinoco. Furthermore, my observations indicate that white waters
in the upper Orinoco are less turbid and correspondingly less productive than those of the
Llanos. In any case, South American fishes inhabiting highly productive waters feed more
on autochthonous foods (e.g., aquatic insects, fishes, and so on), whereas fishes
inhabiting nutrient-poor waters depend more on allochthonous material for food (e.g.,
fruits, seeds, leaves, and terrestrial and arboreal insects).
Historical Perspective
It is interesting to speculate as to what effects past climatic changes might have had
on the distribution and abundance of piranhas and other serrasalmine fishes. Herbivorous
serrasalmine fishes existed more than 15 million years ago during the Miocene, long before
the start of the Quaternary (Lundberg et al. 1986). As described in Chapter 2, the
equatorial lowland regions of South America experienced dryer and hotter climates during
major glaciations resulting in an expansion of savanna and open-land environments.
Because humid forests would have contracted in size, herbivorous serrasalmines would
either have had to adjust to changes in food, or been forced either to retreat to the remaining
forested regions or to maintain close ties to rivers with large gallery forests. On the other
hand, interglacial or pluvial periods were wetter and relatively cooler, contributing to the
expansion of humid forests, a situation clearly favoring herbivorous fishes.


young piranhas is common in both the low Llanos and the upper Orinoco. Chemical
analysis indicated that fins are similar to scales in energy and protein content, but less than
that of small whole fish. Orinoco piranhas > 80 mm SL fall into two general dietary
categories: species that are primarily carnivorous and others that are largely herbivorous.
The seven carnivorous piranhas (Pygocentrus caribe, Serrasalmus altuvei, S. manueli, S.
rhombeus, S. elongatus, S. irritans, and S. medinai) feed heavily on fish or fish fins.
Adults of the four herbivorous species (.Serrasalmus cf. eigenmanni, Pygopristis
denticulatus, and two Pristobrycon spp.) are seed predators, biting seeds and hard fruits
into small fragments before ingesting them. Serrasalmus manueli was one of the few
carnivorous species that occasionally took seeds or fruit in mass. Overall, relative intestine
length differed among serrasalmine species and was closely correlated with diet Seed
eating piranhas tended to have long intestines, similar to those of highly herbivorous
Myleus, Mylossoma, and Metynnis species, but I found no significant difference in relative
intestine lengths between forest and savanna populations of S. manueli even though diets
differed.
Both carnivorous and herbivorous species are somewhat flexible in their use of
food resources. I found that upper Orinoco piranhas, at both the group and species levels,
exploit plant material more than piranhas from the low Llanos. Many piranhas, especially
those that are largely herbivorous, shift their diets in response to spatial as well as temporal
variation in the availability of fish prey versus plant food. Even though savanna and forest
regions have a similar piranha species makeup, herbivorous species are much more
common in forested regions. Nevertheless, even though seeds and fruits are a locally
abundant resource, assemblages of forest piranhas were typically dominated by one or two
large, highly carnivorous species (5. rhombeus, S. manueli, or both).


51
/=1
Diet breadth (B) = 1/
n
where P is the proportion of food category i in the diet. B ranges from 1, when one
resource state is used exclusively, to n (the total number of food categories recognized),
when all resource states are used in equal proportion. This measure is the reciprocal of
Simpson's index of diversity (Krebs 1989).
I used the Schoener Overlap Index (Schoener 1970) to estimate the similarity in
diets between and within species. This particular index is also known as the Renkonen
Index, the Percent or Proportional Similarity Index, Percentage Overlap, and
Czekanowski's Index (Krebs 1989); the Bray-Curtis Coefficient gives the same results as
the above index if its scores are standardized (Boesch 1977:26, Bloom. 1981). The
Schoener Overlap Index is calculated as:
= 1
Overlap = 1 0.5 ( 2, \ pxi py¡ | = Y, (minimum p*/, Pyi),
n n
where pxi is the proportion of food category i in the diet of species x, pyi is the proportion
of food category i in the diet of species y, and n is the number of food categories. The
Schoener Index gives values from 0 to 1 (or 0 to 100%) indicating no overlap to complete
similarity in the proportion of food categories used by the two groups compared.
There are many indices available for estimating niche or diet width and overlap, but
as yet there is no general consensus as to which of the many indices is best (Hurlbert 1978,
Abrams 1980, Wallace 1981). Recent reviews of frequently used indices include Ludwig
and Reynolds (1988) and Krebs (1989). All measures of breadth and overlap are biased in
some way, the bias usually being reduced with increasing sample size (Schluter 1988,
Krebs 1989). It has also been shown that measures of breadth and overlap are sensitive to
the number of resource categories used. Although lumping resource states can inflate niche


202
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Table 4-4. Summary of species occurrence by habitat and water type, based on samples in Orinoco River basin, Venezuela. Physico
chemical data represent minimum-maximum values recorded for water at capture sites. Transparency measured with Secchi disk.
Species
Habitat Type
Water Type
Physico-Chemical Ranges
Big
River
Stream
Lagoon/
Oxbow
Flooded-
forest
Flooded-
savanna
While
Clear
Black
pH
Temperature
(C)
Transparency
(m)
Pygocentrus caribe
X
X
X
X
X
X
X
X
6-7
26-30
0.1->2.0
Pristobrycon striolatus
X
X
X
X
X
X
X
6-6.7
27.5-30.5
0.5-1.0
Pristobrycon sp.
X
X
X
4.5
27
~2
Pygopristis denticulatus
X
X
X
X
4.5-6
26-38
1-2
Serrasalmus altuvei
X
X
X
X
X
6-7.2
24.5-31
0.1-1.0
Serrasahnus cf.
X
X
X
X
X
X
X
6-7
25-33
0.5-0.9
eigenmanni
Serrasalmus elongatus
X
X
X
X
X
6-6.5
29-29.5
0.1->2.0
Serrasalmus irritans
X
X
X
X
X
X
6-7
27-29.5
0.1->2.0
Serrasalmus manueli
X
X
X
X
X
X
X
4.5-6.5
24.5-31
0.7-2.3
Serrasalmus medinai
X
X
X
X
X
X
6-7
27-33
0.1-1.0
Serrasalmus rhombeus
X
X
X
X
X
X
X
6-7.2
24.5-31
0. l->2.0
Note: Physico-chemical parameters not measured at all sites, therefore ranges given in many cases are probably conservative.
-J
o


43
habitat (grassland, savanna, gallery forest, or forest); (8) dominant riparian vegetation
(none, grasses/forbes, shrubs/trees, narrow forest border, or forest); (9) water depths at
site and capture depths (very shallow [0-5 cm], shallow [5-20 cm], moderate [20-50 cm],
deep [50-100 cm], very deep [100-150 cm], extremely deep [>150 cm]); (10) water
velocities, as measured with a mechanical flowmeter (General Oceanics) or using a floating
stick or cork, were classified into six categories (zero [<0.02 m/sec], very slow [0.02-0.10
m/sec], slow [0.10-0.25 m/sec], moderate [0.25-0.75 m/sec], fast [0.75-1.25 m/sec], and
torrential [>1.25 m/sec]); (11) water temperature; (12) water pH measured with a Hach pH
Pocket Pal meter or a Hach colorimetric (color disc) wide range pH test kit (Model 17-N);
(13) water color and turbidity (very-clear, clear-tannin, clear-green, slightly-turbid,
moderately turbid, or very turbid); (14) water clarity as measured with a 20-cm diameter
Secchi disk; (15) estimated maximum and average water width; (16) degree of shading (full
sun, partial shade, temporary full shade, permanent full shade).
Substrate types and types of aquatic or instream cover for each collecting site were
recorded by estimating their proportion of the total surface area: (0)=none/few; (1)<10%;
(2)10-50%; and (3)>50%. Substrate types recognized were: silt/mud; sand; gravel;
rubble; boulder; bedrock/claypan; vegetation; litter; and detritus/decomposed organics.
Fish cover categories recognized were: floating aquatic vegetation: emergent vegetation;
submergent vegetation; litter on bottom; overhanging vegetation; undercuts; bank cover;
brush/roots; rocks; logs; and artificial structures (e.g., culverts, bridge piers).
Identification and Nomenclature of Piranhas
At least 12 species of piranha occur in the Orinoco River basin (personal
observation). As with most groups of South American freshwater fishes, there has been a
great deal of confusion surrounding the classification and nomenclature of the subfamily
Serrasalminae, due to a combination of factors. Some species exhibit marked changes in


Table 6-7. Food items of Pygopristis denticulatus from the upper Orinoco River basin by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %V = percent volume. N = 25.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
1(10-19)
4
0
%D
%v
%o
II (20-39)
20
0
%D
%V
%0
V (>160)
1
0
%D
%v
Masticated seeds
-
-
-
-
-
-
100.0
100.0
96.8
Plant material
-
-
-
20.0
-
1.7
-
-
-
Microcrustaceans
100.0
-
15.2
5.0
5.0
3.7
-
-
-
Aquatic insects
100.0
100.0
84.8
95.0
95.0
94.1
-
-
-
Other invertebrates
-
-
-
5.0
-
0.7
100.0
-
1.6
Fish scales
-
-
-
-
-
-
100.0
-
1.6
Other
-
-
-
5.0
-
<0.1
-
-
-


47
(7) Serrasaimus rhombeus (Linnaeus) 1766: Serrasalmus rhombeus in Nico and
Taphom (1988) and Winemiller (1989a, 1989b); and color illustration in Nico and Taphom
(1986:40-41).
(8) Pygocentrus caribe Valenciennes 1849: Pygocentrus notatus in Taphom and
Lilyestrom (1984), Nico and Taphom (1988), Winemiller (1989a, 1989b), Nico (1990);
color illustrations are given as P. notatus in Nico and Taphom (1986:31, 40, 41), photos
reproduced as Serrasalmus (Pygocentrus) notatus in Schulte (1988:109, 110), as
Serrasalmus niger in Schulte (1988: 111), and as Serrasalmus natter eri (incorrect locality
given) in Schulte (1988:12-13).
(9) Pristobrycon striolatus (Steindachner) 1908: Pristobrycon striolatus in Nico
and Taphom (1988); color illustrations as Pristobrycon striatus in Nico and Taphom
(1986:31,41), and as Pygocentrus striolatus in Nico and Taphorn (1986:33), photo
reproduced in Schulte (1988:120). Machado-Allison et al. (1989) concluded that
Pygopristis antoni Fernndez-Ypez, 1965 is a junior synonym of P. striolatus.
(10) Pristobrycon sp.: This species is in the process of being described as new by
W. Fink and A. Machado-Allison.
(11) Pygopristis denticulatus Muller and Troschel 1844: photograph as
Serrasalmus (Pygopristis) antoni in Romn (1983:51).
Faunal Comparisons
The Coefficient of Biogeographic Resemblance (CBR) proposed by Duellman
(1990) was used to compare the composition of piranha assemblages between the two
regions studied and among the different drainages. This qualitative index of similarity has
been reinvented a number of times, consequently it is known by several names including
the Faunal Resemblance Factor, the Sorenson Index, and the Dice Coefficient (Boesch
1977, Romesburg 1984, Magurran 1988, Duellman 1990). This index is one of the more


69
microhabitats where there was high cover provided by herbaceous plants. In the Llanos,
small piranhas relied on water hyacinth or flooded grasses for shelter and as a foraging
place. In the upper Orinoco, young juveniles were limited to a few sites where there were
mats of flooded grasses (e.g., stream edges) or shallow waters with dense growths of
submergent plants, such as beds of the aquatic plant Elodea.


Fig. 5-1. Location of Cao Caicara study area, Apure Drainage, in low Llanos of Apure State, Venezuela. (Arrow indicates
Fernando Corrales ranch and research station of UNELLEZ).
to


171
Axis of Habitat Variables
Forest Habitat < > Savanna Habitat
Wet Season < > Dry Season
High Water < > Low Water
Low Perturbation < > High Perturbation
Low
Relative
Amount of
Fish
in Diet
High
High Plant Material < > Low Plant Material
Low Fish Prey < > High Fish Prey
Axis of Food Availability
Fig. 8-1. Proposed hypothetical model showing the dietary responses of carnivorous
versus herbivorous piranha species to changes in various habitat parameters and
food resources. Dashed vertical line indicates the condition where both plant
material and prey fish are in approximate equal supply and relatively abundant
(see Table 8-1 for list of piranha species involved).


APPENDIX A
MATERIAL EXAMINED
Specimens examined are deposited at the Museo de Ciencias Naturales (MCNG) at
UNELLEZ, Guanare, Venezuela, and the Florida Museum of Natural History (UF),
Gainesville, Florida. Catalogued specimens are designated by MCNG or UF numbers and
uncataloged specimens by field collection numbers (PIMA, DCT or LN). Total number of
fish in that series and number of specimens in which gut contents were examined, or
intestine measured, is given in parentheses. Small juveniles (jv) are specimens less than 20
mm Standard Length.
Pristobrvcon strinlatus
Llanos
Apure River drainage: Cao MaporaL-1980: MCNG 9102 (1-0); MCNG 11373
(1-0). 1981: MCNG 9178 (2-0); MCNG 10127 (1-0); MCNG 10247 (6-3); MCNG
11371 (8-5); MCNG 11372 (5-3). 1983: MCNG 10073 (2-1). 1984: MCNG 11347 (6-
2); MCNG 11360 (5-1); MCNG 15736 (1-1?). 1985: MCNG 11511 (2-1). 1989:
MCNG 19454 (1-1).
Cinaruco River drainage: 1986: MCNG 1793 (1-1). 1987: MCNG 17157 (4-4).
1989: MCNG 21805 (1-1); MCNG 20018 (1-1);
Capanaparo River drainage: 1989: MCNG 20283 (4-4);
Other: 1987: MCNG 17387 (2-2).
181


CHAPTER 8
DISCUSSION AND CONCLUSIONS
In this work, I have attempted to describe the diets and trophic ecology of piranhas
from contrasting environments of the Orinoco River basin. The main questions addressed
in this study are: (1) Do the same species of piranhas occur in both savanna and forested
regions? (2) Do diets differ, and, if so, are fish from populations in forested habitats
significantly more herbivorous than their savanna counterparts? (3) How do ontogenetic
changes in diet compare among species and do they correlate with regional environments?
(4) Is intestinal length of piranhas and other serrasalmine fishes correlated with diet?
(5) What are the nutritional benefits associated with different diets or food preferences?
(6) How do diets of piranhas compare with those of other serrasalmine species? (7) What
is the relationship between piranha ecology and serrasalmine phylogeny? In this final
chapter, I briefly reexamine these questions in view of my results and I speculate on the
findings in relation to mechanistic, ecological, and evolutionary issues.
Composition of Piranha Assemblages
It it difficult to determine with certainty the precise effect ecological conditions have
had on current piranha abundance and distribution patterns. Gilbert (1980) considered both
historical and ecological elements as being equally important in interpreting the
geographical distributions of most freshwater fishes. Along these same lines. Burr and
Page (1986) suggested that similarities in fish faunal compositions among North American
streams were dependent upon several factors, for instance drainage size and proximity,
155


Coefficient of Resemblance (CBR)
66
Distance between drainage pairs (km)
Fig. 4-4. Scatter diagram showing similarities in piranha species composition between all
possible paired drainages and the distance between paired drainages. Similarity
values and distances are from Table 4- 2.


Fig. 2-2. Major savanna (hatched) and forest (shaded) ecosystems in the Orinoco River basin
to
Lh


117
SL) taken from a shallow, blackwater oxbow lake covering several hectares in the forested
floodplain of the Mavaca River; several additional fish were transported alive for later
observation. The species is the only representative of the genus Pygopristis, and closely
resembles Pristobrycon striolatus in both body form and markings. Pygopristis
denticulatus is the only piranha with five cusps (pentacuspid) on the jaw teeth, whereas
adults of all other piranhas have only three (tricuspid) (Machado-Allison 1985). The body
is deep, the snout is somewhat rounded, and the jaws are relatively small compared with
that of S. rhombeus. The body is typically silvery and sometimes dark, and parts of the
cheek and breast, as well as most fins, are red-orange. Juveniles are silvery, and parts of
unpaired fins are reddish orange. From about 25 mm SL, the sides are marked by a series
of about ten brownish, vertical bars, narrow and somewhat irregularly shaped; the bars
become faint with age. Unpaired fins are marked with a thin, blue-white terminal border.
Results of stomach content analysis are given in Figure 6-2 and Table 6-7. The
stomach of the single adult examined was full of masticate,! seeds (96.8% by volume)
along with a few fish scales (1.6%) and the remains of two small invertebrate larvae
(1.6%) (Fig. 6-2). L/SL was 1.9. I examined the stomach contents of 24 of the 80
preserved juveniles (Table 6-7). Both Group I (Fig. 6-3) and II (Fig. 6-2) had fed heavily
on aquatic insects, mostly chironomid and ephemeropteran larvae, and odonata nymphs.
Upon reaching a SL of about 40 mm SL a single juvenile that had survived in an aquarium
began stalking and chasing other fishes and clipping out pieces of fins.
Other Serrasaimine Fishes
In addition to piranhas, there are several other genera of the subfamily
Serrasalminae that occur in the upper Orinoco basin. Catoprion, a monotypic genus, is a
fin eater widely distributed in South America. All other genera of serrasaimine fishes, a
group in dire need of taxonomic revision, are primarily herbivores and all have relatively


167
on occasion by adult piranhas, mostly terrestrial and flying insects, and shrimp and crabs.
Braga (1954) reported that shrimp were the main prey of adult Serrasalmus rhombeus
inhabiting a man-made lake.
5) Seed Predators. Many serrasalmine species feed on seeds and the hard parts
surrounding the seed (mainly endocarp). The term "seed predator" was used by Goulding
(1983) to refer to fishes that destroy seeds by mastication or other digestive processes.
This is in contrast to several other basically herbivorous serrasalmids (most often
Colossoma macropomum and Piaractus brachypomus) which, in addition to masticating
seeds, occasionally act as seed dispersal agents by swallowing and passing whole seeds
(Gottsberger 1978, Goulding 1980, 1983, personal observation). Four piranhas
representing three genera (Table 8-1) were largely herbivorous and all were primarily seed
predators. Myleus species from the upper Orinoco also sometimes feed on seeds that they
bite into small fragments. Llanos piranhas rarely eat seeds, but seed predation was
common among piranhas in all six upper Orinoco drainages. Goulding et al. (1988)
reported that Myleus switch from seed-eating to folivory during low water when fruits and
seeds are in shorter supply, this may be the case with Orinoco Myleus as well (see next
section on folivores), but I found that herbivorous piranhas continued to feed on seeds
even during the dryer season. Herbivorous fishes are known to gather around trees that are
dropping their fruit (Goulding et al. 1988). A few carnivorous serrasalmine species are
somewhat territorial (Sazima 1988, personal observation). Like their carnivorous relatives,
herbivorous piranhas can be very aggressive at times and it is conceivable that they
maintain feeding territories around fruiting trees during the low water season, driving away
other herbivorous fishes that might compete for a limited number of seeds.
Several authors list examples of the seeds and fruits eaten by various South
American fishes, including a few serrasalmine species (Gottsberger 1978, Goulding 1980,
Smith 1981, Goulding et al. 1988). I was unable to identify the crushed seeds found in the
stomachs of Orinoco piranhas, but a large Piaractus (560 mm SL) from the upper Orinoco


20
The headwaters of the Orinoco are traditionally considered to be in southern
Venezuela where it receives water from both the western slopes of the Guyana Shield and
from extensive lowland areas dominated by deciduous or evergreen tropical forest. In
contrast, most tributaries in the northern and western parts of the basin originate in the
Andes and adjoining coastal mountains and then flow through the Llanos, a vast alluvial
plain supporting tropical savanna vegetation. The main channel of the Orinoco forms an
unusual U-shaped pattern, the river winding around the western borders of the Guyana
Shield. From its source the Orinoco flows several hundred kilometers west-northwest until
it is met by the Atabapo and Guaviare rivers; here the river makes an abrupt turn to the
north. Along its northward segment the Orinoco forms the border between Colombia and
Venezuela.
At about 530'N latitude the river courses through several series of treacherous
cataracts near Puerto Ayacucho, the most prominent being the Atures Rapids where the
river drops 17.5 m over a distance of 9.3 km (CODESUR 1979). The Atures Rapids and
the other cataracts are spread along a reach of nearly 100 km, marking the boundary
between the upper and lower sections of the Orinoco. Farther downstream the Orinoco is
joined from the west by the Meta, Cinaruco, Capanaparo, and Apure rivers as it gradually
swings to the east. Finally, below the confluences with the Caura and Caroni rivers the
Orinoco arrives at its large delta. Here the huge main river is subdivided into a multitude of
smaller channels that empty into the Atlantic Ocean near the island of Trinidad. The main
causeway of the Orinoco, from its origin in the Sierra Parima in the Guyana Shield to its
mouth, is estimated to be 2,140 km long (DISCOLAR 1983). High-order tributaries
draining highland areas of the Andes and the Guyana Shield are characterized by large
numbers of waterfalls, rapids, and fast-flowing waters. However, the larger streams and
rivers common to lowland areas typically have slight gradients. The upper Orinoco, at the


Fig. 6-1. Eight piranha species from the upper Orinoco River basin of Venezuela.
Sm = Serrasalmus manueli, Sr = S. rhombeus, Seg = S. cf. eigenmanni,
Sa = S. altuvei, Pst = Pristobrycon striolatus, Pc = Pygocentrus caribe,
Pyp = Pygopristis denticulatus, and Psp = Pristobrycon sp.


Fig. 3-2. Map of Apure State, Venezuela, showing principal low Llanos sampling sites. Solid circles represent localities
sampled by the author; solid squares represent areas collected by others (specimens from all sites deposited at
MCNG and examined by the author). Each symbol may represent more than one sampling site.


152
There have been no previous studies of the nutrient content of fins as relates to fin-eating
fishes. My results show that the energy and protein content of fins and scales are very
similar, about 10 kj/g and approximately 34% protein (Table 7-1, Fig. 7-1). Like scales,
the fins of fishes are covered with protein-rich mucus; similar to scales they probably also
contain a significant amount of calcium phosphate.
Fish and Fish Flesh
Many adult piranhas prey heavily on fishes, either biting out chunks from larger
fishes, sometimes as carrion, or taking small fish whole or almost whole. Compared with
feeding only on fins or scales, the nutrient advantages of such behavior are obvious
because the predator gets a combination of fins, scales, and flesh. The energy, protein,
and lipid contents of entire small fish are higher than those of either fins or scales (Table 7-
1, Fig. 7-1). Smith (1981:90), citing Junk (1977), presented a list of the fat, protein, and
ash content of 21 medium and large-sized Amazonian food fishes from a floodplain lake at
low water. Protein (12.4 to 20.2%) and ash (1.0 to 5.2%) contents did not vary much;
however, fat content showed wide variation among species, ranging from 0.2 to 28.8%.
Fat contents also show seasonal differences since many species accumulate fat after feeding
during the high-water season (Smith 1981). My values for small prey fishes showed a
much higher protein content (51.5%) and ash content (33.5%) than Smith reported for
large fishes, with a fat content (6.5%) within the lower part of his reported range.
Arthropods
Insects and other invertebrates are some of the richer foods in terms of nutrient
value per mass. Bell (1990) reported that the dry mass composition of an average insect is
59.5% protein, 15.5% fat, 5.0% ash and 7.2% carbohydrate, and yields approximately 22
kJ/g dry mass through combustion. Ranges of 5.3 to 85.4% fat, and 12 to 29.7% kJ/g
were reported, with highest values often associated with larval forms (Cummins and


82
It was usually not possible to identify the fins eaten, but the thick red anal fins of
Pygocentrus caribe were found in two individuals. Large S. irritans preyed mostly on
small whole fish, fish flesh, fins, and occasionally scales. Fishes eaten whole or in pieces
by S. irritans are given in Table 5-2. A small juvenile P. caribe was found in the stomach
of one individual. No nonfish vertebrate remains were found.
Serrasalmus medinai Valenciennes 1849
Serrasalmus medinai was the third most common piranha in the study area; 124
specimens were analyzed for diet (Table 5-4 and Fig. 5-3). It is a medium-sized piranha,
usually less than 160 mm SL with a head shape that is intermediate between the robust P.
caribe and species with pointed snouts (Fig. 5-2). Unlike Pygocentrus, but similar to
other Serrasalmus, it has a series of ectopterygoid teeth that is easily seen even in small
individuals (from about 25 mm SL). It is primarily a fin-eater when small (20-79 mm
SL). The largest individuals (Group IV) fed chiefly on fish flesh, fins and scales, and
small whole fish. Prey fish identified from the stomachs of S. medinai are given in Table
5-2. The only fin identified was from an armored catfish. Shrimp and crabs were also
eaten.
Serrasalmus rhombeus (Linnaeus) 1766
Serrasalmus rhombeus was uncommon in flooded savanna of the Cao Caicara
study area, although on several occasions adults were taken in large numbers by hook and
line at night in Cao Maporal. Juvenile Serrasalmus rhombeus have a somewhat elongate
body and sharp snout (Fig. 5-2). They resemble S. irritans in body form, but are slightly
more robust. Adults have heavy rhomboidal bodies. The body and fins of large
individuals, some well over 300 mm SL, are black or blue-black, and the iris is often deep
red. I examined the stomach contents of 51 S. rhombeus from the Cao Caicara area
(Table 5-5 and Fig. 5-3).


112
(Table 6-5 and Fig. 6-2). Fins were the most important food item, accounting for 63.9%
of total food volume; scales were second in importance, 25.9% by volume. IL/SL ratio
(n = 8) ranged from 0.65 to 1.02 (mean = 0.87).
Pygocentrus caribe (Lutken 1874)
Although it was the most abundant piranha in many fish communities in the low
Llanos, Pygocentrus caribe was uncommon in samples from the upper Orinoco, and was
restricted to more lentic habitats such as abandoned river meanders and floodplain lakes.
Pygocentrus caribe (Fig. 6-1) is a robust, heavy-bodied species with broad and powerful
jaws; individuals reach about 300 mm SL. The body is silvery, and the cheek and venter
are often bright reddish orange, usually with a prominent black humeral spot. Based on
observations of P. caribe collected in other parts of Venezuela, the body and fins of large
adults in breeding condition turn almost black.
My samples showed that Pygocentrus caribe is primarily a piscivore. Examination
of stomach contents of 11 specimens (135-235 mm SL) from the upper Orinoco (Fig. 6-2)
indicated that fish flesh was the main prey in terms of frequency of occurrence, volume,
and dominance. Food items were as follows (%0-%D-%V): Group IV (n=3)-other
invertebrates (66.7-0-0.7), fish flesh (100.0-100.0-88.4), fish fins (66.7-0-8.3), fish
scales (66.7-0-2.7); Group V (n=8, 3 empty)-plant material (80.0-40.0-9.4), fish flesh
(80.0-60.0-71.8), fish fins (20.0-0-0.7), fish scales (20.0-0-15.5), other (20.0-0-2.7).
Plant material consisted of leaf fragments and woody material, which most likely was taken
incidental to attacking or ingesting other prey. No small juveniles of P. caribe were found
in the upper Orinoco. IL/SL was low, ranging from 0.7 to 1.4 for the 11 specimens
examined.


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Ecology Progress Series 5:125-128.
Boesch, D. F. 1977. Application of numerical classification in ecological investigations of
water pollution. EPA-600/3-77-033. U.S. Environmental Protection Agency,
Corvallis, Oregon. 115 pp.
Bohlke, J. E., S. H. Weitzman, and N. A. Menezes. 1978. Estado atual da sistemtica
dos peixes de gua doce da Amnca do Sul. Acta Amaznica 8(4):657-677.
Bonetto, A., C. Pignalberi, and E. Cordiviola. 1967. Las "palometas" o "piraas" de las
aguas del Paran medio. Acta Zoolgica Lilloana (Tucuman, Argentina) 23:45-65.
Braga, R. A. 1954. Alimentagao de pirambeba, Serrasalmus rhombeus (L., 1766)
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198


page
Figure
6-8 Comparison of the proportion of plant material in the diets of carnivorous
and herbivorous piranha species (> 80 mm SL) from the low Llanos to
those from upper Orinoco River drainages in terms of percent adjusted
volume (%Va), percent dominance (%D), and percent frequency of
occurrence (%0) 138
6-9 Diets by size class (>40 mm SL) of Serrasalmus manueli comparing low
Llanos (Cinaruco drainage) and upper Orinoco populations 141
6-10 Scatter diagram showing relationship between mean intestine
length/standard length and percent volume of plant material in diet for
selected serrasalmine fish (>80 mm SL) 145
6-11 Scatter diagram showing relationship between intestine length and standard
length for the three most common piranha species in samples from the upper
Orinoco River basin of Venezuela 146
6-12 Scatter diagram showing relationship between intestine length and standard
length for Serrasalmus manueli comparing upper Orinoco and Llanos
populations 146
7-1 Bar graph comparing dry mass composition of small whole fish, scales and
fins 150
8-1 Proposed hypothetical model showing the dietary responses of carnivorous
versus herbivorous piranha species to changes in various habitat parameters
and food resources 171
8-2 Diets and intestine length mapped onto the proposed phylogeny of
Machado-Allison (1985) for genera of the subfamily Serrasalminae 179


S.L. (mm) MYLEUS
ASTERIAS
MYLEUS
SCHOMBURGKII
MYLEUS
TORQUATUS
CATOPRION
MENTO
80-159
>160
n=6 (1.04)
n=3 (1.08)
n=20 (2.24)
Masticated Seeds
\ \ N '
/ / /
S \ S '
/ *
\ \ \ '
Aquatic Insects
Fish Fins
Leaves/Flowers
Other Invertebrates
Fish Scales
Other Plant Material
Fish Flesh
Other ^


72 70 68 66 64 62 60
Fig. 3-1. Map of Venezuela showing nine selected drainages in Orinoco River basin sampled during present
study. Low Llanos rivers: (1) Apure, (2) Capanaparo, and (3) Cinaruco; Upper Orinoco rivers:
(4) Sipapo, (5) Atabapo, (6) lower Ventuari, (7) Matacuni, (8) Ocamo, and (9) Mavaca.


88
Table 5-7. Food items of Serrasalmus altuvei from the Apure River drainage (Cao
Caicara area) by size class. %0 = percent frequency of occurrence; %D = percent
dominance; and %Va = percent adjusted volume. N = 10.
Size class (mm, SL)
m(40-79)
IV(80-159)
Number examined
3
7
Number empty
0
. 0
Food items
%0
%D
%va
%0
%D
%va
Plant material
-
-
-
28.9
-
-
Small whole fish
33.3
33.3
50.0
-
-
-
Fish flesh
33.3
-
-
42.9
30.0
50.0
Fish fins
66.7
66.7
50.0
71.4
40.0
31.3
Fish scales
-
-
-
42.9
30.0
18.8
Other
_
_
_
14.3
_
_


85
Juvenile S. rhombeus in size classes II-IV specialized on fish fins. Aquatic insects,
mostly plecopterans, were packed in the guts of several specimens from Cao Guaritico.
The ten largest S. rhombeus (Group V) had taken almost equal volumes of whole small
fish, chunks of fish flesh, and fish fins. Fishes identified from the stomachs of larger S.
rhombeus are given in Table 5- 2. Three large S. rhombeus collected at night in Cao
Maporal contained entire or partial individuals of small 20-30 mm SL doradid catfishes.
One individual had eaten a small adult frog.
Serrasalmus elonaatus Kner 1860
Serrasalmus elongatus was rare to uncommon in my samples in the study area. It
is a pikelike piranha (Fig. 5-2), having the most elongate body, relative to body depth, of
all piranhas. I examined 42 individuals, including a few from the small size class (Group
II) from other locations in the Apure River drainage (Table 5-6 and Fig. 5-3). Stomachs of
three small juveniles (20-39 mm SL) were packed with fins of other small fishes, and one
also contained a nematode (possibly a parasite). Stomachs of large specimens contained
fish fins and many scales. In addition, small whole fish and chunks of fish flesh were
taken by the largest S. elongatus.
Serrasalmus altuvei Ramirez 1965
Serrasalmus altuvei was rare in the Cao Caicaia area, and was found in both
streams and floodplain pools. It is a medium-sized piranha; maximum length in my
samples was less than 200 mm SL, with a deep narrow body and a slender pointed snout
(Fig. 5-2). It has a silver body and a broad, black terminal band on its unpaired fins,
none of my specimens from the Apure drainage had any red on the body. I examined the
stomachs of ten of 17 individuals collected in Cao Maporal and the flooded savanna


24
The Low Llanos
The Llanos (Fig. 2-2) are a vast plain of up to 400 km width along the north bank
of the Orinoco, stretching from near the delta mouth westward for over 1,000 km through
Venezuela, far into Colombia (Walter 1973). It occupies about 500,000 km2, is essentially
unbroken by major forests, and is the largest continuous savanna in the neotropics north of
the equator (Sarmiento 1984). A combination of factors, for instance soil type and rainfall
patterns, prevent the establishment of forest in large parts of the Llanos. Dry season fires,
of mostly human origin, are also important in limiting the growth of woody vegetation.
Several systems have been used to divide the Llanos into different categories using
combinations of physical and biological features. In most cases, a distinction is made
between the low Llanos and high or upper Llanos, based on elevation and extent of
flooding during the rainy season (Walter 1973:73, Cole 1986). The low Llanos are
characterized by open grass savannas with fairly level terrain that undergo frequent or
long term flooding during the rainy season. According to Cole (1986:92), savanna
grasslands cover some 150,000 km2 of the low Llanos in the Orinoco basin. Apure State,
in western Venezuela, encompasses a large portion of the low Llanos. Here the terrain is
relatively flat, with elevations of 100 m or less above sea level. In Apure, the landscape is
dominated by herbaceous cover, mainly bunch grasses and sedges, with occasional shrubs
and small trees (Sarmiento 1984, Cole 1986). Most trees, including palms, exist in small
isolated groups (matas) or in gallery forest situations fringing the rivers and larger streams
(Sarmiento 1984, Cole 1986). These gallery forests range from narrow bands, only a few
trees wide, to fairly extensive stands, in some places many hundreds of meters wide, as
seen existing along reaches of the lower Cinaruco and Capanaparo rivers.
The low Llanos of Apure State (Fig. 2-3) comprise a vast open floodplain
containing a diversity of aquatic habitats (Mago-Leccia 1970). All undergo pronounced
seasonal changes. Because of its low elevation and flat physical relief, most of the


61
geographically close (Fig. 4-3, Table 4-2). For instance, the Mavaca and Cinaruco were
somewhat similar in terms of species composition (CBR = 0.73), yet the two drainages are
far apart geographically. Similarly, the Apure drainage had four species in common with
the Ocamo, even though these two rivers are separated by roughly 1000 km of waterway
(Fig. 4-1). As expected, there was a significant negative correlation between species
composition resemblance (i.e., CBR) and the distance between adjacent drainages (rs =
- 0.66, one-tailed P < .05, n = 8; Table 4-2, Fig. 4-3). However, the relationship was
not significant at the 0.05 level when plotting all possible combinations of drainage-pair
distances against their CBR values (rs = 0.23, one-tailed, .10 > P > .05, n = 36; Table 4-
2, Fig. 4-4).
Figure 4-5 summarizes results of a UPGMA cluster analysis showing affinities
among the nine drainages based on CBR similarity values given in Table 4-3. In addition
to similarity in species composition, most resulting groups of drainages were related by
either geographic proximity, characteristics of the drainage (e.g., water type), or some
combination of these two factors. The first major cluster consisted of the three savanna
drainages (Capanaparo, Cinaruco, and Apure) and one upper Orinoco tributary (Ventuari).
The Capanaparo and Cinaruco are adjacent drainages and both were classified as
blackwater, but each receives high input from Clearwater streams. The Apure River is a
whitewater river with many small blackwater and Clearwater tributaries. The Ventuari also
is mainly a whitewater river although it has several large blackwater and Clearwater
tributaries. The second major cluster was formed by three drainages in the upper Orinoco.
This cluster consisted of the Matacuni, Ocamo, and Mavaca; all are whitewater rivers and
geographically close. The remaining two drainages, the Sipapo and Atabapo, did not
cluster with any of the other drainages. They were blackwater rivers with relatively few
piranha species. Clustering based on the farthest neighbor strategy resulted in drainage
groupings identical to that of the UPGMA method.


139
CARNIVORES
HERBIVORES
40-
30-
%D 20'
10-
0-
Low Llanos Upper Orinoco


144
savanna populations (Table 6-10, Figs. 6-8 and 6-9). However, in examining possible
geographic variation in the EL/SL of S. manueli, I found no significant difference in the
slopes of the EL and SL regression lines (F = 0.67, P = 0.4157) between forest and
savanna populations (Fig. 6-12).


Fig. 6-3. Diets of selected small juvenile piranhas (10-19 mm SL) from upper Orinoco River drainages and the low Llanos,
Venezuela. Size of segments represents percentage of volume of each prey type; n = number of stomachs examined;
numbers in parentheses represent diet breadth using formula of Levins (1968).


Table 6-8. Matrix of diet overlaps among different size classes of serrasalmine fishes from upper Orinoco River drainages. Overlap
index is that of Schoener (1970). (SL = Standard Length, see Table 3-1 for species abbreviations).
Species and
Size Range (SL, mm)
SR
40-79
SR
80-159
SR
>160
SM
40-79
SM
80-159
SM
>160
SEG
40-79
SEG
80-159
SEG
>160
PC
80-159
PC
>160
PST
80-159
PST
>160
PSP
>160
PYP
>160
SR 40-79
100
69.75
50.05
88.16
84.05
69.95
20
19.2
14.05
88.25
72.45
18.65
0
0
0
SR 80-159
100
59
80.79
59.91
57.8
31
25.15
22.6
61.4
64.1
25.2
4.95
3.55
3.05
SR >160
100
53.09
52.6
54.5
3.8
20.35
17
53.4
54.5
19.3
2.35
2.85
2.25
SM 40-79
100
74.51
72.79
28.7
21.34
14.09
77.19
71.19
21.71
1.54
1.24
0.84
SM 80-159
100
84.1
4.1
17.66
14.1
86.5
81.8
22.8
4.55
1.45
1.05
SM >160
100
1.4
25.25
23.7
70.9
79.9
30.8
14.35
11.45
11.05
SEG 40-79
100
7.6
1.6
8.3
0.7
6.7
0
0
0
SEG 80-159
100
91.25
22.55
17.15
92.45
75.8
77.7
77.1
SEG >160
100
16.7
22.6
85.4
76.95
78.25
78.05
PC 80-159
100
75.1
19.3
0.5
2.45
2.25
PC >160
100
19.3
4.95
2.15
1.55
PST 80-159
100
76.25
73.55
73.35
PST >160
100
95.9
95.5
PSP >160
100
99.4
PYP >160
100


15
State, Brazil. They reported that heaviest feeding took place during the summer months
with a corresponding heavy build up of body fat by autumn.
Several recent works dealing with piranhas in the Venezuelan Llanos have
documented diet shifts during ontogeny (Machado-Allison and Garcia 1986, Nico and
Taphom 1988, and Winemiller 1989a). All found that early juveniles ate principally
zooplankton, while older individuals were predominantly piscivores. In addition to
discussing ontogenetic changes in dental morphologies, Machado-Allison and Garcia
(1986) examined 134 specimens, mostly juveniles, of three species (Pygocentrus caribe
Pristobrycon striolatus, and Serrasalmus rhombeus) taken from the Camagun lagoon, a
large wetland between the Portuguesa and Apure rivers, Guarico State. Predominant food
items, in terms of frequency of occurrence, of young piranhas were microcrustaceans,
aquatic insects, fins, and scales. In addition, they found small seeds (i.e., Cyperaceae) in
the stomachs of 33 of 134 specimens, but did not provide information on volume and
numbers of seeds eaten. Nico and Taphom (1988) examined the diets of seven piranha
species from streams and flooded savannas in the western Llanos of the Orinoco River
Basin. Their work suggested that savanna piranhas do not depend on fruits and seeds as
had been reported by Goulding (1980) for piranhas in flooded tropical rain forests. Nico
and Taphom found that juveniles and sub-adults of six of seven piranhas from a single
locality fed heavily on fins. Winemiller (1989a) studied the fish community of Cao
Maraca, a seasonal stream in the Apure River drainage that meanders through a region of
wooded savannas used for cattle ranching and cropland in Portuguesa State. His findings
on four piranha species (P. caribe, S. irritaos, S. rhombeus, and S. medinai), mostly
juveniles and sub-adults, supported the earlier work of Nico and Taphom.
For the most part, piranhas have been found to be daytime feeders, usually most
active during twilight periods (Lowe-McConnell 1964, Goulding 1980, Barthem 1987,
Nico 1990, personal observations). Barthem (1987) reported on activity patterns of several
vrzea lake fishes from near Manaus, Brazil. His results, based on -analysis of gillnet


194
Table B-6. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and low Llanos 5.
manueli (n = 20).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
1857.851
1857.851
0.815
0.3696
SL
1
1147080.511
1147080.511
503.084
0.0001
Species x SL
1
1527.190
1527.190
0.670
0.4157*
Residual
76
173287.427
2280.098
^Conclude that slopes of regression lines are not different at 0.05 level of significance,
therefore eliminate interaction effect (see Table B-6) to see if y-intercept is the same..
Table B-7. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and low Llanos S.
manueli (n = 20) while eliminating interactive effect (i.e., adjusting for differences in
SL).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Population
1
336.248
336.248
0.148*
0.7014*
SL
1
1481368.833
1481368.833
652.493
0.0001
Residual
127
174814.617
2270.320
* Adjusting for differences in SL, reject null hypothesis and conclude that y-intercepts are
different, therefore the IL of the two species differ significantly (F = 33.89, P = 0.0001).


44
body shape with growth. Individuals are also fairly variable in terms of body pigmentation
and color patterns; such differences can be associated with age, size, or sexual condition,
and may also be environmentally induced. To further complicate piranha taxonomy, the
complete geographic distribution of most species is unknown. Moreover, because little if
any comparative material was available to previous taxonomists, most earlier descriptions
were incomplete, and thus inadequate for making accurate identifications. Fink (1988)
reported that fewer than half of the about 60 nominal species of piranhas were valid.
Nevertheless, sampling in previously uncollected regions has resulted in the discovery of a
few new species (personal observation). Except for difficulties in identifying some of the
smallest specimens (less than 25 mm SL), I believe I have successfully sorted out the
different species encountered in this study. Preserved specimens examined are deposited in
the Museo de Ciencias Naturales (MCNG), UNELLEZ, Guanare, Venezuela. Voucher
material has also been donated by MCNG under an official cooperative agreement to the
Florida Museum of Natural History (UF), Gainesville, Florida. Institutional acronyms are
from Levitn et al. (1985).
Because of the taxonomic confusion, piranhas have often been misidentified in the
literature. Drs. William Fink (UMMZ) and Antonio Machado-Allison (MBUCV) are
currently revising the piranhas of Venezuela; I have relied on both for identifications of
certain voucher specimens. They have also made available their unpublished key to
Venezuelan piranhas. Taphom (1990) prepared keys to the characiform fishes of the Apure
drainage, and also listed probable generic and specific synonyms of serrasalmine fishes.
His nomenclature for piranhas follows that of Fink and Machado-Allison. Abbreviations
used for piranhas and other serrasalmine fishes in illustrations and tables are given in Table
3-1. In the following section species names used in the present report are listed together
with names used by me and colleagues for the same species in recent publications:


Table 6-2. Food items of Serrasalrnus rhombeus from the upper Orinoco River basin by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %V = percent volume. N = 83.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
HI(40-79)
2
0
%D
%V
%o
IV(80-159)
29
7
%D
%M
%0
V(>160)
52
16
%D
%V
Plant material
-
-
-
18.2
4.6
5.1
13.9
5.3
1.9
Decapoda
-
-
-
-
-
-
2.8
2.6
5.2
Aquatic insects
-
-
-
4.6
4.6
0.7
-
-
-
Other invertebrates
-
-
-
13.6
-
1.5
5.6
2.6
0.7
Small whole fish
4.6
4.6
3.4
8.3
5.3
33.3
Fish flesh
50.0
50.0
80.0
40.9
36.4
49.8
58.3
50.0
46.3
Fish fins
50.0
50.0
20.0
59.1
40.9
31.0
13.9
13.2
3.8
Fish scales
-
-
-
22.7
9.1
8.6
25.0
15.8
3.0
Other
-
-
-
-
-
-
8.3
5.3
5.9


122
(93.1-74.1-84.4), other plant material (24.1-13.8-4.6), fish scales (3.4-0-0.1); Group V
(n=6)-masticated seeds (16.7-0-2.2), leaves/flowers (100.0-100.0-97.8). Several of the
flowers could be identified: one stomach was packed with small whole flowers of a
Machaerium sp. (Papilionaceae), and a second contained flower fragments of a
Campsiandra sp. (Caesalpiniaceae). Four fish collected in an abandoned meander of the
Putaco River with dense aquatic vegetation had fed on flowers and leaves of the water
lettuce Pistia stranotes (Araceae).
Myleus torquatus was taken along the main channels of rivers and streams, but not
in backwater areas. It is a medium-sized fish. The body coloration is silver, and there is a
black border on the caudal fin that may vary widely in intensity. A few males had long
dark filaments extending from the dorsal-fin rays. My examination of the stomachs of 24
individuals (109-192 mm SL) (Fig. 6-4) indicated that the species is highly opportunistic in
its feeding behavior. Many stomachs contained either crushed seeds or well-digested fruit;
one was full of cooked white rice (having fed on our discarded camp food); the stomachs
of several specimens were packed with large scales. Because scales of serrasalmine fishes
are small, scale eating was not the result of intraspecific aggression. Unlike other members
of the genus examined, Myleus torquatus has a unique "overbite", the upper jaw extending
past the lower jaw, causing several of the upper teeth to be exposed. Other scale-eating
fish are known to ram their victims and use their projecting teeth to dislodge scales
(Sazima and Machado 1982, Sazima 1983); the exposed teeth of M. torquatus could be
used for the same purpose. Food items were as follows (%0-%D-%V): Group IV (n=4, 2
empty) plant material (50.0-50.0-21.1), fish fins (50.0-0-5.3), fish scales (50.0-50.0-
73.7); Group V (n=20, 2 empty) masticated seeds (77.8-61.1-50.4), leaves/flowers
(27.8-27.8-43.6), other plant material (5.6-5.6-1.0), other invertebrates (11.0-0-0.2), fish
flesh (5.6-0-0.2), fish scales (22.2-0-3.9), and other (5.6-5.6-0.7). IL/SL ranged from
2.6 to 3.2.


103
Table 6-1. List of laxa identified from the stomach contents of the three most common
piranha species from upper Orinoco River drainages, Venezuela.
Species
Food Item
(frequency of occurrence)
Serrasalmus rhombeus
Fish remains (small whole fish or flesh): Ctenoluciidae Boulengerella
sp. (1); catfish: Callichthyidae Corydoras sp. (1); Auchenipteridae
(1); Pimelodidae (1); Doradidae (probably Liphodoras).( 1); unidentified
catfish remains (2); Cichlidae (2), other fish (32).
Bird; fragments of feather and bone (1).
Amphibians: skeletal remains of adult toad Bufo marinus.il).
Invertebrates: Decapoda: crab(l); Arthropoda- terrestrial beetle (1),
adult beetle Gyrinidae (1), insect larva (1), unidentified insect (1),
terrestrial insect (1), Orthopteran leg (1); Gastropoda snail (1).
Plant Material: Filamentous algae (1); unidentified flower (1); leaf or leaf
fragments (2); woody twigs (1); root fibers (5), seed fragments? (2)
Serrasalmus manueli
Fish (whole fish or flesh): characoid ( ); Cichlidae juvenile Cichia
temensis.{\)\ gymnotoid eel remains (1); catfish remains (Doradidae
or Auchenipteridae) (2), catfish remains (1), unidentified fish (24).
Reptiles: Lizard remains (1).
invertebrates: Decapoda: Macrobrachium olfersi (1), unidentified shrimp
(2), decopod leg fragment (1); terrestrial insect (3), unidentified insect
(1).
Plant Material: small flowers of a Lecythidaceae Gustavia sp.? (1);
Palmae fruit of Bactris gasipaes ? (2); unidentified masticated seeds
(9); leaf fragments (3); unidentified pieces of fruit (exocarp and
mesocarp) (1); vascular plant material (2).
Serrasalmus cf. eigenmannii
Fish (whole fish or flesh): unidentified fish remains (7).
Plant Material (all unidentified): flowers fregments (2); masticated seeds
(mostly endocarp) (35).


204
Menezes, R. S., and M. F. Menezes. 1946. Notas sobre o regime alimentar de algumas
especies ictiolgicas de agua doce do Nordeste. Rev. Brasil. Biol. 6(4): 537-542.
Mota, A., J. D. Rodrigues, M. N. Moraes. and A. E. Ferreira. 1982. Dinmica da
nutrigo da pirambeba. Serrasalmus spilopleura Kner 1859 (Pisces, Cypriniformes)
na Represa de Bariri, Estado de Sao Paulo, Brasil. B. Inst. Pesca, Sao Paulo 9:13-
19.
Myers, G. S. (editor). 1972. The piranha book. Tropical Fish Hobbyist Publications.
Neptune City, New Jersey, 128 pp.
Nico, L. G. 1990. Feeding chronology of juvenile piranhas, Pygocentrus notatus, in the
Venezuelan Llanos. Environmental Biology of Fishes 29:51-57.
Nico, L. G., and D. C. Taphorn. 1984. Biologa de la curvinata, Plagioscion
squamosissimus, en el Mdulo "Femando Corrales" de la UNELLEZ, Edo. Apure.
Revista UNELLEZ de Ciencia y Tecnologa. No. 2, pp. 31-39.
Nico, L. G., and D. C. Taphorn. 1985. Diet of Acesrrorhynchus microlepis (Pisces:
Characidae) in the low Llanos of Venezuela. Copeia 1985(3):794-796.
Nico, L. G and D. C. Taphorn. 1986. Those bitin' fish from South America. Tropical
Fish Hobbyist 34(4):24-27,30-34,36,40-41,56-57.
Nico, L. G., and D. C. Taphorn. 1988. Food habits of piranhas in the low Llanos of
Venezuela. Biotropica 20:311-321.
Northcote, T. G.< R. G. Northcote, and M. S. Arcifa. 1986. Differential cropping of the
caudal fin lobes of prey fishes by the piranha, Serrasalmus spilopeura Kner.
Hydrobiologia 141:199-205.
Northcote, T. G., M. S. Arcifa, and O. Froehlich. 1987. Fin-feeding by the piranha
(Serrasalmus spilopleura Kner): The cropping of a novel renewable resource.
Proceedings of the Fifth Congress of European Ichthyologists, Stockholm 1985, pp.
133-143.
Odum, W. E. 1970. ITtilization of the direct grazing and plant detritus food chains by the
striped mullet Mugil cephalus. Pages 220-240 in J. H. Steele, editor. Marine Food
Chains. Oliver and Boyd, Edinburgh.
Okeyo, D. O. 1989. Herbivory in freshwater fishes: a review. The Israeli Journal of
Aquaculture Bamidgeh 41(3):79-97.
Pierce, R. J., T. E. Wissing, J. G. Jaworski, R. N. Givens, and B. A. Megrey. 1980. Energy
storage and utilization patterns of gizzard shad in Acton Lake, Ohio. Transactions of the
American Fisheries Society 109:611-616.
Prance, G. T. 1979. Notes on the vegetation of Amazonia EH. The terminology of
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University Press, New York, 752 pp.


Fig. 6-5. Dendrogram from cluster analysis depicting similarities among diets of piranhas
and related species (by size class) from the upper Orinoco River basin,
Venezuela. Similarity values are from Table 6-7, dendrogram UPGMA-
generated using overlap index of Schoener (1970) and eleven resource
categories. See Table 3-1 for species abbreviations.


169
Orinoco species found in the Llanos (Machado-Allison and Garcia 1986, Nico and Taphom
1988, Winemiller 1989a, Nico 1990) and for Serrasalmus spilopleura from a reservoir in
southern Brazil (Sazima and Zamprogno 1985) (Table 1-1). In general, piranhas change
their preferred prey as they grow from invertebrates as small juveniles, to fins as large
juveniles, and finally to a diet of mainly fish or plant matter. The size at which individuals
switch from one mode of feeding may be species specific, related to food resource
availability, or more likely, a combination of both of these factors. All juveniles less than
about 20 mm SL specialize on invertebrate prey (i.e., microcrustaceans and aquatic insect
larvae), some not switching to fins until about 40 mm SL. Fin eating is most common in
juveniles between 40 and 80 mm SL, but I found that juveniles as small as 20 mm SL
(e.g., Serrasalmus manueli) already begin feeding on fins taken from Other small fishes.
Although data are incomplete on several species, Pygocentrus caribe is the only common
piranha that does not feed on fins to any great extent as a juvenile (but see Machado-Allison
and Garcia 1986). Although some species continue to feed heavily on fins as adults, larger
individuals of most species switch to a diet consisting primarily of fish or seeds.
Herbivory among piranhas seems to be mainly an adult trait, whereas the young of other
serrasalmine fishes (e.g., Metynnis) will frequently feed on plant matter. In contrast to the
findings of Machado-Allison and Garcia (1986), young piranhas that I studied rarely ate
seeds or other plant matter.
Camivorv versus Herbivorv
Although adult piranhas may be classified as either largely carnivorous or largely
herbivorous (Table 1-1), my results suggest that they can adjust their diets to changes in
food resources. There is a certain amount of omnivory in both groups. However, when
specimens of both groups were taken together, diets were usually distinctly different. In
the upper Orinoco, when finding two or more piranha species in the same gill net, then-
stomachs were either full of seeds or fish flesh. Such partitioning of food resources was


Fig. 2-1. Map of northern South America showing Orinoco River basin.


129
of the three Myleus species. Cluster VI was comprised of insectivores and consisted of
small juvenile piranhas that fed on the larva of small aquatic insects.
Of the six different feeding guilds recognized for serrasalmine fishes from the upper
Orinoco, piranhas were represented in four. None of the piranhas was considered to be
leaf-eaters or scale-eaters. My results indicate that most piranhas eat scales on occasion,
but none did so consistently, or to any great degree. Only in the non-piranha
serrasalmines, Catoprion memo and Myleus torquatus (80-159 mm SL), did scales make
up a high proportion of total diet volume. Adults of a few Orinoco piranhas were
considered to be truly herbivorous, and these fed mostly on seeds. Nevertheless, most
species exhibit some flexibility in feeding behavior, species considered to be primarily
herbivorous occasionally took animal prey, and the more carnivorous species sometimes
fed on plant material in bulk. In contrast to seed-eating piranhas, other primarily
herbivorous serrasalmine fishes exploited a more varied plant diet, frequently feeding on
leaves and flowers, in adddition to seeds and fruits.
Diet width measures diversity and evenness of resource use. Diet breadth usually
changed with age (Fig. 6-6), but there was no consistent pattern among species. The
lowest diet breadth values were found in both small and large size classes of piranhas.
Serrasalmus rhombeus >160 mm SL, Group V, had the highest diet breadth (i.e., 2.99).
In summary, of the eight piranha species found in the upper Orinoco River basin:
the adults of four species (Serrasalmus rhombeus, S. manueli, S. altuvei, and Pygocentrus
caribe) fed heavily on fish or fish fins: and adults of the other four piranha species
(Serrasalmus cf. eigenmanni, Pygopristis denticulatus, and two Pristobrycon species) were
basically seed predators, biting seeds into small fragments before ingesting them. Of the
three most abundant species in my samples (,Serrasalmus rhombeus. S. manueli, and S. cf.
eigenmanni), two were primarily piscivores, but S. manueli, though primarily a fish-eater,
occasionally took seeds or fruits in mass. All drainages in the upper Orinoco are heavily


119
long intestines. The diets of several of the more commonly encountered species are
presented in Figure 6-4.
Catoprion ment (Cuvier 18191 Although locally abundant in parts of the low
Llanos, C. ment was uncommon in my samples from southern Venezuela, where it was
limited to lentic, back-water areas. It is a small species; those taken in the upper Orinoco,
all over 90 mm SL, were some of the largest I saw in all of Venezuela. The body is
silvery, cheek usually marked with reddish orange. Both males and females may have long
filaments extending from the first rays of dorsal fin. The seven large adults examined (99
to 128 mm SL) contained mostly fish scales (81.7% by volume) and a small amount of
plant material (10.4%) (pieces of leaves, and some filamentous algae), and aquatic insects
(8.0%) (Fig. 6-4). IL/SL ratio (n=7) ranged from 0.7 to 0.9.
Myleus species. The genus Myleus is represented by several species of deep
bodied, laterally compressed fishes. Jaw teeth are essentially molariform, with high cusps
that are adapted for cutting and possibly crushing plant material. The sexes exhibit striking
differences in body color and fin morphology; the males sometimes develop bright colors
and long fin filaments that are most pronounced during the breeding season. Three species
of Myleus were common in my samples from the upper Orinoco, Myleus asteias, M.
schomburgkii, and M. torquatus.
Myleus asterias was the most common species of this genus encountered. My
largest specimen was 185 mm SL, although maximum size may be much larger. It is a
silvery fish, with the bodies of males often spotted with variable hues of purple and
yellow. The anal fin of the male consists of two lobes with very small hooks present
during the breeding season. In contrast, the anal fin of females forms single a long lobe.
Most of the 37 specimens examined (98-185 mm SL) contained leaves that had been
clipped or sliced into small fragments (Fig. 6-4). Food items were as follows (%0-%D-
%V): Group IV (n=31, 2 empty)-masticated seeds (24.1-12.1-10.9), leaves/flowers


22
two or more of the basic water types; some change seasonally as flows from a diverse array
of smaller tributaries rise and fall. For example, during high water the Guayapo River of
the Sipapo drainage changes from a Clearwater river in its upper and middle reaches to a
blackwater river in its lower segments, due to increased input of tannin-stained waters from
adjacent flooded forests. To a large extent, the hydrochemistry of the Orinoco tributaries is
controlled by the geomorphological and floristic character of their watersheds. In general,
rivers of the Andes and Llanos are high in suspended sediments, whereas streams
originating in the weathered Guayana highlands and the forests of the upper Orinoco
transport low sediment loads. Nevertheless, exceptions to the above-mentioned
hydrochemical pattern can be found in all regions as a result of local conditions.
History of the Basin
The details and precise timing of geological events involved in the formation of the
Orinoco River basin are not well understood. The oldest land form in the basin is the
Guyana Shield, ancient mountains composed of Precambriun material that underwent
additional uplift and exposure during the Tertiary (Whitmore and Prance 1987). Because
they have been exposed for many millions of years, these highlands have been heavily
worn and dramatically shaped by erosion. The mountains of the Andes were created later,
uplifted as a result of plate tectonic events during the Miocene-Pliocene, 2-8 million years
ago (Whitmore and Prance 1987:7). The Llanos are thought to be the most recent major
topographical feature in the basin. During Quaternary periods of raised sea-level
(interglacials) the Llanos plains were the bed of a large interior sea. Thus, similar to many
lowland areas in South America, these central plains are primarily composed of Quaternary
sediments that mantle Tertiary and older sediments, with recent additions of alluvial river
deposits carried down from the surrounding mountains during the Pleistocene (Beek and
Bramao 1968:86, Walter 1973: 72-73, Cole 1986).


159
the upper Orinoco. Carnivorous piranha species were abundant in both the upper Orinoco
and the low Llanos, but they were more common in the Llanos.
Ecological Considerations
There seems to be no single habitat parameter that will reliably predict the makeup
of piranha assemblages in given areas. Nevertheless, local ecological conditions are
probably more important than regional differences in determining species abundance and
local species composition. Various ecological factors, both physical (e.g., water
temperature, clarity, pH, stream gradient) and biological (e.g., vegetation, availability of
food, spawning requirements, symbiotic interactions with other organisms) can be
considered as potentially limiting numbers and kinds of piranhas. Some of these factors
have already been touched upon briefly in the preceding sections.
Most Orinoco piranha species, in addition to being widespread, are found in a
variety of lowland habitats (e.g., rivers, streams, floodplain lagoons and oxbow lakes)
over a wide range of environmental conditions (Table 4-4). If numbers of individuals can
be used as an indicator of habitat quality, then the preferred habitats of most species are
lentic white waters. Serrasalmus cf. eigenmanni is the most common herbivorous species
in the upper Orinoco, and it was found in both whitewater streams and cutoff meanders.
Carnivorous piranha species seem more able than herbivorous species to adapt to
perturbation. For example, several of the more carnivorous species occur in great numbers
in reservoirs: Serrasalmus rhombeus and Pygocentrus caribe in the Orinoco (personal
observations), 5. rhombeus, S. spilopleura, and P. nattereri in Brazil (Table 1-1). To my
knowledge, those species that I have categorized as largely herbivorous (Table 8-1) are
never found in reservoirs. Still, many species are apparently able to maintain smaller
populations in what might be described as less desirable habitats.
Several species are widely distributed but seem to be uncommon throughout their
ranges (e.g., Serrasalmus altuvei. Pristobrycon stiiolatus, Pygopristis denticulatus).


123
Myleus schomburgkii. M. schomburgkii, possibly a species complex (Machado-
Allison, personal communication), is fairly common and widespread in the upper Orinoco,
and is also found in the Capanaparo and Cinaruco rivers of the Llanos. Maximum size is
over 300 mm SL. Myleus schomburgkii is silvery, with a single large black marking that
runs vertically on each side of the body that gives the appearance of having been stroked
with a paint brush. In breeding males the dorsal fin develops many long black filaments,
and large parts of the body may be covered with various combinations of bright reddish
orange, dark red, and black. I examined the stomachs of nine specimens (87-310 mm SL)
(Fig. 6-4). Common food items included seeds (masticated), filamentous algae, and
fragments of leaves of a bryophyte. IL/SL ranged from 2.3 to 3.8. Seeds were also the
most important food item in eight M. schomburgkii collected in the Llanos during the dry
season.
Summary of Upper Orinoco Trophic Patterns
Table 6-8 presents a matrix giving the diet overlap values, calculated by size class
for eight piranhas and four related species from the upper Orinoco River basin. Cluster
analysis of the Table 6-8 data produced six major trophic groupings or feeding guilds (Fig.
6-5): general piscivore, aquatic insectivore, scale-eater, fin-eater, seed-predator, and
folivore. Cluster I includes the general piscivores, predators that bit out chunks of flesh
from other fishes or ate small fish whole; this guild consisted of three species in the three
larger size classes (>40 mm SL). Cluster II were fin eaters and consisted of four piranha
species and four different size classes. Cluster IE, the seed-predator guild, consisted of
fish that fed mostly on seeds, which they bit into small fragments before ingesting. Seed-
predators were represented by six species in the two larger size classes. Cluster IV were
scale-eaters, represented by two species. Cluster IV were folivores, fish that fed on leaves
and flowers, usually by clipping them into small fragments; this group was limited to two


150
Prey items
Fig. 7-1. Bar graph comparing the dry mass composition of small whole fish, scales, and
fins. Energy expressed as kJ/g of dry mass, all others given as percent of dry
mass. Vertical bars represent 2 SE.


154
carbohydrate contents. Giving nutrient content values as a percentage of the dry mass
composition of the fruit pericarp, Snow reported ranges of 1.9 to 21.6% protein, 0.6 to
67.0 % fat, and 10.8 to 90.9% carbohydrate. Worthington (1989) found that the fleshy
parts of fruits eaten by manakins, a group of neotropical frugivorous birds, typically had
low nutrient concentrations. However, the energy content of fruit pulp ranged from 15 to
17 kJ/g of dry pulp. Similarly, Kerley and Erasmus (1991) reported a range of 17 to 20
kJ/g dry mass for seeds commonly eaten by African rodents.
In conclusion, because of their high sugar and oil content, the energy yield of seeds
and fruits is frequently higher than that of fish flesh. Nevertheless, herbivorous species
probably need to supplement their diets with animal matter. Sugars supply only calories
rather than essential nutrients (see Karasov and Diamond 1988). From his research on the
Gray's monitor lizard, Auffenberg (1988) concluded that fruits alone, being low in both
proteins and calcium, forces vegetarian reptiles to include other items such as land snails in
their diet.


143
Ecomorphological Correlates: Intestine Length and Diet
In general, intestine length (IL) was positively correlated with standard length (SL),
that is, the IL/SL ratio typically increased with greater body size, or age, in most species.
Small juvenile piranhas tended to have fairly low IL/SL, usually less than 1.0. To reduce
the effect on variability due to body size the following comparisons were limited to larger
specimens, those >80 mm SL. Relative intestine length (IL/SL) among the serrasalmine
fishes (> 80 mm SL) examined ranged from less than 1.0 to greater than 3.0. Differences
among species were correlated with adult diet (Fig. 6-10). The association between
intestine length and degree of herbivory among species (> 80 mm SL) was significant
(Spearman rank correlation, rs = 0.79, P < .001, n = 35; Fig. 6-11); carnivorous species
have a short intestine (<1.5 IL/SL) and all herbivorous species have a relatively long
intestine (usually >1.5). In a few cases data seemed to indicate differences in IL/SL
between populations of the same species, but such variation was usually associated with
small sample size or body size effects.
Large sample sizes for the three most common piranhas in the upper Orinoco (i.e.,
(,Serrasalmiis rhombeus, S. manueli, and S. cf.eigenmanni) permitted a more detailed
analysis of IL, SL, and diet relationships (Fig. 6-11). Serrasalmus cf. eigenmanni, a
species that fed heavily on seeds, had the longest relative IL; its IL/SL ratio was
significantly greater than that of the other two species (ANCOVA; F = 21.44 and 26.09,
P = 0.0001). Serrasalmus rhombeus, the most carnivorous of the three, had the relatively
shortest intestine, whereas S. manueli had an intermediate intestine length. The latter
species occasionally takes seeds or fruit in large quantity. Although slopes of the IL/SL
regression lines did not differ between S. rhombeus and S. manueli (F = 3.24, P =
0.0741), the IL of the two species differed after adjusting for differences in SL (F = 33.89,
P = 0.0001); S. rhombeus had a shorter intestine, as expected from its diet. My data show
that adult S. manueli from the upper Orinoco fed more on plant material than conspecific


Fig. 6-7. Diets by size class (>40 mm SL) of three piranha species from the Cinaruco and
Capanaparo river drainages of the low Llanos, Orinoco River basin, Venezuela.
Size of segments represents percentage of volume of each prey type; n = number
of stomachs examined; numbers in parentheses represent diet breadth using
formula of Levins (1968).


Table l-l--continued.
Basin
(State, Country)
Site or
Habitat
Study Period and
Duration
Species
No. Examined
(Size range)
Comments
Source
8. Amazon
(Amazonas,
Brazil)
Madeira River
drainage
Rio Machado
(rivers, flooded
forest)
1977 and 1978
high and low
water; 1979 high
water
1) Serrasalmus rhombeus
2) S. elongatus
3) S. serrulatus
4) S. cf.striolatus
5-7) Serrasalmus spp.
n = 254 (180-370)
n = 67? (140-220)
n = 36 (130-250)
n = 9 (150-200)
n = 5? (no data)
Adults of some species highly
carnivorous, other species feed on
seeds and fruits; concluded all or
many omnivorous
Goulding
(1980)
9. Tiet River
(So Paulo,
Brazil)
Bariri
Reservoir
Sampled four
seasons of year,
Jan. to Dec. 1979
1) Serrasalmus spilopleura
n = 299 (75-295
TL)
Study of seasonal changes in
average stomach fullness,
heaviest feeding in Summer.
Mota et al.
(1982)
10. Atibaia
River (Sao
Paulo, Brazil)
Americana
Resevoir
Feb. to Apr. 1983
1) Serrasalmus spilopleura
n = 41
(10.5-19.5)
Stomach contents of larval and
small juveniles, feeding behavior
of juveniles in aquaria
Sazima and
Zamprogno.
(1985).
11. Amazon
(Par, Brazil)
Curu-Una
Reservoir
Three collections,
Aug., Nov., 1982
Feb. 1983
1) Serrasalmus rhombeus
n = 250 (50-320)
Compared diets among five sites
in reservoir, mainly fed on fish,
one site aquatic insects
Ferreira (1984b,
also see 1984a)
12. Orinoco
(Guaneo,
Venezuela)
Apure drainage
savanna lagoon
Intermittent
1982-1984
wet seasons
1) Pygocentrus notatus
2) Serrasalmus rhombeus
3) Pristobrycon striolatus
n = 44 (10-100)
n = 50 (10-100)
n = 40 (10-100)
Juvenile diets, smallest fed on
microcrustaceans; larger ate fins,
scales, fish flesh, small seeds
Machado-
Allison and
Garcia (1986)
13. Paran
(S3o Paulo
Brazil)
Tiet drainage
Americana
Reservoir of
Atabaia River,
Intermittent
1982 to 1984
1) Serrasalmus spilopleura
n = 115?
(10-207)
Diet mainly fins, scales, fish
flesh, and whole fish
Northcote et al.
(1986, 1987)
14. Paran
(Mato Grosso,
Brazil)
Pantanal region
1985 and 1986
1) Pygocentrus nattereri
2) Serrasalmus spilopleura
Not applicable
Investigated three reported cases
of piranhas scavenging on human
corpses
Sazima and
Guirnaraes
(1987)
o


114
Pristobrycon striolatus (Steindachner 19081
Pristobrycon striolatus was rare in my samples from the upper Orinoco. It is a
medium-sized piranha found in both the Llanos and in southern Venezuela. The body is
silvery, partly covered with very small black spots, and has black along the base of the
caudal fin. The cheek and breast are typically reddish orange. My upper Orinoco sample
consisted of five adult specimens (106-165 mm SL), all taken during low water, four from
Cao Jenita of the Ocamo River, and one from a lagoon of the Mavaca River. The
stomachs of all five adults were packed with unidentifiable crushed seeds (Fig. 6-2 and
Table 6-6), which accounted for 84% of total food volume. Other plant material included
small stems and flower fragments. EL/SL ratio of the five specimens ranged from 1.5 to
2.8.
In addition to the larger fish, I also examined 38 small Pristobrycon juveniles (<40
mm SL), tentatively identified as P. striolatus. Characteristic of the genus, they had a
preanal spine (Fink, personal communication), but lacked ectopterygoid teeth. All were
taken from a mat of aquatic vegetation near the shore of the Yureba River, a blackwater
tributary of the Ventuari. Those of 10 to 19 mm SL fed heavily on the larvae of aquatic
insects (7.2 insects per stomach), mostly small chironomids, trichopterans and
ephemeropterans (Fig. 6-3). Food items of these Group IP. striolatus (n = 16) were as
follows (%0-%D-%V): microcrustaceans (18.8-0-1.7), aquatic insects (93.8-93.8-90.0),
and fish fins (12.5-6.3-8.3). Stomachs of fish 20-39 mm SL (n = 22, 2 empty) had fed
mostly on fins (55.3% by volume) and aquatic insects (44.3%) (Fig. 6-2). Aquatic insects
(3.1 per stomach) identified from stomachs comprised chironomids, ephemeropterans, and
coleopteran larvae and pupae. Mean IL/SL for small juveniles was less than 1.0.
Pristobrycon sp.
Pristobrycon sp. is a rare species. My sample consisted of only five adult fish
(182-245 mm SL) all taken in November during high water from flooded forest along Cao


75
savanna becomes flooded, with low areas covered by as much as 2 m of water. Lower
areas and deeper borrow pits contain water throughout the year, but most permanent water
sites are reduced to less than 1 m depth during the dry season. The fish species
composition of borrow pits resembles that of natural lagoon habitats. Large free-floating
mats of vegetation, primarily Eichhomia crassipes and E. azurea, are common in streams
and savanna pools. During high water, fishes can move between the streams and the
interior of the diked areas through culverts or low sections of the dike, but this interchange
has been greatly reduced as dike stability has been achieved. During the late dry season
(January to early April), the streams have little or no flow and are often reduced to isolated
pools. Rainy season flow is continuous with depths to 5 m or more. Width ranges from 3
to 12 m during low water to over 30 m during peak flooding. Although the Apure River
itself is white water in character, streams of the study area are essentially blackwater
habitats with low transparency. The flooded savanna pools are white water habitats,
usually very turbid (<10 cm Secchi disk), but the larger pools often become quite clear (>1
m Secchi disk) late in the rainy season.
Species Accounts
In this section, I describe the general morphology, local distribution and habitat,
and the diets of the piranha species found in the Cao Caicara study area. Information on
the smallest size class of piranhas, juveniles less than 20 mm SL, were pooled; all were
tentatively identified as Pygocentrus caribe. Figure 5-3 is a summary of the diets by size
class (Group II and larger) of the seven piranhas and Catoprion ment from the Cao
Caicara area.


140
Table 6-10. One-tailed Marm-Whitney U-test results testing the prediction that piranha
species (> 80 mm SL) from upper Orinoco River drainages are more herbivorous than
those from the low Llanos. Diet measures are percent adjusted volume (%Va), percent
dominance (%D), and percent frequency of occurrence (%0) (see Chapter 3 methods for
explanation). Ni = number of piranha species from upper Orinoco; N2 = number of
piranha species from low Llanos. See Table 6-9 for number of specimens examined for
each species.
Diet Measure
Ni
n2
u
Mean
SD*
z value*
P
%va
8
10
23
40
11.22556
- 1.514402
0.0655
%D
8
10
22.5
40
11.21973
- 1.559752
0.0594
%0
8
10
23
40
11.21556
- 1.514402
0.0655
* Corrected for ties


7
making it possible to recognize how particular characters arise under the influence of
contrasting selective forces (Clutton-Brock and Harvey 1984). Furthermore, comparisons
across a broad biogeographical scale offer what Wiens et al. (1986) suggested as perhaps
the best opportunity to understand a species' limits or responses to different environmental
conditions, revealing patterns that suggest something of its adaptive abilities or
evolutionary potential.
Literature Review
The following is a brief review of the literature relating to piranha feeding behavior
and trophic ecology. A summary of field studies investigating piranha feeding and diets is
given in Table 1-1. Unless otherwise stated, scientific names are as used in the original
literature. All references to Serrasalmus nattereri should be Pygocentrus nattereri.
Early naturalists and explorers were the first to report on piranhas, and most
accounts, such as those by Alexander von Humboldt, Henry Bates, and Theodore
Roosevelt, were primarily devoted to describing attacks by piranhas on animals and
humans, or relating the destruction done by piranhas to fishing gear (Bates [1863]
1975:202, Roosevelt 1914). Humboldt, who traveled extensively in South America
between 1799 and 1804, wrote the following passage while on the Orinoco River:
On the morning of the 3rd of April our Indians caught with a hook the fish
known in the country by the name of caribe* [*Caribe in the Spanish
language signifies cannibal], or caribito, because no other fish has such a
thirst for blood. It attacks bathers and swimmers, from whom it often bites
away considerable pieces of flesh. The Indians dread extremely these
caribes; and several of them showed us the scars of deep wounds in the calf
of the leg and in the thigh, made by these little animals. They swim at the
bottom of rivers; but if a few drops of blood be shed on the water, they rise
by thousands to the surface, so that if a person be only slightly bitten, it is
difficult for him to get out of the water without receiving a severer wound.
Humboldt ([ 1816-1831 ] 1971:166-167)


3
tip of snout to base of tail (Standard Length, SL) to large species such as Serrasalmus
rhombeus, which grow to well over 35 cm SL. The general body form ranges from sharp
snouted and elongate, Serrasalmus elongatus, to blunt-headed and robust species such as .
the red-bellied piranhas Pygocentrus caribe of the Orinoco and P. nattereri of the Amazon.
Of the approximately thirty species of piranhas, at least twelve occur in the Orinoco
basin where, as in many other areas of tropical South America, they are exploited for
subsistence fisheries and also commercially. Piranhas occur in rivers and floodplains of
both open savannas and densely forested regions and often make up a high percentage of
fish biomass and numbers of individuals (Mago-Leccia 1970, Taphom and Lilyestrom
1984). Thus, they play a major role in the food web of many lowland aquatic
communities. Contrary to common belief that they are strictly carnivorous, piranhas and
their close relatives exploit a broad spectrum of food resources including arthropods, fishes
and other vertebrates, fish fins and scales, carrion, seeds, fruits, leaves, and flowers
(Goulding 1980, Sazima 1983, Sazima and Guimares 1987, Nico and Taphom 1988,
Winemiller 1989a, Sazima and Machado 1990). Serrasalmine fishes living in tropical
savannas encounter substantially different habitat conditions in comparison to those
populations occupying forested regions. Thus, comparative studies of piranha diets and
trophic ecology can provide insights into their responses and adaptations to the selective
forces of different environments
Purpose of Present Study
Tropical South America possesses the most diverse freshwater fish fauna of any
continent (Bohlke et al. 1978). Considering both described and undescribed taxa,
Lundberg et al. (1987) estimated that the Orinoco River basin alone probably contains
almost 1,000 fish species, more species than are found in all the freshwater systems of
temperate North America. Unfortunately, the extremely diverse faunas and floras of many


63
CD
O)
CO
c
2
T3
u_
CD
Q.
C/3
QD
O
CD
Q.
CO
CO
JZ
c
co
1
CL
10-
8-
6-
4-
2-
0 +-
3.0
o
Mav
3.5
*Cap
Apu
Cin*
OOca
Ata
O
Mat
O
Sip
o
Ven
= Low Llanos
O = Upper Orinoco
T 1 1 1 r
4.0 4.5 5.0 5.5
Log drainage area (km 2)
6.0
Fig. 4-2. Scatter diagram showing relationship between number of piranha species per
drainage and log of the drainage area size (km2) for nine sampled drainages in
Orinoco River basin, Venezuela. Drainage abbreviations are: Apu = Apure,
Ata = Atabapo, Cap = Capanaparo, Cin = Cinaruco, Mat = Matacuni, Mav =
Mavaca, Oca = Ocamo, and Sip = Sipapo.


187
21957 (6-6); MCNG 22020 (1-1); MCNG 21795 (5-5); MCNG 21966 (6-6); LN 89-153
(3-3); LN 89-154 (2-2); LN 89-161 (4-4); LN 89-165 (16-16).
Ventuari River drainage: 1989: MCNG 21969 (3-3); MCNG 21837 (2-2 ): MCNg
22128 (2-2); MCNG 21972 (1-1); MCNG 21982 (1-1); MCNG 21980 (2-2); MCNG
21969 (3-3); MCNG 22022 (5-5); MCNG 22115 (1-1); Small juveniles tentatively
identified as Serrasalmus manueli: MCNG 22053 (5-5jv).
Orinoco main stem: 1989: LN 89-92 (1-1). 1990: MCNG 21849 (2-2). 1991:
MCNG 25408 (3-3); MCNG 25396 (3-3); LN 91-50 (1-0).
Serrasalmus medinai
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 7684 (1-1); MCNG
8408 (1-1); MCNG 11311 (1-1). 1980: MCNG 5900 (16-16). 1981: MCNG2124(4-
4); MCNG 2165 (1-1); MCNG 2285 (2-2); MCNG 2299 (1-1); MCNG 2358 (3-3);
MCNG 2378 (8-8); MCNG 3887 (1-1); MCNG 3918 (1-1): MCNG 4167 (1-1); MCNG
4340 (1-1); MCNG 4559 (2-2); MCNG 4778 (2-2); MCNG 4881 (1-1); MCNG 4926 (4-
4); MCNG 4975 (4-4); MCNG 10421 (1-1); MCNG 10422 (1-1); UF 31458 (1-0); UF
36156 (3-0). 1984: MCNG 10710 (20-20); MCNG 11365 (1-1). 1985: MCNG 11384
(21-21); MCNG 12472 (3-3); MCNG 12561 (6-6). 1989: MCNG 23171 (7-7); MCNG
23142 (5-5); MCNG 23152 (5-5); MCNG 23157 (4-4); MCNG 23162 (1-1); MCNG
23155 (1-1); LN 89-20 (1-1). Cao Maporal.-1980: MCNG 9099 (1-1). 1981: MCNG
10126(1-1); MCNG 10244(2-2); MCNG 11017 (1-0). 1983: MCNG 10072 (1-1).
1984: MCNG 11351 (2-0); MCNG 12562 (1-1). Other.-1979: MCNG 9684 (14-6);
MCNG 9751 (1-1). CaoCaicara: 1990: LN 90-62 (2-2).


131
forested and I found evidence of herbivory (i.e., seed-eating) by piranhas in all six
drainages studied.
Data on diets of the smaller size class piranhas from the upper Orinoco is
incomplete. Stomach contents of five species (<80 mm SL), supplemented by my
observations on feeding behavior of wild-caught juveniles of Serrasalmus nianueli and
Pygopristis denticulatus kept in aquaria, suggest that most species in the upper Orinoco
pass through a growth stage, between 20 and 80 mm SL, when fin-eating is common or
even their predominant mode of feeding. Smaller juveniles (< 30 mm SL) taken in the
upper Orinoco had fed heavily on small aquatic insects; microcrustaceans only accounted
for a small part of their diets. Young piranhas rarely ate seeds or other plant matter.
Comparison with Savanna Populations
Much of my original data on the trophic patterns of savanna populations comes
from the low Llanos of the Apure River basin. As seen in the previous chapter,
information on the Cao Caicara area, an Apure River tributary, contrasted sharply with my
findings on adult piranhas from the upper Orinoco. Fish (flesh, fins, and small whole fish)
was the main component of adult diets of all seven species of piranhas from the Cao
Caicara region. I rarely found evidence of seed-eating by piranhas in the Cao Caicara
site. The few seeds eaten were very small and probably were taken incidentally along with
intended prey items. Of hundreds of specimens examined, not one stomach contained
many seeds. Other plant material, such as bits of leaves, grass blades, root wads, tiny
flowers, and filamentous algae, was ingested, but was of minor importance in terms of
dominance and volume. Pristobrycon striolatus was a seed predator in the upper Orinoco,
but none of the 16 P. striolatus from the Apure drainage had fed on seeds; however, most
specimens examined were juveniles that had fed heavily on fins. A 84-rrtm SL juvenile,
collected in Cao Maporal and kept in an aquarium, fed on small seeds and fish fins while


CHAPTER 7
ANALYSIS OF NUTRIENT VALUES OF PIRANHA PREY
Piranhas and their close relatives exploit a broad range of food resources, including
arthropods, fishes and other vertebrates, fish fins and scales, carrion, seeds, fruits, leaves,
and flowers (Goulding 1980, Sazima 1983, Sazima and Guimaraes 1987, Nico and
Taphorn 1988, Winemiller 1989a, Sazima and Machado 1990). These diverse food items
differ in terms of protein, lipid, carbohydrate and caloric content, offering piranhas a range
of foods that differ in nutrient quality and digestibility. The nutrient value of a particular
type of food item, along with its relative availability and digestibility, is an important factor
in food preference or selection.
My results from the chemical analysis of scales, fin.->, and small whole fish are
given in Table 7-1 and Figure 7-1. I also present some information from the literature on
the energy contents and chemical components of other types of general food items, for
example insects and various types of plant material.
Animal Matter
Ssaks
Scale-eating, or lepidophagy, is known for several unrelated freshwater fishes of
South America (Roberts 1970, Sazima 1983). Many of the serrasalmine species that I
examined took scales in small quantities, but Catoprion ment was the only species in
which individuals of all sizes fed heavily on scales. The stomachs of several specimens of
My lens torquatus of size class IV were packed with scales, but the few specimens available
148


161
piranhas are basically carnivorous (Nico and Taphom 1988, Winemiller 1989a, see
Chapter 5). However, my later research of piranhas in other low Llanos drainages gave
evidence of seed eating by adults of two, and perhaps three, savanna species. The savanna
drainages studied (Apure, Cinaruco, and Capanaparo) are all located in the low Llanos of
Apure State; but study sites in the Cinaruco and Capanaparo drainages differed somewhat
from the Cao Caicara site of the Apure River drainage in having large gallery forests.
Similar to the flooded forests of the upper Orinoco, savanna regions having extensive
gallery forests provide a significant amount of edible plant material during high-water
periods when fishes are able to move across their floodplains; but plant foods are rarely
available to savanna fishes during the dry season when water levels have dropped. This
fact alone may explain why the more herbivorous piranha species are not very common in
savanna drainages. Admittedly, quantitative studies of availability of food resources across
a range of habitats are still required.
The possibility that South American fishes might segregate according to water type
is an attractive idea, only partly supported by recent field work (e.g., Taphom 1990,
Rodriguez and Lewis 1990). Nine of the 11 Orinoco piranha species studied were either
found in two or in all three major water types (Table 4-4). Nevertheless, as found by
Taphom (1990) in his study of Apure River fishes, blackwater habitats have a more unique
fish fauna than whitewater habitats due to a fairly high proportion of endemics or core
species. Even though few species are restricted to a particular water type, there do appear
to be consistent differences in relative abundance between water types for those species that
inhabit both black and white waters. Whereas most piranha species reach their greatest
numbers in whitewater habitats, several Orinoco species (i.e., Serrasalmus manueli,
Pygopristis denticulatiis, Pristobrycon sp.) are apparently restricted to, or much more
common in, black waters. In my study, cluster analysis of drainages based on species
composition also tended to group drainages that were similar in habitat (e.g., water type),
as well as by their geographic proximity.


166
individuals of all sizes fed heavily on scales. It was common in the low Llanos but rare in
samples from the upper Orinoco. Catoprion ment is a widely distributed species and its
scale-eating habits are well documented (Roberts 1970, Vieira and Gry 1979, Sazima
1983, 1988, Nico and Taphom 1988). The stomachs of several specimens of Myleus
torquatiis from the upper Orinoco were packed with scales; this is an unusual behavior not
previously reported for members of this generally herbivorous genus. Although most
studies suggest that adult Serrasalmus elongatus are primarily fin eaters (Roberts 1970) or a
general piscivore (Nico and Taphorn 1988, this study), Goulding (1980) reported that adult
Serrasalmus elongatus in the Madeira River drainage of Brazil preferred scales to fins.
Based on stomach content analysis alone, it is difficult or impossible to determine which
prey species are most frequently attacked. Certain species are obviously more vulnerable to
having scales removed than others. For instance, while the scales of some fish are firmly
attached to the body (e.g.,cichlids), the scales of others (i.e., many characoids) are easily
dislodged and these fish are probably more prone to attack by scale-eaters.
4) Predation on Invertebrates. Like the young of most freshwater fishes, small
juvenile piranhas (less than about 40 mm SL) commonly feed on immature aquatic insects
and microcrustaceans. Most major groups of small freshwater crustaceans were
represented in their diet, including cladocerans, copepods, ostracods, and conchostracans.
Most aquatic insects eaten by young piranhas were immature forms of cnironomids,
ephemeropterans, odonates, and plecopterans. The smallest piranhas in the Llanos fed
almost equally on insects and microcrustaceans, whereas small juveniles taken in
blackwater areas of the upper Orinoco preyed mainly on insects. Earlier it was emphasized
that there is a common association between young piranhas and aquatic vegetation. In
addition to providing some protection from predators, aquatic macrophytes are home to a
large number of invertebrate prey. Based on observations of wild-caught piranhas in
aquarium, Sazima and Zamprogno (1985) described how young juveniles pick
chironomids and ostracods from the roots of water hyacinths. Invertebrates are also taken


Table 5-4. Food items of Serrasalmus medinai from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 124.
Size class (mm, SL)
II (20-39)
in (40-79)
IV (80-159)
Number examined
13
58
53
Number empty
0
2
3
Food items
%o
%D
%Va
%o
%D
%Va
%o
%D
%Va
Plant material
7.7
7.1
3.2
16.1
1.7
1.6
26.0
5.8
2.9
Decapoda
-
-
-
1.8
1.7
2.4
8.0
1.9
2.9
Aquatic insects
7.7
7.1
9.7
-
-
-
-
-
-
Other invertebrates
-
-
-
5.4
1.7
0.8
4.0
-
-
Small whole fish
-
-
-
5.4
3.4
4.0
]
14.0
14.0
9.6
13.7
Fish flesh
7.7
7.1
6.5
23.2
15.3
46.0
36.5
48.0
Fish fins
84.6
71.4
77.4
80.4
62.7
68.4
66.0
30.8
20.1
Fish scales
-
-
-
44.6
11.9
8.0
36.0
15.4
12.3
Other
7.7
7.1
3.2
1.8
1.7
0.8
-
-
-
oo


TROPHIC ECOLOGY OF PIRANHAS (CHARACIDAE: S ERRAS ALMINAE)
FROM SAVANNA AND FOREST REGIONS
IN THE ORINOCO RIVER BASIN OF VENEZUELA
By
LEO G. NICO
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA

ACKNOWLEDGEMENTS
I owe a debt of gratitude to many friends and colleagues for their help during the
field work, data analysis, and manuscript preparation. During my development as a
tropical biologist, I greatly benefited from the guidance of several people. Dr. Jamie
Thomerson launched me into the study of neotropical fishes. Dr. Donald Taphom
provided me with the opportunity to do long-term research in the Orinoco River basin. In
1980, he took me to the Llanos where we netted my first piranha while seining the muddy
waters of Cao Maraca. The botanist Dr. Basil Stergios invited me to accompany his 1985
expedition to the upper Rio Negro and the Brazo Casiquiare where I fell in love with the
rivers and humid forests of southern Venezuela. My graduate committee chairman, Dr.
Horst Schwassmann, opened my eyes to the Amazon River; together we crossed part of its
estuary, from Belm to the Dha de Maraj, a journey I shall always remember.
My investigations have prospered from discussions with various members of my
committee as well as from the exchange of ideas with colleagues and friends, in particular
Drs. Donald Taphom, Steve Walsh, and Kirk Winemiller. Dr. Horst Schwassmann, and
other members of my committee Drs. Carter Gilbert, Martha Crump, Frank Nordlie, and
Nigel Smith were always helpful. I thank them for their advice and for reviewing the
tedious draft manuscripts. I am also grateful to Drs. Stephen Walsh, Jamie Thomerson,
Thomas Keevin, and Carmine Lanciani, and to Frank Jordon for their comments on
various sections and drafts of the manuscript.
I thank the following persons for their assistance with collecting fishes in the
Venezuelan Llanos: Andelo Barbarino, Linda Delashmidt, Terry Dye, Guillermo Feo,
Carter Gilbert, Oscar Leon, Craig Olds, Stewart Reid, Eric Sutton, Donald Taphom, and

Kirk Wmemiller. I am particularly grateful to Donald C. Taphom for providing both a
home and work area in Guanare, and for sharing his knowledge of the Venezuelan fish
fauna. He has always been unselfish in the sharing of fish specimens and field data from
his work in the Orinoco Llanos.
Most of my work in the upper Orinoco resulted from participation in expeditions as
part of a natural resource inventory of southern Venezuela, organized and sponsored by
Corporacin Venezolana Guayana Tcnica Minera (CVG-TECMIN). I thank all those
associated with CVG-TECMIN whose assistance made my work possible, for
administrative and logistic support these include Dr. Femando Susach, Victor Fernandez,
and Pedro Mata. For occasional help in the field, I express my sincere appreciation to
several members of the TECMIN technical staff, Angel Fernandez, Luz'Delgado, Andres
Garcia, Guillermo Fuenmayor, Sandra Giner, and Jesus Santiago. I relied heavily on the
fishing skills of my field assistants and camp workers hired by CVG-TECMIN: Fabian
Morillo, Yovani Aragua, Juan Carlos Castillo, Ambrosio Guayamore, Antonio Gaveln,
and Hilario Bolivar. Assistance in the upper Orinoco was also given by Dr. Basil Stergios,
Carlos Rivas, Carlos Templa, and Mike Dawson; many of the Yanomamo Indians
including Chirino, Pablo and Ramn, Cesar Timanaw, Ramn Pokorai; the Curipaco
Indians Carlos Antonio Guaruya, Eliasa Guaruya, and Eruerto Lpez; and many
individuals whose names I did not record. Together with my field assistants, their intimate
knowledge of the fishes, the rivers, and the forests of the upper Orinoco was invaluable to
me.
I thank Drs. William Fink and Antonio Machado-Allison for identification of
voucher specimens of many of the serrasalmine fishes, and for providing me with their
unpublished key to Venezuelan piranhas. I am also obliged to Dr. Donald Taphom for
identification of fish specimens, and to Dr. Basil Stergios, Gerardo Aymard, and Nidia de
Cuellar for identifying plant material. I thank Darryl Harrison for preparing base maps,
Angelina Licata for the fish drawings used in many of my figures, Kevin Schuck for help
iii

with computer drawing of dendrograms, and Craig Lilyestrom for help with a few of the
graphs and introducing me to the Macintosh computer.
Parts of my research were funded by National Geographic Society grants no. 3811-
88 and 4183-89. The Department of Zoology, University of Florida, provided additional
funds and equipment I thank all those in the Department of Zoology and Florida Museum
of Natural History who gave of their time. I thank George Burgess for use of his library.
The Universidad Nacional de los Llanos Occidentales and Museo de Zoologa (UNELLEZ-
MCNG) gave me lab space and administrative assistance in Venezuela. I am indebted to
many of the UNELLEZ administrators and staff for their help during the last ten years. In
addition, I thank the Venezuelan people, campesinos. Llaneros, and indgenas, for
allowing me do research in their beautiful country.
While conducting this study I came to know many very special people. During my
stay in Venezuela, I enjoyed the warm hospitality and friendship of Luis and Sioux Strebin,
Jose and Sharon Sutera, and Basil and Anita Stergios; along with Terry Dye, Donald
Taphorn, Lucas van Balen and his wife, and Dr. H. Kasem. they brought me through my
bout with falciparum malaria. I express appreciation to Dr. Horst Schwassmann and his
wife Satiko for frequently inviting me into their home during my passages through
Gainesville. I also thank Dr. Carter Gilbert and all my fellow graduate students, especially
Dennis Haney and Dr. Steve Walsh, for their many hospitalities. Finally, I thank my
parents and family for their constant love and support, both at home and during the many
long separations, and I thank Linda for always being there.
IV

TABLE OF CONTENTS
page
ACKNOWLEDGEMENTS ii
LIST OF TABLES vii
LIST OF FIGURES ix
ABSTRACT xii
CHAPTERS
1 INTRODUCTION 1
Introduction to Piranhas 1
Purpose of Present Study 3
Literature Review 7
Organization of Dissertation 16
2 ENVIRONMENTAL SETTING 18
The Orinoco River Basin 18
History of the Basin 22
The Low Llanos 24
The Upper Orinoco 28
Savannas and Forests During the Quaternary 30
Present Climate and Seasonality 32
3 METHODS 35
Field Sampling 35
Field Site Locations and Sampling Periods 37
Evaluation of Habitats 42
Identification and Nomenclature of Piranhas 43
Faunal Comparisons 47
Analysis of Diets 49
Nutrient Content Analysis of Food Items 53
Intestine Length 54
Field and Aquarium Observations 55
Statistical Analyses 55
4 COMPOSITION OF PIRANHA ASSEMBLAGES 57
v

CHAPTERS page
5 TROPHIC ECOLOGY OF SAVANNA PIRANHAS: THE APURE
DRAINAGE 71
Study Area 71
Species Accounts 75
Comparison of Diets 91
6 TROPHIC ECOLOGY OF PIRANHAS FROM THE UPPER
ORINOCO 97
Species Accounts 100
Summary of Upper Orinoco Trophic Patterns 123
Comparison with Savanna Populatons 131
Ecomorphological Correlates: Intestine Length and Diet 143
7 NUTRIENT VALUES OF PIRANHA PREY 148
Animal Matter 148
Plant Matter 153
8 DISCUSSION AND CONCLUSIONS 155
Composition of Piranha Assemblages 155
Trophic Patterns 163
Ecomorphological Correlates 175
A Phylogenetic Perspective 177
APPENDICES
A MATERIAL EXAMINED 181
B DATA ANALYSIS 191
LITERATURE CITED 198
BIOGRAPHICAL SKETCH 209
vi

LIST OF TABLES
Table page
1-1 Summary of principal field studies investigating piranha feeding and diets in
order of publication date 9
3-1 List of abbreviations used in figures and tables for piranhas and other
serrasalmine fishes 46
4-1 Occurrence of piranha species in samples from nine drainages in the
Orinoco River basin, Venezuela 59
4-2 Distance between drainages and Coefficient of Biogeographic Resemblance
among nine sampled drainages in the Orinoco River basin 62
4-3 Number of shared piranha species and Coefficient of Biogeographic
Resemblance among nine sampled drainages in the Orinoco River basin 64
4-4 Summary of piranha species occurrence by habitat and water type, based on
samples in Orinoco River basin, Venezuela 70
5-1 Food items of Pygocentrus caribe from the Apure River drainage (Cao
Caicara area) by size class 79
5-2 List of vertebrate prey taxa identified from the stomach contents of the four
most common piranhas from the Cao Caicara area, Apure River drainage,
in the low Llanos of Venezuela 80
5-3 Food items of Serrasalmus irritaus from the Apure River drainage (Cao
Caicara area) by size class 81
5-4 Food items of Serrasalmus medinai from the Apure River drainage (Cao
Caicara area) by size class 83
5-5 Food items of Serrasalmus rhombeus from the Apure River drainage (Cao
Caicara area) by size class 84
5-6 Food items of Serrasalmus elongatus from the Apure River drainage (Cao
Caicara area) by size class 86
5-7 Food items of Serrasalmus altuvei from the Apure River drainage (Cao
Caicara area) by size class 88
vii

page
Ia¡2k
5-8 Food items of Pristobrycon striolatus from the Apure River drainage (Cao
Caicara area) by size class 89
5-9 Food items of Catoprion ment from the Apure River drainage (Cao
Caicara area) by size class 90
5-10 Food items of small juvenile piranhas (Size Class I, 10-19 mm SL),
tentatively identified as Pygocentrus caribe, from the Apure River drainage
(Cao Caicara area) 92
5-11 Matrix of diet overlaps among different size classes of piranhas from Apure
River drainage, low Llanos 95
6-1 List of taxa identified from the stomach contents of the three most common
piranha species from upper Orinoco River drainages, Venezuela 103
6-2 Food items of Serrasalmus rhombeus from the upper Orinoco River basin
by size class 104
6-3 Food items of Serrasalmus manueli from the upper Orinoco River basin by
size class 107
6-4 Food items of Serrasalmus cf. eigenmanni from the upper Orinoco River
basin by size class Ill
6-5 Food items of Serrasalmus altuvei from the upper Orinoco River basin by
size class 113
6-6 Food items of Pristobrycon striolatus from the upper Orinoco River basin
by size class 115
6-7 Food items of Pygopristis denticulatus from the upper Orinoco River basin
by size class 118
6-8 Matrix of diet overlaps among different size classes of serrasalmine fishes
from upper Orinoco River drainages 124
6-9 Incidence of herbivory in piranhas (> 80 mm SL) as associated with the low
Llanos and upper Orinoco 136
6-10 One-tailed Mann-Whitney U-test results testing the prediction that piranha
species (> 80 mm SL) from upper Orinoco River drainages fed more on
plant material than those from the low Llanos 140
7-1 Estimates of the lipid, protein, ash, carbohydrate, and caloric contents of
fins, scales, and whole fish for two taxa of typical prey fish 149
8-1 Orinoco River basin piranhas categorized by adult diet 158
viii

LIST OF FIGURES
Figure page
1-1 Hypothesized phylogenetic relationships among genera of the subfamily
Serrasalminae as proposed by Machado-Allison (redrawn from Machado-
Allison 1985) 2
2-1 Map of northern South America showing Orinoco River basin 19
2-2 Major savanna and forest ecosystems in the Orinoco River basin 25
2-3 Approximate distribution of open savanna (low Llanos) in Venezuelan state
of Apure, Orinoco River basin 26
2-4 Approximate distribution of lowland forests in Federal Amazon Territory of
Venezuela 29
2-5 Monthly rainfall recorded at representative sites in Orinoco River basin,
Venezuela. (1) Upper Orinoco: monthly average 1971-1977 from Santa
Maria de Los Guaicas, mouth of Ocamo River, Federal Territory of
Amazonas, and (2) Low Llanos: for year 1972 from Cao Caicara area,
Apure River drainage. Apure State 34
3-1 Map of Venezuela showing nine selected drainages in Orinoco River basin
sampled during present study 38
3-2 Map of Apure State, Venezuela, showing principal low Llanos sampling
locations 39
3-3 Map of 1988-1991 sampling sites in upper Orinoco, Federal Territory of
Amazonas, Venezuela 41
4-1 Schematic representation showing relative distances among the nine
sampled drainages and their approximate location along Orinoco River main
channel 58
4-2 Scatter diagram showing relationship between number of piranha species
per drainage and log of the drainage area size (km2) for nine sampled
drainages in Orinoco River basin, Venezuela 63
4-3 Scatter diagram showing similarity in piranha species composition between
adjacent sampled drainages versus distance between adjacent drainages 65
IX

Figure page
4-4 Scatter diagram showing similarities in piranha species composition
between all possible paired drainages and the distance between paired
drainages 66
4-5 Dendrogram from cluster analysis depicting similarities among nine sampled
drainages of Orinoco River basin based on piranha species composition 67
5-1 Location of Cao Caicara study area, Apure River drainage, in low Llanos
of Apure State, Venezuela 72
5-2 General body form and major fin markings of seven piranha species (55-70
mm SL) and Catoprion ment from Cao Caicara study area, Apure River
drainage, in the low Llanos of Venezuela 73
5-3 Diets by size class of seven piranha species and Catoprion ment from Cao
Caicara study area, Apure River drainage, in the low Llanos of Venezuela 76
5-4 Diet breadths estimated for seven piranha species and Catoprion ment, by
size class, from the Cao Caicara area of the low Llanos, Apure River
drainage, Orinoco River basin, Venezuela 94
5-5 Dendrogram from cluster analysis depicting similarities among diets of
piranha species (by size class) from the Cao Caicara area of the low
Llanos, Apure River drainage, Orinoco River basin, Venezuela 96
6-1 Eight piranha species from the upper Orinoco River basin of Venezuela 98
6-2 Diets by size class (>40 mm SL) of eight piranha species from the upper
Orinoco River basin, Venezuela 101
6-3 Diets of selected small juvenile piranhas (10-19 mm SL) from upper
Orinoco River drainages and the low Llanos, Venezuela 108
6-4 Diets by size class (>80 mm SL) of four common serrasalmine species from
the upper Orinoco River basin: Catoprion ment, Mylens asterias, M.
schomburgkii, and M. torquatus 120
6-5 Dendrogram from cluster analysis depicting similarities among diets of
piranha and related species (by size class) from the upper Orinoco River
basin, Venezuela 127
6-6 Diet breadths estimated for eight piranha species, by size class, from the
upper Orinoco River basin, Venezuela 130
6-7 Diets by size class (>40 mm SL) of three piranha species from the Cinaruco
and Capanaparo river drainages of the low Llanos, Orinoco River basin,
Venezuela 133
x

page
Figure
6-8 Comparison of the proportion of plant material in the diets of carnivorous
and herbivorous piranha species (> 80 mm SL) from the low Llanos to
those from upper Orinoco River drainages in terms of percent adjusted
volume (%Va), percent dominance (%D), and percent frequency of
occurrence (%0) 138
6-9 Diets by size class (>40 mm SL) of Serrasalmus manueli comparing low
Llanos (Cinaruco drainage) and upper Orinoco populations 141
6-10 Scatter diagram showing relationship between mean intestine
length/standard length and percent volume of plant material in diet for
selected serrasalmine fish (>80 mm SL) 145
6-11 Scatter diagram showing relationship between intestine length and standard
length for the three most common piranha species in samples from the upper
Orinoco River basin of Venezuela 146
6-12 Scatter diagram showing relationship between intestine length and standard
length for Serrasalmus manueli comparing upper Orinoco and Llanos
populations 146
7-1 Bar graph comparing dry mass composition of small whole fish, scales and
fins 150
8-1 Proposed hypothetical model showing the dietary responses of carnivorous
versus herbivorous piranha species to changes in various habitat parameters
and food resources 171
8-2 Diets and intestine length mapped onto the proposed phylogeny of
Machado-Allison (1985) for genera of the subfamily Serrasalminae 179

Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
TROPHIC ECOLOGY OF PIRANHAS (CHARACIDAE: SERRASALMINAE)
FROM SAVANNA AND FOREST REGIONS
IN THE ORINOCO RIVER BASIN OF VENEZUELA
by
Leo G. Nico
December, 1991
Chairman: Dr. Horst O. Schwassmann
Major Department: Zoology
This study emphasizes interspecific and intraspecific comparisons of the trophic
ecology of piranhas (Characidae: Serrasalminae) from two vegetatively distinct regions in
the Orinoco River basin of Venezuela: (1) the upper Orinoco in the Federal Amazon
Territory, an area dominated by dense tropical forests, and (2) the low Llanos of Apure
State, a region characterized by immense open savannas. Eleven piranha species were
taken from the two regions studied. Since 1979, ten species have been collected from the
low Llanos of Apure State, whereas my 1989-1991 samples indicate that at least eight
species occur in the upper Orinoco. Seven species were widely distributed and inhabited
both regions. The high similarity in species composition between the two regions suggests
that there are really no distinct savanna versus forest piranha assemblages.
All piranhas exhibit changes in diet with age. The smallest juveniles, < 20 mm
standard length (SL), prey mainly on microcrustaceans and small aquatic insects. Older
juveniles of most species, between 20 and 80 mm SL, commonly eat fins. Fin eating by
xii

young piranhas is common in both the low Llanos and the upper Orinoco. Chemical
analysis indicated that fins are similar to scales in energy and protein content, but less than
that of small whole fish. Orinoco piranhas > 80 mm SL fall into two general dietary
categories: species that are primarily carnivorous and others that are largely herbivorous.
The seven carnivorous piranhas (Pygocentrus caribe, Serrasalmus altuvei, S. manueli, S.
rhombeus, S. elongatus, S. irritans, and S. medinai) feed heavily on fish or fish fins.
Adults of the four herbivorous species (.Serrasalmus cf. eigenmanni, Pygopristis
denticulatus, and two Pristobrycon spp.) are seed predators, biting seeds and hard fruits
into small fragments before ingesting them. Serrasalmus manueli was one of the few
carnivorous species that occasionally took seeds or fruit in mass. Overall, relative intestine
length differed among serrasalmine species and was closely correlated with diet Seed
eating piranhas tended to have long intestines, similar to those of highly herbivorous
Myleus, Mylossoma, and Metynnis species, but I found no significant difference in relative
intestine lengths between forest and savanna populations of S. manueli even though diets
differed.
Both carnivorous and herbivorous species are somewhat flexible in their use of
food resources. I found that upper Orinoco piranhas, at both the group and species levels,
exploit plant material more than piranhas from the low Llanos. Many piranhas, especially
those that are largely herbivorous, shift their diets in response to spatial as well as temporal
variation in the availability of fish prey versus plant food. Even though savanna and forest
regions have a similar piranha species makeup, herbivorous species are much more
common in forested regions. Nevertheless, even though seeds and fruits are a locally
abundant resource, assemblages of forest piranhas were typically dominated by one or two
large, highly carnivorous species (5. rhombeus, S. manueli, or both).

CHAPTER 1
INTRODUCTION
Introduction to Piranhas
Piranhas (Characidae: Serrasalminae) are neotropical freshwater fishes found in the
major Atlantic drainages of South America, from 10 North latitude in the Orinoco River
basin of Venezuela and Colombia, through the Amazon basin, and south in the La Plata-
Paraguay-Parana basin to about 35 South latitude. Called caribes in Venezuela, they
comprise a monophyletic group of at least 30 species in the genera Serrasalmus,
Pygocentrus, Pristobrycon and Pygopristis (Fig. 1-1) (Machado-Allison 1983, 1985, Fink
1988). Piranhas possess many unique morphological traits that distinguish them from
other serrasalmines (Machado-Allison 1985), but they are most easily recognized by their
unusual and impressive dentition. They have a single row of sharp, somewhat triangular
teeth in both jaws; the teeth are tightly packed, partially interlocking, and are typically used
for rapid puncture and shearing.
Examples of other serrasalmine fishes are species of Mylossoma, Myleus, and
Metynnis (silver dollars, pmpanos, palometas), the scale-eating characin Catoprion ment,
and the nearly one-meter long Piaractus brachypomas (morocoto) and Colossoma
macropomum (cachama or tambaqui). In contrast to the piranhas, the dental morphologies
of other serrasalmine fishes are variable. Most species have combinations of relatively
broad and strong molariform and incisive teeth, often with more than one row of teeth in
the upper jaw. Serrasalmine fishes are laterally compressed and most are fairly deep
bodied; however, maximum adult size, body shape, and color patterns vary among species.
Piranhas range from medium-sized fishes such as Serrasalmus irritans, some 20 cm from
1

Colossoma
A
B
Fig. 1-
Piaractus
Mylossoma
Myleus
Mylesinus
Utiarichthys
Acnodon
Metynnis
Catoprion
Pygopristis
Pygocentrus
Pristobrycon
Serrasalmus
- PIRANHAS
1. Hypothesized phylogenetic relationships among genera of the subfamily
Serrasalminae as proposed by Machado-Allison (redrawn from Machado-
Allison 1985).

3
tip of snout to base of tail (Standard Length, SL) to large species such as Serrasalmus
rhombeus, which grow to well over 35 cm SL. The general body form ranges from sharp
snouted and elongate, Serrasalmus elongatus, to blunt-headed and robust species such as .
the red-bellied piranhas Pygocentrus caribe of the Orinoco and P. nattereri of the Amazon.
Of the approximately thirty species of piranhas, at least twelve occur in the Orinoco
basin where, as in many other areas of tropical South America, they are exploited for
subsistence fisheries and also commercially. Piranhas occur in rivers and floodplains of
both open savannas and densely forested regions and often make up a high percentage of
fish biomass and numbers of individuals (Mago-Leccia 1970, Taphom and Lilyestrom
1984). Thus, they play a major role in the food web of many lowland aquatic
communities. Contrary to common belief that they are strictly carnivorous, piranhas and
their close relatives exploit a broad spectrum of food resources including arthropods, fishes
and other vertebrates, fish fins and scales, carrion, seeds, fruits, leaves, and flowers
(Goulding 1980, Sazima 1983, Sazima and Guimares 1987, Nico and Taphom 1988,
Winemiller 1989a, Sazima and Machado 1990). Serrasalmine fishes living in tropical
savannas encounter substantially different habitat conditions in comparison to those
populations occupying forested regions. Thus, comparative studies of piranha diets and
trophic ecology can provide insights into their responses and adaptations to the selective
forces of different environments
Purpose of Present Study
Tropical South America possesses the most diverse freshwater fish fauna of any
continent (Bohlke et al. 1978). Considering both described and undescribed taxa,
Lundberg et al. (1987) estimated that the Orinoco River basin alone probably contains
almost 1,000 fish species, more species than are found in all the freshwater systems of
temperate North America. Unfortunately, the extremely diverse faunas and floras of many

4
tropical environments are seriously threatened. Because of expanding human populations
and increased development, natural habitats are being destroyed or degraded at a rapid
pace. Forests are being cleared for agriculture, ranching, timber, and minerals; rivers and
their floodplains are being modified by dams, levees, and pollution. Aquatic and terrestrial
systems in the lowland tropics are intricately interwoven, the changes to each inevitably
affecting the other. The profound and likely irreversible changes now occurring
throughout tropical America make it increasingly important to understand more about the
interrelationships between tropical environments and their diverse fauna and flora. Such an
understanding is necessary for successful conservation of habitats, species, and genetic
stocks.
The science of ecology attempts to understand the complex interrelationships
between an organism and its physical and biotic environment. Studies in trophic ecology
are a way to investigate such interrelationships, and often permit analysis at several levels
or scales. Obviously, what an animal eats is limited by the kinds and availability of food
resources in its local surroundings. Valid interpretations of feeding patterns, however, also
require consideration of past environmental conditions, inasmuch as the probability of an
animal taking a particular type of prey depends on its array of interrelated morphological
and behavioral characters that result from its particular phylogenetic history. Trophic
studies provide insights into the biology of organisms, because food, unlike many other
resources or niche parameters, can be measured, analyzed, and compared in a large number
of ways using a variety of techniques. Evidence for the importance and practicality of
research on trophic ecology is provided by the tremendous volume of literature on the
subject (for review of fishes see Ross 1986). Accordingly, the study of diets and food
resources has contributed to the development of many ecological concepts, including
resource partitioning, niche theory, optimality theory, energetics, food webs, and predator-
prey relationships.

5
The aim of this study is to increase our knowledge of the ecology and natural
history of piranhas and a few of their close relatives. I have attempted to document and
explain similarities and differences in trophic ecology within and among closely related
species by comparing populations from two floristically distinct regions of the Orinoco
River Basin of Venezuela: (1) the upper Orinoco, an area dominated by dense forests, and
(2) the low Llanos of Apure State, a region characterized by immense open savannas.
Piranhas are widely distributed geographically and very abundant in many lowland
tropical habitats, but we know relatively little about their ecology, behavior, and natural
history. Goulding (1980) found many fishes in the Amazonian forest ecosystems,
including several piranhas, to be herbivorous or omnivorous and to depend heavily on
flooded forests for food resources. Influenced by Goulding's findings.' Donald Taphom
and I began, in late 1983, to study the trophic ecology and natural history of piranhas and
other fishes in savanna ecosystems of the Venezuelan Llanos (Nico and Taphom 1988,
Nico 1990). Although my initial research on piranhas focu.-ed on savanna regions in the
Orinoco Basin, I also made visits to southern Venezuela and the Rio Casiquiare in 1985,
and to Marajo Island in the lower Amazon of Brazil in 1986. Subsequently, between May
1988 and March 1991,1 participated in five expeditions to the upper Orinoco basin and its
forests to broaden my investigation of the feeding ecology of Orinoco piranhas as related to
their habitat
Waters of the low Llanos are typically high in fish and invertebrate biomass, and
many sites support large numbers of carnivores (Mago-Leccia 1970, Taphom and
Lilyestrom 1984, Machado-Allison 1987, Saunders and Lewis 1988, Rodriguez and Lewis
1990). However, large woody plants are uncommon, and in conjunction with water stress
caused by the yearly dry periods, production of seeds and fruits is highly seasonal
(Sarmiento 1984). As a result, availability of plant materials, especially fruits and large
seeds, as food for savanna fishes is low, markedly seasonal, and very localized (personal
observations). On the other hand, the few phenologieal studies of wet forests in lowland

6
areas of tropical South America (Terborgh 1983, Goulding et al. 1988, Janson and
Emmons 1990), or information gleaned from botanical exploration of the upper Orinoco
(B. Stergios, personal communication), suggest that such habitats make a wide variety and
abundance of fruits and seeds available to fishes during most of the year (Goulding 1980,
Goulding et al. 1988). Even though species diversity is often high in the upper Orinoco,
our collections made with a variety of fishing gear indicate that fish biomass in tropical
forest regions is generally lower than in the low Llanos.
If present ecological conditions are important, environment should strongly
influence both species composition and trophic ecology of piranha assemblages in
particular regions. Accordingly, comparisons of piranhas from the more heavily forested
upper Orinoco basin with those from the open savannas or low Llanos were made to
address the following questions: (1) Do the same species of piranhas occur in both
savanna and forested regions? (2) Do diets differ, and, if so, are fish from populations in
forested habitats significantly more herbivorous than their savanna counterparts? (3) Do
ontogenetic shifts in diet occur and, if so, how do they compare among species and do they
correlate with regional environments? (4) Because gut length is often an indicator of
natural diet in vertebrates (i.e., longer in herbivores), is intestinal length of piranhas and
other serrasalmine fishes correlated with diet? (5) What are the nutritional benefits
associated with different diets or food preferences (e.g., scale- or fin-eating versus flesh
eating)? (6) How do diets of piranhas compare with other serrasalmine species? (7) What
is the relationship between piranha ecology and serrasalmine phylogeny?
The comparative approach is useful in helping us understand aspects of the
evolution and adaptations of closely related species (Clutton-Brock and Harvey 1984,
Huey and Bennett 1986). Recent comparative studies in tropical vertebrate ecology have
focused on birds (Schluter 1988), mammals (Terborgh 1983), and reptiles and amphibians
(Duellman 1990). An objective in many comparative studies is discovery of evolutionary
trends in morphological and behavioral adaptations to different environments, thereby

7
making it possible to recognize how particular characters arise under the influence of
contrasting selective forces (Clutton-Brock and Harvey 1984). Furthermore, comparisons
across a broad biogeographical scale offer what Wiens et al. (1986) suggested as perhaps
the best opportunity to understand a species' limits or responses to different environmental
conditions, revealing patterns that suggest something of its adaptive abilities or
evolutionary potential.
Literature Review
The following is a brief review of the literature relating to piranha feeding behavior
and trophic ecology. A summary of field studies investigating piranha feeding and diets is
given in Table 1-1. Unless otherwise stated, scientific names are as used in the original
literature. All references to Serrasalmus nattereri should be Pygocentrus nattereri.
Early naturalists and explorers were the first to report on piranhas, and most
accounts, such as those by Alexander von Humboldt, Henry Bates, and Theodore
Roosevelt, were primarily devoted to describing attacks by piranhas on animals and
humans, or relating the destruction done by piranhas to fishing gear (Bates [1863]
1975:202, Roosevelt 1914). Humboldt, who traveled extensively in South America
between 1799 and 1804, wrote the following passage while on the Orinoco River:
On the morning of the 3rd of April our Indians caught with a hook the fish
known in the country by the name of caribe* [*Caribe in the Spanish
language signifies cannibal], or caribito, because no other fish has such a
thirst for blood. It attacks bathers and swimmers, from whom it often bites
away considerable pieces of flesh. The Indians dread extremely these
caribes; and several of them showed us the scars of deep wounds in the calf
of the leg and in the thigh, made by these little animals. They swim at the
bottom of rivers; but if a few drops of blood be shed on the water, they rise
by thousands to the surface, so that if a person be only slightly bitten, it is
difficult for him to get out of the water without receiving a severer wound.
Humboldt ([ 1816-1831 ] 1971:166-167)

8
Eigenmann (1915), Eigenmann and Allen (1942), and Myers (1972) have reviewed
many of the earlier stories about piranhas. Although published anecdotal information
brought notoriety to this group of South American fishes, early accounts did not
significantly contribute to our knowledge of piranha biology and natural history, and many
stories simply aided to perpetuate myths about piranha ferocity.
There have been a moderate number of studies that have addressed the natural diets
of piranhas (Table 1-1). Most of these have focused on only one or a few of the most
common and widespread species, from a single locality or region. The diets of several of
the more uncommon species have never been described. Most studies of piranha diets have
been of fishes inhabiting artificially altered environments. Because a few of the more
common piranha species seem to flourish in man-made lakes, several studies focused on
populations inhabiting reservoirs or impoundments. Work on piranhas has also been done
in watersheds modified to some extent by cattle ranching, agriculture, and by construction
of roadways. Few investigations have been carried out in pristine habitats.
Several of the earliest efforts to characterize piranha diets were carried out in the
Jaguaribe River basin, a coastal drainage located in northeastern Brazil. The first was that
of Menezes and Menezes (1946). Along with information on several other species, they
presented a simple listing of food items, primarily fish remains and insects, found in the
stomachs of 138 specimens of a single piranha species taken in 1944 from the Lima
Campos Reservoir in Cear State. First identified by Menezes and Menezes as Serrasalmo
immaculatus, Braga (1954) later indicated the species was Serrasalmus rhombeus. Braga
also studied Lima Campos piranhas. He recorded the frequency of occurrence and volume
of stomach contents of a large sample of S. rhombeus (n = 2,222; 100-290 mm total
length) during a 12-month study, 1952-1953 (Braga 1954). Of the 1,713 individuals
containing food, predominant food items were freshwater shrimp (Palaemonidae) and fish,
65 and 28 percent of the total food volume, respectively. Braga later published results
from other studies on piranhas in a single volume (Braga 1975), providing diet information

Table 1-1. Summary of principal field studies investigating piranha feeding and diets in order of publication date. All studies based on
analysis of stomach contents unless otherwise indicated. Most measured size as standard length in mm, if not, size given as total length
(TL) or weight in grams (g). Scientific names are as used in original literature unless marked with asterisk (*) (also see nomenclatural
changes discussed in Chapter 3).
Basin
Site or
Study Period and
Species
No. Examined
Comments
Source
(State, Country)
Habitat
Duration
(Size range)
1. Jaguaribe
(Cear, Brazil)
Lima Campos
Reservoir
1944, May to
October
1) Serrasalmo immaculatus
(^Serrasalmus rhombeus)
n= 138
(wt: 10-215 g)
Diet consisted mainly of fish
remains
Menezes and
Menezes (1946)
2. Jaguaribe
(Cear, Brazil)
Lima Campos
Reservoir
12-month study,
1952-1953
1) Serrasalmus rhombeus
n = 2,222
(100-290 TL)
Fed mainly on shrimp and fish
Braga (1954)
3. Essequibo
and Amazon
(Guyana)
Rupununi
Savanna, savanna
pools
Intermittent 1957,
1958, and 1961
(~2 months total)
1) Serrasalmus nattereri,
2) S. rhombeus
3) S. gymnogenys
4) Pygopristis denticulatus
Number examined
not given
Reduced feeding found during dry
season
Lowe-
McConnell
(1964)
4. Paran
(Argentina)
Middle Paran
rivers, lagoons (?)
Intermittent
1962 to 1966
1) Serrasalmus spilopleura
2) S. nattered
n = 104 (3-657 g)
n = 21 (10-200 g)
Diet of mostly fish
Bonetto et al.
(1967)
5. Amazon
(Par, Brazil)
Three sites: Lago
Jacup, no data on
other two
1967 (?)
1) Serrasalmus elongatus
n = 7 (89-152)
All contained fins, some scales;
fins major item in all but two
Roberts (1970)
6. -Jaguaribe
(Cear, Brazil)
Three reservoirs:
Roque de Macdo,
Cruzeiro do Sul,
Assis Machado
Intermittent 1970-
1972: Nov. 1970,
May 1972, other
date?
1) Serrasalmus nattered
n = 500
(125-370 TL)
Fed mainly on fish (small
characins)
Braga (1975)
7. Napo-Amazon
(Ecuador)
Rio Aguarico
floodplain lakes,
side channels
Intermittent
1967 and 1968
(~3 1/2 months)
1) Serrasalmus nattered
2) S. marginatus
n = 6 (30-321)
n = 4 (45-224)
1) fish remains and insects
2) fish remains
Saul (1975)

Table l-l--continued.
Basin
(State, Country)
Site or
Habitat
Study Period and
Duration
Species
No. Examined
(Size range)
Comments
Source
8. Amazon
(Amazonas,
Brazil)
Madeira River
drainage
Rio Machado
(rivers, flooded
forest)
1977 and 1978
high and low
water; 1979 high
water
1) Serrasalmus rhombeus
2) S. elongatus
3) S. serrulatus
4) S. cf.striolatus
5-7) Serrasalmus spp.
n = 254 (180-370)
n = 67? (140-220)
n = 36 (130-250)
n = 9 (150-200)
n = 5? (no data)
Adults of some species highly
carnivorous, other species feed on
seeds and fruits; concluded all or
many omnivorous
Goulding
(1980)
9. Tiet River
(So Paulo,
Brazil)
Bariri
Reservoir
Sampled four
seasons of year,
Jan. to Dec. 1979
1) Serrasalmus spilopleura
n = 299 (75-295
TL)
Study of seasonal changes in
average stomach fullness,
heaviest feeding in Summer.
Mota et al.
(1982)
10. Atibaia
River (Sao
Paulo, Brazil)
Americana
Resevoir
Feb. to Apr. 1983
1) Serrasalmus spilopleura
n = 41
(10.5-19.5)
Stomach contents of larval and
small juveniles, feeding behavior
of juveniles in aquaria
Sazima and
Zamprogno.
(1985).
11. Amazon
(Par, Brazil)
Curu-Una
Reservoir
Three collections,
Aug., Nov., 1982
Feb. 1983
1) Serrasalmus rhombeus
n = 250 (50-320)
Compared diets among five sites
in reservoir, mainly fed on fish,
one site aquatic insects
Ferreira (1984b,
also see 1984a)
12. Orinoco
(Guaneo,
Venezuela)
Apure drainage
savanna lagoon
Intermittent
1982-1984
wet seasons
1) Pygocentrus notatus
2) Serrasalmus rhombeus
3) Pristobrycon striolatus
n = 44 (10-100)
n = 50 (10-100)
n = 40 (10-100)
Juvenile diets, smallest fed on
microcrustaceans; larger ate fins,
scales, fish flesh, small seeds
Machado-
Allison and
Garcia (1986)
13. Paran
(S3o Paulo
Brazil)
Tiet drainage
Americana
Reservoir of
Atabaia River,
Intermittent
1982 to 1984
1) Serrasalmus spilopleura
n = 115?
(10-207)
Diet mainly fins, scales, fish
flesh, and whole fish
Northcote et al.
(1986, 1987)
14. Paran
(Mato Grosso,
Brazil)
Pantanal region
1985 and 1986
1) Pygocentrus nattereri
2) Serrasalmus spilopleura
Not applicable
Investigated three reported cases
of piranhas scavenging on human
corpses
Sazima and
Guirnaraes
(1987)
o

Table l-l--contnued.
Basin
(State, Country)
Site
Habitat
Study Period and
Duration
Species
No. Examined
(Size range)
Comments
Source
15. Orinoco
(Apure,
Venezuela)
Apure drainage,
savanna streams,
pools, flooded
savanna; cattle
ranch
Intermittent from
1979 to 1986, all
months sampled
1) Pygocentrus caribe*
2) Serrasalmus medinai*
3) S. irritans
4) S. rhombeus
5) S. elongatus
6) S. altuvei
7) Pristobrycon striolatus
Unidentified juveniles
n = 516 (20-280)
n = 124 (31-150)
n = 271 (22-162)
n = 51 (20-235)
n = 42 (23-175)
n = 10 (55-155)
n= 16 (21-159)
n= 114(10-19)
Ontogenetic changes in diet,
smallest fed on microcrustaceans,
most large juveniles ate fins,
adults were mainly piscivores.
Plant material not important in
diet (see Chapter 5)
Nico and
Taphorn (1988)
(see Chapter 5)
16. Amazon
(Amazonas,
Brazil)
lower Rio Negro
beaches, lakes,
swamps, flooded
forest
Intermittent 1979
to 1987
Six piranha species (not
identified)
n = 392 ?
(size range not
given)
Part of larger study, piranhas fed
on fish and plant matter
Goulding et al.
(1988)
17. Orinoco
(Portuguesa,
Venezuela)
Apure drainage
small seasonal
stream; cattle
ranch
~ 12-month
1984
1) Pygocentrus caribe*
2) Serrasalmus medinai*
3) Serrasalmus rhombeus
4) Serrasalmus irritanss
n = 230 (20-200)
n = 68 (20-80)
n = 50(20-200)
n = 76 (20-150)
Piranhas taken 8 of the 12
months, mostly juveniles.
Ontogenetic changes in diet
documented
Winemiller
(1989a)
18. Paran
(Mato Grosso,
Brazil)
Pantanal region
Paraguai drainage
Clearwater pools
and creeks:
Intermittent from
1981 to 1989,
mostly during wet
season
1) Serrasalmus marginatus
2) S. spilopleura
3) Pygocentrus nattereri,
n = 13 (63-146)
n = 26 (64-160)
n = 24 (80-240)
Stomach contents presented and
detailed underwater observations
totalling 314 hours
Sazima and
Machado (1990)
19. Orinoco
(Apure,
Venezuela)
Apure drainage
small seasonal
stream; cattle
ranch
24-hour period,
August 4-5, 1988
wet season
1) Pygocentrus caribe*
n = 123 (40-68)
24-hour diel study of juvenile
feeding; fed mostly on small fish
and aquatic insects, peak feeding
in morning
Nico (1990)

12
on S. nattereri from three other reservoirs of the Jaguaribe basin. In that work, Braga
concluded that piranhas were carnivorous, preferring to feed on other fishes, although they
also prey on other vertebrates (i.e., birds and amphibians), some invertebrates, and only
occasionally on plant material, such as seeds, parts of leaves, and algae.
Bonetto et al. (1967) reported on the feeding habits of two piranhas, Serrasalmus
spilopleura (n = 104) and S. nattereri (n = 21), taken from the middle Paran River and its
floodplain in Argentina. Both species fed predominantly on fish, but prey were not
identified to lower taxa. Stomachs of many of the individuals examined contained small
amounts of plant material, for example, roots and leaves of the aquatic plant Salvinia sp.
and roots of Eichhornia sp. (water hyacinth); however, these items were thought to have
been taken accidentally during capture of their principle prey.
Lowe-McConnell (1964) studied the ecology of fishes in the Rupununi savanna of
the Essequibo River basin, British Guiana (present day Guyana). Although not focusing
on fish diets, she briefly mentioned that the stomachs of fishes trapped in drying pools,
including the piranhas Serrasalmus nattereri, S. rhombeus, and Pygopristis denticulatus,
contained only mud and bottom debris; however, these same fishes had large amounts of
body fat. From her work in the Essequibo River drainage, Lowe-McConnell concluded
that the dry season was a period when fishes exhibited reduced feeding and high diet
overlap.
Roberts (1970) was the first to report on the more unusual feeding practices of
piranhas when he found large amounts of fins and some scales in the stomachs of seven
Serrasalmus elongatus from several sites in the Amazon River basin. He also discussed
scale-eating by the serrasalmine Catoprion ment. Saul (1975) collected two piranha
species during his study of habitat and food preferences of fishes at a site along the
Aguarico River, a tributary of the Napo River in the western Amazon Basin, Ecuador. He
found the stomachs of Serrasalmus nattereri (n = 6) to contain fish remains and insects;

13
those of S. marginatus (n = 4) held fish and fish remains. Both species were found
primarily in floodplain lakes or side channels, as opposed to the main river.
The relationship between piranha feeding patterns and environment had not been
investigated in any detail, however, until Goulding (1980) studied the diets of medium and
large-sized adult fishes, including seven piranha species, from in and around the Machado
River, a Clearwater tributary of the turbid-water Madeira River in Amazonia Brazil, a region
of seasonally inundated forests. He found that large Serrasalmus rhombeus (n = 254), the
most common piranha taken, were primarily piscivores that often bit chunks of flesh out of
large fish. Of added interest, fruits and seeds made up an estimated 10 percent of the total
volume of food eaten by S. rhombeus. Adult S. elongatus (n = 85) collected by Goulding
were similar to the juveniles examined by Roberts in that they had fed heavily on fins and
scales. Goulding reported that five of the seven species fed heavily on seeds, which they
masticated before swallowing. These five piranhas, which were relatively uncommon in
samples, included Serrasalmus serrulatus (n = 36), Serrasalmus cf. striolatus (n 9), and
three unidentified Serrasalmus species (n = 5?). Goulding concluded that Amazonian
fishes had evolved a close interrelationship with lowland forests, and that many fishes
depended on flooded forests for food in the form of fruit, seeds, and other allochthonous
materials. In addition to being seed predators, Goulding (1983) later indicated that
piranhas sometimes took seeds whole, and suggested that these fish also acted in dispersal
of seeds.
After Goulding completed his work in the Madeira River basin, he was joined by
Carvalho and Ferreira (Goulding et al. 1988) in a study on the natural history of
Amazonian fishes in habitats associated with the main channel of the lower Rio Negro. Of
approximately 450 species taken in the Rio Negro, six were piranhas. They did not
discuss piranha diets in much detail, but reported that fin and scale eating by adult piranhas
seemed to be common. Their collections of juvenile piranhas from the Rio Negro are yet to

14
be analyzed. In the published proceedings of a symposium Leao et al. (1989) reported on
the morphology, reproduction, and diet of Serrasalmus altuvei from the Rio Negro.
Sazima and his colleagues have explored the behavior of piranhas and related
species, particularly in reference to fin and scale-eating, through laboratory work with
captive fishes and underwater observations of free-living fishes in the Pantanal region,
western Brazil (Sazima 1983, 1986, 1988; Sazima and Zamprogno 1985, Sazima and
Pombal 1988, Sazima and Machado 1990). Sazima and Guimares (1987) recognized
Pygocentrus nattereri and Serrasalmus spilopleura as scavengers, feeding on dead and
sometimes decaying fishes, birds, and mammals. They suggested that deaths of humans
attributed to piranhas might often be the result of scavenging on victims already dead from
drowning or other causes. Sazima and Machado (1990) presented data from their
underwater observations on the behavior of three species, S. marginatus, S. spilopleura,
and P. nattereri, with emphasis on their predatory tactics, feeding behavior, and social
interactions while foraging.
Ferreira (1984b) studied the food and feeding habits of the principal fish species
inhabiting the Curu-Una River Reservoir, in the Amazon Basin near Santarm, Brazil.
Ferreira found that the diet of Serrasalmus rhombeus, taken from five localities in the
reservoir, showed slight differences among stations, feeding mainly on fish at four sites,
and on aquatic insects (i.e., ephemeroptera) at a fifth locality. In total, 250 specimens
were examined (ranging from 50 to 320 mm SL) of which 196 piranhas contained food.
Northcote et al. (1986, 1987) reported fin feeding by Serrasalmus spilopleura from
the Americana Reservoir, an impoundment on the Atibaia River in southeastern Brazil.
Analysis of prey fishes with damaged fins showed that S. spilopleura usually nip the lower
lobe of fins, indicating that attacks are made from below and behind prey fishes. They also
suggested that 5. splilopleura was the main, if not the only, fin-feeder in the reservoir fish
community. Mota et al. (1982) studied the seasonal variation in the intensity of feeding, as
measured by stomach fullness, of 5. spilopleura from the Bariri Reservoir in Sao Paulo

15
State, Brazil. They reported that heaviest feeding took place during the summer months
with a corresponding heavy build up of body fat by autumn.
Several recent works dealing with piranhas in the Venezuelan Llanos have
documented diet shifts during ontogeny (Machado-Allison and Garcia 1986, Nico and
Taphom 1988, and Winemiller 1989a). All found that early juveniles ate principally
zooplankton, while older individuals were predominantly piscivores. In addition to
discussing ontogenetic changes in dental morphologies, Machado-Allison and Garcia
(1986) examined 134 specimens, mostly juveniles, of three species (Pygocentrus caribe
Pristobrycon striolatus, and Serrasalmus rhombeus) taken from the Camagun lagoon, a
large wetland between the Portuguesa and Apure rivers, Guarico State. Predominant food
items, in terms of frequency of occurrence, of young piranhas were microcrustaceans,
aquatic insects, fins, and scales. In addition, they found small seeds (i.e., Cyperaceae) in
the stomachs of 33 of 134 specimens, but did not provide information on volume and
numbers of seeds eaten. Nico and Taphom (1988) examined the diets of seven piranha
species from streams and flooded savannas in the western Llanos of the Orinoco River
Basin. Their work suggested that savanna piranhas do not depend on fruits and seeds as
had been reported by Goulding (1980) for piranhas in flooded tropical rain forests. Nico
and Taphom found that juveniles and sub-adults of six of seven piranhas from a single
locality fed heavily on fins. Winemiller (1989a) studied the fish community of Cao
Maraca, a seasonal stream in the Apure River drainage that meanders through a region of
wooded savannas used for cattle ranching and cropland in Portuguesa State. His findings
on four piranha species (P. caribe, S. irritaos, S. rhombeus, and S. medinai), mostly
juveniles and sub-adults, supported the earlier work of Nico and Taphom.
For the most part, piranhas have been found to be daytime feeders, usually most
active during twilight periods (Lowe-McConnell 1964, Goulding 1980, Barthem 1987,
Nico 1990, personal observations). Barthem (1987) reported on activity patterns of several
vrzea lake fishes from near Manaus, Brazil. His results, based on -analysis of gillnet

16
catches, suggest an early morning peak of activity in Pygocentrus nattereri, Serrasalmus
elongatus, and S. rhombeus, and a late afternoon peak for the latter two species. Nico
(1990) found that young Pygocentrus notatus ( = P. caribe) had a peak feeding activity in
the morning, whereas adults seemed to be more active near dusk.
Intestine length of a few piranha species has been measured by Braga (1954),
Luengo (1965), Bonetto et al. (1967), and Jgu and dos Santos (1988). Braga reported
that the digestive tract of Serrasalmus rhombeus averaged 1.4 times the standard length.
Luengo (1965), relating intestine length to natural diet, reported that the highly carnivorous
Serrasalmus nattereri ( = Pygocentrus caribe) taken in the Venezuelan Llanos had a short
intestine compared with that of Prochilodus reticulatus (= Prochilodus mariael), a
prochilodid fish that feeds primarily on organic mud and detritus. Martinez (1976:67)
studied the anatomy of what was identified as Serrasalmus nattereri ( = Pygocentrus caribe)
and reported 10 to 12 intestinal caeca originating near and slightly past the pylorus. In a
taxonomic treatment, Jgu and dos Santos (1988) provided information on intestine length
and number of pyloric caeca for several piranha species from the Rio Tocantins of Brazil,
but they did not suggest dietary correlations.
Organization of Dissertation
The content and sequence of the chapters reflect the major components of my study.
Chapter 2 provides an overview of the Orinoco River basin and describes the environment
of the two study regions. Chapter 3 identifies the study sites and details field and
laboratory methods used. Chapter 4 compares the species composition of piranha
assemblages between the two regions and among the different drainages. Chapter 5
presents results from long-term studies on the trophic ecology and natural history of
savanna populations of piranhas from a site in the Apure River drainage. Chapter 6
focuses on the trophic ecology of populations of serrasalmine fishes from six drainages in

17
the upper Orinoco River Basin, a region characterized by extensive forests that undergo
seasonal flooding. In addition, my findings from the upper Orinoco are compared to
results from my studies of savanna populations, including data on a few savanna species
not reported in previous studies. Chapter 7 then gives results of an analysis of the nutritive
values of various food items commonly taken by piranhas. Finally, Chapter 8 summarizes
the major findings of the study, and attempts to interpret and synthesize the results in terms
of relevant mechanistic, ecological, and evolutionary issues.

CHAPTER 2
THE ENVIRONMENTAL SETTING
In this chapter I give an overview of the Orinoco River basin and describe the two
regions dealt with in the present study: (1) the open savannas or low Llanos of Apure
State, and (2) the upper Orinoco in the Venezuelan Federal Territory of Amazonas, an area
dominated by forests. Little is known about the geological and ecological history of
tropical lowlands in South America (Whitmore and Prance 1987). Because historical
events undoubtedly influenced present-day ecological patterns, I briefly review several
hypotheses concerning the basin's and the river's formation, as well as climatic and
vegetation changes that purportedly took place in northern South America during the recent
past.
The Orinoco River Basin
The Orinoco River, although dwarfed by the Amazon, is a major tropical river. The
basin is located in northern South America between 2 and 10 N latitude, and empties into
the Atlantic Ocean (Fig. 2-1). The Orinoco's mean annual discharge is about 35,800
m3/sec from a drainage area of approximately 1,100,000 km2, located in Venezuela (70%)
and Colombia (30%) (Lewis 1988). Compared to the Mississippi River, the Orinoco has
more than twice the annual discharge, yet drains an area of only one-third the size. The
basin is geologically and ecologically diverse, having large mountain ranges and broad
low-lying plains, with habitats ranging from immense open grasslands to lush tropical
forests.
18

Fig. 2-1. Map of northern South America showing Orinoco River basin.

20
The headwaters of the Orinoco are traditionally considered to be in southern
Venezuela where it receives water from both the western slopes of the Guyana Shield and
from extensive lowland areas dominated by deciduous or evergreen tropical forest. In
contrast, most tributaries in the northern and western parts of the basin originate in the
Andes and adjoining coastal mountains and then flow through the Llanos, a vast alluvial
plain supporting tropical savanna vegetation. The main channel of the Orinoco forms an
unusual U-shaped pattern, the river winding around the western borders of the Guyana
Shield. From its source the Orinoco flows several hundred kilometers west-northwest until
it is met by the Atabapo and Guaviare rivers; here the river makes an abrupt turn to the
north. Along its northward segment the Orinoco forms the border between Colombia and
Venezuela.
At about 530'N latitude the river courses through several series of treacherous
cataracts near Puerto Ayacucho, the most prominent being the Atures Rapids where the
river drops 17.5 m over a distance of 9.3 km (CODESUR 1979). The Atures Rapids and
the other cataracts are spread along a reach of nearly 100 km, marking the boundary
between the upper and lower sections of the Orinoco. Farther downstream the Orinoco is
joined from the west by the Meta, Cinaruco, Capanaparo, and Apure rivers as it gradually
swings to the east. Finally, below the confluences with the Caura and Caroni rivers the
Orinoco arrives at its large delta. Here the huge main river is subdivided into a multitude of
smaller channels that empty into the Atlantic Ocean near the island of Trinidad. The main
causeway of the Orinoco, from its origin in the Sierra Parima in the Guyana Shield to its
mouth, is estimated to be 2,140 km long (DISCOLAR 1983). High-order tributaries
draining highland areas of the Andes and the Guyana Shield are characterized by large
numbers of waterfalls, rapids, and fast-flowing waters. However, the larger streams and
rivers common to lowland areas typically have slight gradients. The upper Orinoco, at the

21
community of La Esmeralda, nearly 1,800 km by river from the sea, is only 135 m above
sea level, an average drop of less than 1 m for every 10 km of river.
In summary, large rivers of lowland forests that feed the upper Orinoco from the
south include the Mavaca and Atabapo rivers. Big-river tributaries originating in the
Guyana Shield and feeding into the upper Orinoco include the Ocamo, Padamo,
Cunucunuma, Ventuari, and Sipapo; those flowing into the lower Orinoco include the
Caura and Caroni rivers. Large tributaries of the Orinoco that originate on or near the
Andean slopes are the Inirida, Guaviare, Vichada, Tomo, Meta, Cinaruco, Capanaparo,
Arauca, and Apure rivers. About 31 percent of the upper Orinoco volume is continually
diverted into the Amazon basin by way of the Brazo Casiquiare, a natural canal
(CODESUR 1979).
In addition to a diverse flora and topography, the Orinoco River basin is a mosaic
of water types. Alfred Russel Wallace ([1853] 1972) was one of the first to mention the
striking differences in water colors among the various South American waters using the
terms whitewater, blackwater, and Clearwater rivers. In a later and more detailed analysis,
Sioli (1975, 1984) summarized differences among these three water types based on
differences in water color, amount of suspended matter, and chemical properties.
Whitewater streams are turbid because of inorganic sediments, of milk-coffee color (cafe
con leche), relatively rich in nutrients, and of near neutral pH. Blackwater streams are
transparent but reddish brown, the color of tea due to humic acids (the color appears black
where water runs deep), very poor in nutrients and very acidic. Clearwater streams are
also transparent, often greenish in color, typically poor in nutrients, and have a pH that can
range from slightly acidic to slightly alkaline.
In the Orinoco River basin, whitewater and blackwater habitats predominate. Clear
waters are more typical of small caos and the upland reaches of certain rivers. However,
the classification of rivers by water color is not always easy to apply and thus the
usefulness Sioli's classification scheme is somewhat limited. Many, rivers are a mixture of

22
two or more of the basic water types; some change seasonally as flows from a diverse array
of smaller tributaries rise and fall. For example, during high water the Guayapo River of
the Sipapo drainage changes from a Clearwater river in its upper and middle reaches to a
blackwater river in its lower segments, due to increased input of tannin-stained waters from
adjacent flooded forests. To a large extent, the hydrochemistry of the Orinoco tributaries is
controlled by the geomorphological and floristic character of their watersheds. In general,
rivers of the Andes and Llanos are high in suspended sediments, whereas streams
originating in the weathered Guayana highlands and the forests of the upper Orinoco
transport low sediment loads. Nevertheless, exceptions to the above-mentioned
hydrochemical pattern can be found in all regions as a result of local conditions.
History of the Basin
The details and precise timing of geological events involved in the formation of the
Orinoco River basin are not well understood. The oldest land form in the basin is the
Guyana Shield, ancient mountains composed of Precambriun material that underwent
additional uplift and exposure during the Tertiary (Whitmore and Prance 1987). Because
they have been exposed for many millions of years, these highlands have been heavily
worn and dramatically shaped by erosion. The mountains of the Andes were created later,
uplifted as a result of plate tectonic events during the Miocene-Pliocene, 2-8 million years
ago (Whitmore and Prance 1987:7). The Llanos are thought to be the most recent major
topographical feature in the basin. During Quaternary periods of raised sea-level
(interglacials) the Llanos plains were the bed of a large interior sea. Thus, similar to many
lowland areas in South America, these central plains are primarily composed of Quaternary
sediments that mantle Tertiary and older sediments, with recent additions of alluvial river
deposits carried down from the surrounding mountains during the Pleistocene (Beek and
Bramao 1968:86, Walter 1973: 72-73, Cole 1986).

23
An ancient Orinoco River is thought to have flowed to the northwest, emptying into
the Caribbean before the Miocene uplift of the Andes near or through the present day
Maracaibo Lake Basin. In addition to geologic evidence, this idea of a northward flow has
received added support from comparisons of fossil and living fishes found in northern
Colombia and Venezuela (Lundberg et al. 1986, 1988). According to the proposed
scenario, the river slowly shifted to the east some time between the Late Cretaceous and
early Oligocene, finally assuming its present course by the Oligocene epoch, about 30
million years ago (Lundberg et al. 1988). However, it is still uncertain how the river's
movements affected or coincided with the formation and eventual draining of the sea that
covered the interior lowlands at about the same time periods (Taphom 1990).
The Orinoco and Amazon rivers are connected today by the Casiquiare canal, a
natural waterway flowing southward from the upper Orinoco into the upper Rio Negro,
permitting interchange of fishes between the two basins. However, the Orinoco and
Amazon basins may have had an even closer association in the past, partly based on studies
in western Brazil. The Amazon once flowed westward to the Pacific before the major rise
of the Andes in the Miocene (Goulding 1980, Putzer 1984). After the Andes uplift blocked
its westward flow, a huge lake, or more likely, a series of large lakes and wetlands, were
formed covering much of the lowland areas in the basin (Frailey et al. 1988). Eastward
flow was prevented at the time by higher elevations joining the Brazilian and Guyana
shields. Before the Amazon had completely carved its way east between the two shields,
the proposed Pleistocene/Holocene lake or lakes had their prime outlet north into the
Orinoco. Indeed, tectonic events may have resulted in shifting the primary outlet several
times between the north and east (Frailey et al. 1988).

24
The Low Llanos
The Llanos (Fig. 2-2) are a vast plain of up to 400 km width along the north bank
of the Orinoco, stretching from near the delta mouth westward for over 1,000 km through
Venezuela, far into Colombia (Walter 1973). It occupies about 500,000 km2, is essentially
unbroken by major forests, and is the largest continuous savanna in the neotropics north of
the equator (Sarmiento 1984). A combination of factors, for instance soil type and rainfall
patterns, prevent the establishment of forest in large parts of the Llanos. Dry season fires,
of mostly human origin, are also important in limiting the growth of woody vegetation.
Several systems have been used to divide the Llanos into different categories using
combinations of physical and biological features. In most cases, a distinction is made
between the low Llanos and high or upper Llanos, based on elevation and extent of
flooding during the rainy season (Walter 1973:73, Cole 1986). The low Llanos are
characterized by open grass savannas with fairly level terrain that undergo frequent or
long term flooding during the rainy season. According to Cole (1986:92), savanna
grasslands cover some 150,000 km2 of the low Llanos in the Orinoco basin. Apure State,
in western Venezuela, encompasses a large portion of the low Llanos. Here the terrain is
relatively flat, with elevations of 100 m or less above sea level. In Apure, the landscape is
dominated by herbaceous cover, mainly bunch grasses and sedges, with occasional shrubs
and small trees (Sarmiento 1984, Cole 1986). Most trees, including palms, exist in small
isolated groups (matas) or in gallery forest situations fringing the rivers and larger streams
(Sarmiento 1984, Cole 1986). These gallery forests range from narrow bands, only a few
trees wide, to fairly extensive stands, in some places many hundreds of meters wide, as
seen existing along reaches of the lower Cinaruco and Capanaparo rivers.
The low Llanos of Apure State (Fig. 2-3) comprise a vast open floodplain
containing a diversity of aquatic habitats (Mago-Leccia 1970). All undergo pronounced
seasonal changes. Because of its low elevation and flat physical relief, most of the

Fig. 2-2. Major savanna (hatched) and forest (shaded) ecosystems in the Orinoco River basin
to
Lh

Fig. 2-3. Approximate distribution of open savanna (low Llanos) in Venezuelan state of Apure, Orinoco River basin.
to
ON

27
landscape floods during the rainy season, whereas surface water during the dry season is
usually limited to a few large permanent lagoons, large streams, and rivers. As the dry
season progresses, the savanna vegetation turns yellow and the earth becomes hard and is
fissured with cracks from the intense heat of the sun. Rivers and streams in the low Llanos
are of low gradient, with many wide meanders and anastomoses. The Apure River and
many of its tributaries are whitewater in character, with a relatively high sediment load and
high conductance (Saunders and Lewis 1988). In contrast, the Capanaparo and Cinaruco
are essentially blackwater rivers, with moderate sediment loads. In addition to stream
channels, the landscape of the low Llanos is dotted with shallow marshes (esteros) that
hold water after floods or rain. Lagoons (lagunas) form in deeper depressions, some
created from abandoned stream meanders, and are more permanent aquatic habitats.
Human population density is low and most of the low Llanos is used for cattle ranching.
Since the early 1970's extensive networks of low earthen dikes, called modules {mdulos),
have been constructed, surrounding large areas of the floodplain savanna. These modules
lessen the extreme effects of seasonal changes within their boundaries by controlling
flooding and by holding water in lower areas, available to cattle year round. The hundreds
of borrow pits {prestamos) excavated during the construction of these dikes, as well as
from building of roads, collect water and serve as permanent and semi-permanent artificial
lagoons. Typically less than 25 m wide, some prestamos stretch unbroken for several
kilometers.
During high water, adjacent rivers and streams in the Llanos are often connected by
sheet flooding of the savanna or by filling of small interconnecting channels. Thus, fish
are generally able to move across the entire floodplain. However, where dikes or
roadways are present, run-off patterns have changed and local fish movements are
somewhat restricted (Taphom and Lilyestrom 1984, Nico and Taphom 1988).
Many of the wetlands in the Llanos contain large amounts of organic material and
become highly productive during the rainy season (Mago-Leccia 1970, Saunders and

28
Lewis 1988). During high water, the flooded savanna habitats are important to fish as
breeding and feeding areas. Aquatic vegetation flourishes and emergent and floating plants
may cover large portions of the surface of both permanent and temporary water bodies.
Large mats of water hyacinth [Eichhornia species) are especially abundant in many of the
lagoons, prestamos, and some of the streams. Partially inundated grasses and sedges
commonly grow in the shallows of streams, prestamos, and other standing waters. Other
common aquatic and semi-aquatic plants of the low Llanos include Ludwigia, Benjamania,
and Pontederia. Some common aquatic plants with floating leaves are Salvinia, Lemna,
and Pistia.
The Upper Orinoco
The upper Orinoco drainage is situated in the Federal Territory of Amazonas
(Fig. 2-4) in southern Venezuela, a vast area covering 178,095 km2 (CODESUR 1979).
Main features of the heavily forested landscape are flat alluvial plains, large mountain
valleys, and massive granitic hills [lajas) (CODESUR 1979, Huber and Wurdack 1984).
About 70 percent of the territory is drained by the Orinoco, with the remainder flowing into
the Rio Negro of the Amazon basin (CODESUR 1979). Together with the adjacent state of
Bolivar, this southern section of the country is often referred to collectively as Venezuelan
Guyana because the Precambrian Shield dominates the topography. Little developed and
with few inhabitants, the great majority of intact forests in Venezuela occur in this southern
region. Steyermark (1982) estimated that forests covered 82 percent of the region, or about
146,000 km2. Due to forest clearing, the total coverage is probably slightly less today.
Because forests of the upper Orinoco are continuous with those of the northern Amazon
Basin, the region is part of the largest area of humid forests within the neotropics
(Whitmore and Prance 1987).

29
Fig. 2-4. Approximate distribution of lowland forests (shaded area) in Federal Amazon
Territory of Venezuela.

30
The flat lowlands or peneplains of southern Venezuela are dominated by wet
tropical forests (Figs. 2-2 and 2-4). The altitude of these lowland regions in the upper
Orinoco range from 100 to 500 m, with most less than 200 m (Huber and Wurdack 1984).
Similar to the situation described for Amazonian lowlands (Prance 1979, Kubitski 1989),
many lowland forests in the upper Orinoco are inundated by the annual high water, with
some sites being permanently waterlogged. Aerial photos of the lowlands reveal a history
of streams meandering across their adjacent floodplains. Large and small streams, cutoffs,
and oxbows abound in many of the drainages (e.g., Mavaca River) and, similar to the low
Llanos, interconnections with adjacent drainages within the upper Orinoco are common
during high water. However, aquatic vegetation in the region is much more sparse and
localized in comparison to the low Llanos. Although a few backwaters are choked with
submergent and emergent vegetation, most floodplain lakes in the upper Orinoco have few
or no aquatic plants. The reasons for such scarcity are likely related to high shade,
unconsolidated bottoms, and few available nutrients in the water or substrate. In flowing
waters there are often small bands of flooded grasses along bank edges of inner bends.
The fish fauna of the upper Orinoco is the least known in all of Venezuela, largely because
of the inaccessibility of the region. With very few roads, modes of transportation within
the area are limited almost exclusively to small and medium-sized boats and small planes.
Savannas and Forests during the Quaternary
Both tropical forest and tropical non-forest vegetation originated in the Cretaceous
and Tertiary, about 100 million years ago, periods when world climates were apparently
rather stable and tropical conditions much more widespread (Whitmore and Prance 1987).
However, during the last two million years there have been periodic and dramatic
fluctuations in the distribution of savannas versus forest environments in northern South

31
America that are associated with climatic oscillations (Prance 1982, Whitmore and Prance
1987). Although lowland regions remained essentially tropical, during major glaciations
the equatorial lowland regions experienced dryer and hotter climates (but see Colinvaux
1976). As a result, savanna and open-land environments expanded, whereas humid forests
contracted. During these dry periods, forests were often reduced to combinations of
variably-sized isolated refuges and fingers of gallery forests along major rivers. Indeed,
new data on Pleistocene mammals indicate that savanna habitat may have expanded to such
an extent as to form a continuous band connecting the Orinoco Llanos with the pampas of
Argentina by way of the western Amazon basin (Raney 1991). The last major glacial event
causing a cold, dry Pleistocene climatic phase occurred 13,000-18,000 years ago.
Much controversy exists about the extent and precise location of forests during the
Pleistocene dry periods. Haffer (1987:12) presented a map outlining possible distribution
of both relatively humid areas and tropical forests, forest "refugia, surviving in northern
South America during that period of savanna expansion. His map delineates three major
regions of humid forests in the Orinoco basin: several sections in the Andes; a block near
the southern tip of Venezuela; and a long broad belt (100-200 km wide) south of the main
stem Orinoco, extending from near the mouth of the Meta River eastward through the
Guianas.
In contrast to glacial periods, interglacial or pluvial periods were wetter and
relatively cooler, contributing to the expansion of humid forests and contraction of
savannas. Isolated savannas currently found in the upper Orinoco are thought to be
savanna refugia that survived the cooler and wetter phases. The present climatic condition
is wet and warm (i.e., as opposed to dry and hot), and humid forests are at or near their
maximum extent, whereas the extent of natural savannas and dry forests is restricted
(Whitmore and Prance 1987:63).

32
Present Climate and Seasonality
Regional topography and the fact that the entire Orinoco Basin lies immediately
north of the equator are important factors controlling climate and the timing of precipitation
(Walter et al. 1975). There is a trend toward increased rainfall from north to south.
Nevertheless, rainfall patterns can be quite variable from year to year in a single locality, as
well as among different localities within any particular region.
The Llanos have consistently high temperatures and fairly distinct wet and dry
periods. The rainy season is associated with the inner-tropical convergence zone (Walter et
al. 1975), and lasts from seven to nine months, usually from late April to October or
November (Fig. 2-5). Little or no rain falls during the two or three driest months, when
the inner-tropical convergence zone is in the southern hemisphere. Total rainfall in the
Llanos ranges from 1200 to 1800 mm per year (Taphom 1990), with savanna grasslands
common to the low Llanos typically receiving 1300-1400 mm (Cole 1986:97). The
recording station at San Fernando de Apure, located in the center of the low Llanos,
reported a mean annual precipitation of 1416 mm, based on 26 years of records (Walter et
al. 1975); mean monthly temperatures for the locality varied between 26.6 and 29.2 C
(Cole 1986:97). However, daily temperatures can fluctuate widely.
Although the two regions have a fairly similar range of air temperatures, the upper
Orinoco is much more humid than the Llanos. Average annual rainfall is 3,250 mm/yr,
with very humid areas receiving well over 4,000 mm (CODESUR 1979). Although the
amount of rainfall varies seasonally, the dry season in the upper Orinoco is not as
pronounced as in the Llanos (Fig. 2-5). Few areas of record receive less than 75 mm in
any given month during the dry season (CODESUR 1979). Nevertheless, the alternation
of low and high water seasons is distinct Elighest precipitation occurs between May and
September and the lowest between December and March (CODESUR 1979). Monthly
mean temperatures range from 26 to 28.5 C (CODESUR 1979). Both the low Llanos of

Apure State and the lowland forests of the upper Orinoco undergo extensive flooding
during the wetter part of the year by a combination of rising river water and local rains.

34
Month
Fig. 2-5. Monthly rainfall recorded at representative sites in Orinoco River basin,
Venezuela. (1) Upper Orinoco: monthly average 1971-1977 from Santa Maria
de Los Guaicas, mouth of Ocamo River, Federal Territory of Amazonas, and (2)
Low Llanos: for year 1972 from Cao Caicara area, Apure River drainage,
Apure State. Sources: CODESUR (1979) and Taphom and Lilyestrom (1984),
respectively.

CHAPTER 3
METHODS
Field Sampling
In the field I tried to collect as many individuals, sizes, and species of serrasalmine
fishes as possible from each region and drainage, but I did not attempt to measure fish
biomass. Sampling of fishes was done in all major habitats using appropriate combinations
of collecting gear and fishing tactics so as to obtain the most information in a short period
of time. Although piranhas were taken in greatest numbers during the day, especially near
twilight, night collections were also made in the two major regions studied. For sampling
piranhas, I depended mainly on various combinations of seines, gill nets, cast nets, and
hook and line. Harpoons, spear gun, minnow traps, trotlines, and commercial
(5% rotenone) and natural (barbasco) fish toxicants were used only rarely; these capture
methods contributed little to the total sample of serrasalmine fishes taken. In the field, most
fishes collected were preserved immediately in 10-20% formalin; in the laboratory,
preserved specimens (those less than about 200 mm SL) were transfered to 70% ethanol or
35% isopropanol. A few young piranhas were kept alive and maintained in aquaria.
Each type of sampling gear targeted a certain size range of fishes. For collecting
young piranhas and other small fishes, I used small nylon seines (6x2 and 5x2 m, 6.4 mm
mesh), nylon and monofilament cast nets ranging from 1.8 to 3 m diameter (2 to 2.5 cm
mesh), and hand nets (3 mm mesh); these were normally limited to use in shallow areas
(<1.5 m deep). Small seines and hand nets were the most effective equipment for sampling
in areas with dense aquatic vegetation. In instances where vegetation made it difficult to
35

36
effectively pull the seine forward, a seine was set stationary, and one or more "kickers"
drove fishes from the vegetation into the net.
Nylon bag seines (6x2 m with 2x2 m bag, 6.4 mm mesh) or large beach seines
(10x2 m, 6.4 mm mesh) were used in more open shallow water habitats. These nets
sampled for a broad range of fish sizes, but because few areas had clean substrates, large
seines were usually limited to open beaches along rivers or streams, and lagoons, where
there was little submerged debris.
Nylon and monofilament gill nets with float lines were used to sample selectively
for medium and large-sized fishes, including adult and subadult piranhas. Gill net sizes
were 20x2 m (20 cm stretch mesh), 10x5 m (5 cm mesh), 50x2 m (with two 25-m long
panels of 5 and 7 cm mesh, respectively), and 100x2 m (6 cm mesh). For taking piranhas,
gill nets were set in areas with little or no current, used in conjunction with seines, and in
deeper water (>1.5 m) where use of seines was impractical. Set gill nets were monitored
and all fish removed every 0.5 to 6 hours, depending on time of day and local fish
abundance. Because piranhas can damage gill nets, nets set in areas with high piranha
densities were checked more frequently.
All piranha species occurring in the Orinoco River basin take baited hooks (personal
observation). Hook-and-line fishing was done mostly with natural bait, using hand lines
and occasionally rod and reel. Different sizes and types of commercial hooks were used to
sample for fishes of different sizes. Type of bait employed was noted so as to not be
mistakenly recorded later as part of their natural diet. In general, sampling by hook and
line yielded the same piranha species, and proportions of individuals, as those caught by
gill net.
Overall, piranha species that were common in any one area were taken by two or
more types of sampling gear. No one capture technique seemed to be selective for a
particular piranha species, or group of species. Seines, gill nets, cast nets, and hook and

37
line were ail occasionally effective in capturing species considered uncommon in a
particular drainage or region.
To reduce the risk of missing uncommon or rare species in upper Orinoco
drainages, where most sampling was limited to relatively short periods, I supplemented my
own samples with collections of others. In the field, I recorded the catch of hired
fishermen and Indians, including the daily hook-and-line collections of camp workers.
Field Site Locations and Sampling Periods
Nine drainages of the Orinoco River basin in Venezuela were sampled during the
present study, three in the low Llanos and six in the upper Orinoco (Fig. 3-1).
Low Llanos or Savanna Sites
Three major drainages were studied in the low Llanos of Apure State: the Apure,
Cinaruco, and Capanaparo rivers (Fig. 3-2). Principal habitats sampled were rivers,
streams, natural and artificial lagoons and pools, and flooded savanna. The Apure drainage
was the only site where long-term research on piranhas was carried out.
Apure Drainage. Almost all fieldwork was done in the Cao Caicara watershed of
the Apure drainage in and around the Femando Corrales research station and ranch of the
Universidad de Los Llanos (UNELLEZ) (0725'50"N, 693530"W). This area is
bordered by Cao Caicara, its tributary Cao Maporal, and a smaller stream, Cao
Guaritico. I made periodic samples in the Cao Caicara study area during December 1983;
January, March, May, July, September, and November 1984; and March, April, and May
1985; these were followed by samples taken during August 1988, March, April, and
December 1989, and January, March, and May 1990. I also examined material taken

72 70 68 66 64 62 60
Fig. 3-1. Map of Venezuela showing nine selected drainages in Orinoco River basin sampled during present
study. Low Llanos rivers: (1) Apure, (2) Capanaparo, and (3) Cinaruco; Upper Orinoco rivers:
(4) Sipapo, (5) Atabapo, (6) lower Ventuari, (7) Matacuni, (8) Ocamo, and (9) Mavaca.

Fig. 3-2. Map of Apure State, Venezuela, showing principal low Llanos sampling sites. Solid circles represent localities
sampled by the author; solid squares represent areas collected by others (specimens from all sites deposited at
MCNG and examined by the author). Each symbol may represent more than one sampling site.

40
between 1979 and 1984, which included monthly samples of a one-year biomass study of
the area in 1982-1983 (see Taphom and Lilyestrom 1984). A total of about two hundred
fish collections were made in the Apure River drainage in caos Caicara and Maporal and
their adjacent floodplains from 1979 to 1990.
Cinaruco and Capanaparo drainages. I examined collections made by others from
the lower Cinaruco and Capanaparo rivers and their floodplains. Most sites sampled were
within 50 km of the north-to-south road joining San Femando de Apure with Puerto Paez,
a route roughly following 6730' W longitude. Samples were taken in January 1982,
December 1986, January 1987, and March and April 1989. The 1989 collections were the
result of a fish inventory of the two drainages made by D. C. Taphom and A. Barbarino
using seines, cast nets, and hook and line. Overall, sites collected were the main channels
and near-shore areas of the two rivers, as well as Laguna Larga of the Cinaruco River, and
Cao La Pica and Laguna Brava of the Capanaparo drainage.
Upper Orinoco or Forest Sites
Six major drainages in the upper Orinoco, Amazon Territory of Venezuela, were
sampled for analysis of piranha populations from forested regions (Fig. 3-3). These
included the Sipapo, Atabapo, Ventuari, Matacuni, Ocamo, and Mavaca drainages, as well
as the main channel of the Orinoco River. I collected fishes and evaluated habitats during
five expeditions, between early 1989 and 1991, as part of a resource inventory of southern
Venezuela in association with the mineral consortium CVG-TECMIN (Corporacin
Venezolana Guyana Tcnica Minera). Data on serrasalmine fishes from the region are
based on intensive sampling of many sites over relatively short periods of time. Each
expedition lasted between 25 and 40 field days and covered a different drainage or set of

41
Fig. 3-3. Map of 1988-1991 sampling sites in upper Orinoco, Federal Territory of
Amazonas, Venezuela Solid circles represent localities sampled by the
author; solid squares represent areas collected by others (specimens from all
sites deposited at MCNG and examined by the author). Circles and squares
may represent more than one sampling site.

42
drainages. Work in any one drainage was usually limited to one part of the year, either
during the high or low water period.
Lowland habitats sampled in the upper Orinoco were channel borders and beaches
of rivers, streams, side channels, old meanders and other back waters, including isolated
floodplain lakes, as well as inundated forest. Elevations ranged from 90 to about 240 m
above sea level. Collection sites and sampling dates were as follows: (1) Guayapo and
Sipapo rivers, from 12 May to 7 June, 1989; (2) lower Ventuari River, including its
tributaries the Yureba, Parti, Asisa, Guapuch ( = Picure), Marueta rivers and the caos
Cucuritl, Moriche and Tabi-Tabi, from 17 September to 16 October, 1989; (3) Atabapo
River, including its tributaries the Atacavi and Temi rivers and the caos Patacame,
Cuchakn, Bocachico, and Chimita, from 23 October to 17 November, 1989; (4) Ocamo,
Putaco, Padamo, and Matacuni rivers, and the caos Jayuwapuei, Jenita, Maveti, and
Yaraca-bawei, including the upper Orinoco River main channel above its confluence with
the Ventuari, from 16 January to 16 February, 1990; and (5) Mavaca River, its tributary
Cao Mavaquita ( = Cao Hauyapiwei), and the upper Orinoco main channel, from 18
January to 20 February, 1991. A total of 200 fish collections representing 180 individual
sites was made in this region, resulting in over 18,000 specimens, of which 500 were
serrasalmine fishes.
Evaluation of Habitats
A variety of habitat parameters was recorded whenever possible for most collection
sites. Qualitative and quantitative estimates were as follows: (1) season (wet, dry, or
transitional); (2) water type (clear, black, white, or combination); (3) water level (isolated
pools, continuous in bank, bank full, or flood condition); (4) watershed topography (level,
moderately rolling, rolling, mountains); (5) stream gradient (flat, slight, moderate, or >30
degrees); (6) land use (natural, cattle, agricultural, or developed); (7) major terrestrial

43
habitat (grassland, savanna, gallery forest, or forest); (8) dominant riparian vegetation
(none, grasses/forbes, shrubs/trees, narrow forest border, or forest); (9) water depths at
site and capture depths (very shallow [0-5 cm], shallow [5-20 cm], moderate [20-50 cm],
deep [50-100 cm], very deep [100-150 cm], extremely deep [>150 cm]); (10) water
velocities, as measured with a mechanical flowmeter (General Oceanics) or using a floating
stick or cork, were classified into six categories (zero [<0.02 m/sec], very slow [0.02-0.10
m/sec], slow [0.10-0.25 m/sec], moderate [0.25-0.75 m/sec], fast [0.75-1.25 m/sec], and
torrential [>1.25 m/sec]); (11) water temperature; (12) water pH measured with a Hach pH
Pocket Pal meter or a Hach colorimetric (color disc) wide range pH test kit (Model 17-N);
(13) water color and turbidity (very-clear, clear-tannin, clear-green, slightly-turbid,
moderately turbid, or very turbid); (14) water clarity as measured with a 20-cm diameter
Secchi disk; (15) estimated maximum and average water width; (16) degree of shading (full
sun, partial shade, temporary full shade, permanent full shade).
Substrate types and types of aquatic or instream cover for each collecting site were
recorded by estimating their proportion of the total surface area: (0)=none/few; (1)<10%;
(2)10-50%; and (3)>50%. Substrate types recognized were: silt/mud; sand; gravel;
rubble; boulder; bedrock/claypan; vegetation; litter; and detritus/decomposed organics.
Fish cover categories recognized were: floating aquatic vegetation: emergent vegetation;
submergent vegetation; litter on bottom; overhanging vegetation; undercuts; bank cover;
brush/roots; rocks; logs; and artificial structures (e.g., culverts, bridge piers).
Identification and Nomenclature of Piranhas
At least 12 species of piranha occur in the Orinoco River basin (personal
observation). As with most groups of South American freshwater fishes, there has been a
great deal of confusion surrounding the classification and nomenclature of the subfamily
Serrasalminae, due to a combination of factors. Some species exhibit marked changes in

44
body shape with growth. Individuals are also fairly variable in terms of body pigmentation
and color patterns; such differences can be associated with age, size, or sexual condition,
and may also be environmentally induced. To further complicate piranha taxonomy, the
complete geographic distribution of most species is unknown. Moreover, because little if
any comparative material was available to previous taxonomists, most earlier descriptions
were incomplete, and thus inadequate for making accurate identifications. Fink (1988)
reported that fewer than half of the about 60 nominal species of piranhas were valid.
Nevertheless, sampling in previously uncollected regions has resulted in the discovery of a
few new species (personal observation). Except for difficulties in identifying some of the
smallest specimens (less than 25 mm SL), I believe I have successfully sorted out the
different species encountered in this study. Preserved specimens examined are deposited in
the Museo de Ciencias Naturales (MCNG), UNELLEZ, Guanare, Venezuela. Voucher
material has also been donated by MCNG under an official cooperative agreement to the
Florida Museum of Natural History (UF), Gainesville, Florida. Institutional acronyms are
from Levitn et al. (1985).
Because of the taxonomic confusion, piranhas have often been misidentified in the
literature. Drs. William Fink (UMMZ) and Antonio Machado-Allison (MBUCV) are
currently revising the piranhas of Venezuela; I have relied on both for identifications of
certain voucher specimens. They have also made available their unpublished key to
Venezuelan piranhas. Taphom (1990) prepared keys to the characiform fishes of the Apure
drainage, and also listed probable generic and specific synonyms of serrasalmine fishes.
His nomenclature for piranhas follows that of Fink and Machado-Allison. Abbreviations
used for piranhas and other serrasalmine fishes in illustrations and tables are given in Table
3-1. In the following section species names used in the present report are listed together
with names used by me and colleagues for the same species in recent publications:

45
(1) Serrasalmus altuvei Ramrez 1965: Serrasalmus altuvei in Nico and Taphom
(1988); color illustrations in Nico and Taphom (1986:33), photos reproduced in Schulte
(1988:119).
(2) Serrasalmus cf. eigenmanni Norman 1928: Serrasalmus cf eigenmanni may
involve a species complex (W. Fink, personal communication): however, I distinguished
only one species in my samples. This species, to my knowledge, has not been previously
referenced in publications on Venezuelan piranhas. The piranha Serrasalmus nalseni
described and figured by Fernndez-Ypez (1969) is a possible synonym, but I have not
seen the type series. All previous references to Serrasalmus eigenmanni from the Orinoco
probably refer to other species (see Serrasalmus irritans below).
(3) Serrasalmus elongatus Kner 1860: Serrasalmus cf. elongalus in Taphom and
Lilyestrom (1984), Nico and Taphom (1988); color illustrations in Nico and Taphom
(1986), photos reproduced in Schulte (1988:1, 119); photos as S. pingke in Romn
(1983:56).
(4) Serrasalmus irritans Peters 1877: 5. eigenmanni in Taphom and Lilyestrom
(1983); S. irritans in Nico and Taphom (1988) and Winemiller (1989a, 1989b); color
illustrations as Serrasalmus eigenmanni in Nico and Taphorn (1986:31, 33), same photos
reproduced in Schulte (1988:120), photos as S. eigenmanni in Romn (1983:57).
(5) Serrasalmus manueli Fernndez-Ypez and Ramrez 1967: This species has
rarely been referenced in the literature since its original description. I am unaware of
misidentifications. There is no published information on its biology or natural history.
(6) Serrasalmus medinai Ramirez 1965: Serrasalmus caribe in Nico and Taphom
(1988); incorrectly spelled as S. medini in Winemiiler (1989a, 1989b); color illustrations as
Pristobrycon sp. in Nico and Taphom (1986:31, 33, 41), photos reproduced as
Serrasalmus (.Pristobrycon) sp. in Schulte (1988:119), and as Serrasalmus (Pristobrycon)
"iridescent (incorrect locality given) in Schulte (1988:128); photos as S. rhombeus in
Romn (1983:31,60).

46
Table 3-1. List of abbreviations used in figures and tables for piranhas and other
serrasalmine fishes.
Piranhas:
Other Serrasalmine Fishes:
Pc
Pygocentrus caribe
Cm
Catoprion ment
Psp
Pristobrycon sp.
Mag
Metynnis argenteus
Pst
Pristobrycon striolatus
Mya
Myleus asterias
Pyp
Pygopristis denticulatus
Mys
Myleus schomburgkii
Sa
Serrasalmus altuvei
Myt
Myleus torquatus
Seg
Serrasalmus cf. eigenmanni
Md
Mylossoma duriventris
Sel
Serrasalmus elongatus
Sir
Serrasalmus irritans
Sm
Serrasalmus manueli
Smd
Serrasalmus medinai
Sr
Serrasalmus rhombeus

47
(7) Serrasaimus rhombeus (Linnaeus) 1766: Serrasalmus rhombeus in Nico and
Taphom (1988) and Winemiller (1989a, 1989b); and color illustration in Nico and Taphom
(1986:40-41).
(8) Pygocentrus caribe Valenciennes 1849: Pygocentrus notatus in Taphom and
Lilyestrom (1984), Nico and Taphom (1988), Winemiller (1989a, 1989b), Nico (1990);
color illustrations are given as P. notatus in Nico and Taphom (1986:31, 40, 41), photos
reproduced as Serrasalmus (Pygocentrus) notatus in Schulte (1988:109, 110), as
Serrasalmus niger in Schulte (1988: 111), and as Serrasalmus natter eri (incorrect locality
given) in Schulte (1988:12-13).
(9) Pristobrycon striolatus (Steindachner) 1908: Pristobrycon striolatus in Nico
and Taphom (1988); color illustrations as Pristobrycon striatus in Nico and Taphom
(1986:31,41), and as Pygocentrus striolatus in Nico and Taphorn (1986:33), photo
reproduced in Schulte (1988:120). Machado-Allison et al. (1989) concluded that
Pygopristis antoni Fernndez-Ypez, 1965 is a junior synonym of P. striolatus.
(10) Pristobrycon sp.: This species is in the process of being described as new by
W. Fink and A. Machado-Allison.
(11) Pygopristis denticulatus Muller and Troschel 1844: photograph as
Serrasalmus (Pygopristis) antoni in Romn (1983:51).
Faunal Comparisons
The Coefficient of Biogeographic Resemblance (CBR) proposed by Duellman
(1990) was used to compare the composition of piranha assemblages between the two
regions studied and among the different drainages. This qualitative index of similarity has
been reinvented a number of times, consequently it is known by several names including
the Faunal Resemblance Factor, the Sorenson Index, and the Dice Coefficient (Boesch
1977, Romesburg 1984, Magurran 1988, Duellman 1990). This index is one of the more

48
commonly used measures for comparing species presence-absence data (Krebs 1989), and
is calculated as:
CBR = 2C/ (Ni + N2),
where C is the number of species common to two areas, N i is the number of species in the
first area, and N2 is the number of species in the second area. The resulting values range
from 0, if there are no species in common, to 1, if both areas share the same number and
kinds of species. This measure is simple, is not affected by relative numbers of
individuals, and thus is best used when there are no reliable quantitative data on abundance
of species (Magurran 1988, Krebs 1989). Binary similarity measures are not totally
independent of sample size (Wolda 1981, Krebs 1989). However, comparisons when
maximum number of possible species is low give results less affected by sample size
differences than those dealing with many species (see Krebs 1989). CBR is very similar to
the Jaccard Coefficient (Boesch 1977, Romesburg 1984, Duellman 1990); it doubly
weights shared positive attributes (i.e., joint presences), and is preferred over the Jaccard
Coefficient if the entities vary widely in their number of positive attributes (Boesch
1977:22).
To make presence-absence data more reliable, I supplemented my data with
information from collections deposited at MCNG and UF. I also reviewed the literature for
records of species occurrence. A Spearman rank correlation test was used to test for an
association between species composition and drainage area size, and between faunal
similarities and distances among drainages. The similarity or resemblance matrix generated
from the CBR equation was used as a basis for clustering drainages, employing the
unweighted pair-group method using mathematical averages, or UPGMA.

49
Analysis of Diets
In order to analyze diets and document ontogenetic shifts in feeding, sampled fishes
were divided into five size classes: Group I) 10-19 mm SL small juveniles; Group II) 20-'
39 mm SL; Group IQ) 40-79 mm SL; Group IV) 80-159 mm SL; and Group V) >160 mm
SL. Several species were not represented by all size classes.
During the study, more than 2,000 serrasalmine fishes were captured; total number
of specimens examined for stomach contents was 1,538 from the low Llanos and 393 from
the upper Orinoco. Standard length (SL) of each specimen was measured to the nearest
mm. Although a few of the largest fish were dissected and examined in the field, most
specimens were preserved after capture and dissected later in the laboratory to determine
stomach contents. I examined stomach contents and recorded frequency of occurrence
(O), number (N), and dominance by bulk (D) for each food item. I also recorded volume
(V) of food items found in stomachs of fishes taken in the field after 1986. Small food
organisms were counted using a Ward counting wheel under 25X magnification. Volume
was determined by water displacement using appropriately-sized graduated cylinders.
Volumes of smaller items were calculated by measuring dimensions with Vernier calipers
or by examination under a dissecting microscope and comparison with known volumes.
An estimate of relative stomach fullness was made using scores ranging from 0 (empty) to
3 (if full, or almost full) (Thomerson and Wooldridge 1970, Nico and Taphom 1988).
For specimens collected in the Apure River drainage before 1986,1 estimated
volume using a point system, referred to as adjusted volume (Va), and derived from D and
stomach fullness (Nico and Taphom 1988). That is, only the dominant food categories of
a given stomach were included and each was assigned the fullness points (1-3) for that
stomach. If two food items in a single stomach were of about equal volume, each received
half the fullness value. Thus, %Va = total fullness points for each food category as a
percentage of all fullness points, and can be shown as:

50
(=1 ;= 1
%Va =( jFil Yji ) x 100,
/I /I
where F/ is the fullness points for stomachs whose dominant food item is F\ Ti is total
fullness points for all stomachs; and n is the number of stomachs examined of a species or
size class.
I attempted to identify food items to the lowest taxonomic level, whenever possible.
For comparing piranha diets, I recognized eleven general food categories: (1) masticated
seeds crushed or fragmented seeds together with the hard parts (mainly endocarp)that
surround the seed; (2) other plant material mostly leaves, root fragments, fleshy fruits,
and flowers; (3) decapods crabs and shrimp; (4) microcrustaceans copepods,
cladocerans, ostracods and conchostracans; (5) aquatic insects various families, including
larvae and adults; (6) other invertebrates mostly arthropods, including terrestrial forms,
but also aquatic nematodes and snails; (7) small whole fish at least two-thirds of total
body; (8) fish flesh pieces of flesh bitten from fish; (9) fish fins fins not taken with or
attached to pieces of flesh; (10) fish scales scales not taken with or attached to flesh; and
(11) other detritus, sand, nonfish vertebrates, and unidentifiable items.
I compared and contrasted diets within and among the different species and size
groups by calculating estimates of diet breadth and overlap based on percent food volume
or adjusted volume. Because I did not quantitatively measure the relative availability of
food resources in the field, I chose two widely used indices of breadth and overlap that do
not take into account the relative abundance of the various food items in the natural
environment.
Diet breadth, or width, measures the diversity and evenness of resource use. Diet
breadth was computed for each species' size class using Levins' index of niche width
(Levins 1968, Krebs 1989):

51
/=1
Diet breadth (B) = 1/
n
where P is the proportion of food category i in the diet. B ranges from 1, when one
resource state is used exclusively, to n (the total number of food categories recognized),
when all resource states are used in equal proportion. This measure is the reciprocal of
Simpson's index of diversity (Krebs 1989).
I used the Schoener Overlap Index (Schoener 1970) to estimate the similarity in
diets between and within species. This particular index is also known as the Renkonen
Index, the Percent or Proportional Similarity Index, Percentage Overlap, and
Czekanowski's Index (Krebs 1989); the Bray-Curtis Coefficient gives the same results as
the above index if its scores are standardized (Boesch 1977:26, Bloom. 1981). The
Schoener Overlap Index is calculated as:
= 1
Overlap = 1 0.5 ( 2, \ pxi py¡ | = Y, (minimum p*/, Pyi),
n n
where pxi is the proportion of food category i in the diet of species x, pyi is the proportion
of food category i in the diet of species y, and n is the number of food categories. The
Schoener Index gives values from 0 to 1 (or 0 to 100%) indicating no overlap to complete
similarity in the proportion of food categories used by the two groups compared.
There are many indices available for estimating niche or diet width and overlap, but
as yet there is no general consensus as to which of the many indices is best (Hurlbert 1978,
Abrams 1980, Wallace 1981). Recent reviews of frequently used indices include Ludwig
and Reynolds (1988) and Krebs (1989). All measures of breadth and overlap are biased in
some way, the bias usually being reduced with increasing sample size (Schluter 1988,
Krebs 1989). It has also been shown that measures of breadth and overlap are sensitive to
the number of resource categories used. Although lumping resource states can inflate niche

52
overlap values (Greene and Jaksic 1983), bias increases as the number of resource
categories used increases or is large (Ricklefs and Lau 1980, Smith and Zaret 1982, Krebs
1989). Overlap and breadth indices also give somewhat different results depending on the
methods used to tabulate dietary components, for example, percentages based on total food
volume, weight, frequency of occurrence, or food item number (Wallace 1981). An
additional problem implicit in all overlap and breadth measurements is that the investigator
may recognize resource categories that animals do not For instance, Goulding et al.
(1988:52) suggested that .Amazonian frugivorous fishes "select their preferred fruits and
seeds at what taxonomically are referred to as genera" rather than at the species level.
Conversely, organisms may distinguish resources lumped together by human observers
(Ludwig and Reynolds 1988, Krebs 1989). Finally, most overlap and width indices are
based on the relative use of different resources, without accounting for their relative
availabilities. However, resource availability is difficult to assess and therefore rarely
measured. Those indices that do incorporate some estimate of food availability into their
equations are generally less simple to interpret and more variable between sites (Schluter
1988). Abrams (1980) and Wallace (1981) recommended the Schoener Index as the best
of the measures of niche overlap when available resources to the organism have not been
quantified. Krebs (1989:304-306), referencing Wolda (1981), regarded this measure as
one of the better quantitative similarity coefficients available, showing that it is relatively
little affected by sample size and number of species (i.e., resources states).
Because percentage of occurrence and percentage of total number of food items tend
to over-emphasize the importance of small food items, I used proportions based on total
food volume for calculating diet widths and overlaps. Using food volume introduces the
possible bias that a large prey item in a single large piranha might overshadow all other
items when pooling stomach contents data. However, this problem is overcome to a large
extent by dividing fish into different size classes and treating each size class as a separate
"trophic unit" (sensu Stoner and Livingston 1984).

53
In my analysis of diets, the similarity or resemblance matrix generated from the
Schoener Index was used as a basis to cluster species using the unweighted pair-group
method using mathematical averages, or UPGMA. I used 2x2 contingency table X2 tests
(one-tailed) and Mann-Whitney U-tests to test the prediction that forest populations fed
more on plant material than their savanna counterparts.
Nutrient Content Analysis of Food Items
In order to compare nutrient values, analyses were carried out to determine ash,
crude protein, total fat, carbohydrate, and energy contents of different food items. Three
types of food items were examined: small whole fish, fish fins, and fish scales. I also
searched the literature for information on the nutrient value of other types of general food
items, for example insects and various types of plant material. Prey fishes used for
analysis were taken from the Apure River drainage, Venezuela, using cast nets and seines
during the dry season in December 1989 and March 1990. Tissues from members of two
unrelated families of fishes were tested: (1) Curimatidae, represented by Curimatella
immaculata, Cyphocharax spilurus, and Steindachnerina argntea; and (2) Cichlidae,
Aequidens pulcher and Cichlasoma orinocense. These species are common in the Orinoco
River basin and are frequently preyed upon by juvenile and adult piranhas.
In total, 135 small cichlids (SL range 39-77 mm) and 96 curimatids (SL range 45-
78 mm) were used for nutrient content determinations. Fish were placed on ice
immediately after capture, transponed to the laboratory at the Universidad de Los Llanos
Occidentales (UNELLEZ) in Guanare, Venezuela, and refrigerated until analysis was
conducted. Body scales were removed from partially frozen specimens with a small fish
scaler, and no attempt was made to clean off the bodys outer mucous layer. Only caudal
and dorsal fins were used for fin samples; these were removed by clipping with scissors
above the fin base to avoid scales. Two or three entire cichlid and curimatid specimens

54
were used for tests as small whole fish. All subsequent nutrient analyses were carried out
at UNELLEZ under the direction of the biochemist Dr. Margioly de Morales. Samples
were oven-dried to constant weight at 60 C to prevent lipids in the body tissues from
volatilizing. After drying, samples were ground in a Willey mill and stored in desiccators.
Unless otherwise stated, methods of analysis used follow AOAC (1980) guidelines.
Results are expressed as percentages of dry weight, rather than as percentages of ash-free
dry weight (i.e., on organic matter basis), for ease of comparison to previously published
data. All measurements were duplicated; the differences between replicate subsamples of a
particular food item were generally less than 1%. Ash contents were determined by
combustion of samples of dried body tissue at 550 C for 3 hours (Pierce et al. 1980).
Total fat content was determined by extracting lipids for four hours with diethyl ether.
Crude protein was determined by the Kjeldahl method for nitrogen, where crude protein is
total nitrogen concentration multiplied by 6.25. Carbohydrates were determined as the sum
of crude fiber and nitrogen-free extract; total carbohydrates are the sum of both values.
Energy content was measured using a Parr bomb calorimeter and expressed as kJ per g;
this can be converted to kilocalories per g by dividing by 4.184.
Intestine Length
Length of the intestinal tract (IL) was determined by removing the entire
gastrointestinal tract, placing the extended intestine (without stretching) on a flat surface,
and measuring the distance from the pylorus to the anus (Ribble and Smith 1983). Fecal
material was left in the intestine during measurement Relative intestine length for each fish
was calculated by dividing IL by standard length (SL). An analysis of covariance
(ANCOVA) was carried out in order to compare the regression lines of IL versus SL
among species. A Spearman rank correlation test was used to test for an association
between relative intestine length and the percent volume of plant material among the

different species. My data indicated allometric changes in intestine length. In order to
reduce variation and make comparisons more valid, only specimens > 80 mm SL were
used in correlation analysis.
55
Field and Aquarium Observations
I made qualitative and quantitative observations on the feeding behaviors of wild-
caught juvenile and subadult piranhas maintained live in aquaria or large outdoor concrete
tanks (L. Nico, unpublished data). Species represented from low Llanos populations were
Pygocentrus caribe, Serrasalmus elongatus, S. irritans, S. medinai, S. rhombeus, and
Pristobrycon striolatus; those from upper Orinoco sites were Pygopristis denticulatus and
Serrasalmus manueli. In the field, most observations of piranha feeding behavior were
done from shore or from boats while fishing, these qualitative observations totaled over
one hundred hours. I also made brief underwater observations on the feeding behavior of
several species totaling about five hours. Underwater observations were made using mask
and snorkel in Clearwater and blackwater streams in the states of Bolivar, Guarico, and
Monagas. Species observed were juveniles or subadults of Serrasalmus irritans, S.
medinai, S. rhombeus, and Pygocentrus caribe.
Statistical Analyses
All nonparametric tests were run using the computer software program Basic
Statistical Subroutines by DYNACOMP (1983) following Siegel (1956) and Siegel and
Castellan (1988). Statistical tests of ANCOVA were done using the SuperANOVA
program on a Macintosh SE/30 computer. For cluster analysis, I used the computer
program NTSYS-pc (Numerical Taxonomy and Multivariate Analysis System) version 1.5
by Rohlf (1988). Cluster analysis has been shown to be a useful and reliable multivariate

56
procedure for identifying feeding patterns in assemblages of fishes (Stoner and
Livingston 1984, Henderson and Walker 1986) and other vertebrates (Jaksic and Medel
1990). The method has also been used extensively to describe fish distribution patterns
(Hocutt and Wiley 1986). Basically, the UPGMA clustering technique generates a
hierarchical tree, or dendrogram, grouping together those samples or objects that are most
similar. UPGMA is widely applied because it can be used with a variety of resemblance
coefficients and also because it forms clusters in a more conservative manner than many
other clustering methods (Gauch 1982:199, Romesburg 1984, James and McCulloch
1990:147). As a measure of secondary validity, an additional clustering technique,
complete linkage (farthest neighbor), was used to assess whether resulting clusters were
more-or-less real rather than mathematical artifacts (Gauch 1982, Romesburg 1984).

CHAPTER 4
COMPOSITION OF PIRANHA ASSEMBLAGES
In this chapter I compare the species composition of piranha assemblages from the
low Llanos to those from the upper Orinoco. I also examine and compare species
composition and richness among the nine drainages sampled, and present possible habitat
correlates. Little has been published on the distribution of Orinoco River fishes, with the
upper Orinoco being that part of the basin least explored ichthyologically. Because
sampling effort was not equal among all the drainages, I supplemented my data with
information from museum collections and published records. Although additional
collecting will likely add a few species to faunal lists for several of the drainages, the data
presented represent a first attempt at understanding piranha distribution patterns and habitat
preferences.
Figure 4-1 is a schematic representation showing the relative distances among
drainages in relation to their confluence with the main channel of the Orinoco River.
Table 4-1 is based on my samples supplemented by museum material, and shows the
species composition by region and drainage. A total of eleven piranha species were taken
from the two regions studied. Since 1979, ten species have been collected from the low
Llanos of Apure State, whereas my 1989-1991 samples indicate that at least eight species
occur in the upper Orinoco of the Amazon Territory of Venezuela. Seven species were
widely distributed and inhabited both regions. The Coefficient of Biogeographic
Resemblance (CBR) value comparing piranha species composition between the low Llanos
and the upper Orinoco was 0.78.
Piranha assemblages in five of the six upper Orinoco drainages were numerically
dominated by either S. rhombeus or S. manueli, or both. The exception was the Mavaca
57

58
Fig. 4-1. Schematic representation showing relative distances among the nine sampled
drainages and their approximate location along Orinoco River main channel.
Arrow indicates division between upper and lower Orinoco.

Table 4-1. Occurrence of piranha species in samples from nine drainages in the Orinoco River basin, Venezuela. C = common in fish
samples, P = present but uncommon in samples. Data based on my samples and MCNG material unless otherwise indicated.
River Drainages
Low LLanos
Upper Orinoco
Species
Apure
Capanaparo
Cinaruco Sipapo
Atabapo
Ventuari Matacuni
Ocamo
Mavaca
Totals
Serrasalmus medinai
C
1
Serrasalmus irritans
C
P
2
Serrasalmus elongatus
P
P
P
3
Pygocentrus caribe
C
P
P
P
4
Pygopristis denticulatus
P
P
P
P
P
P
6
Serrasalmus manueli
P
C P
C
C
5
Pristobrycon sp.
P
1
Serrasalmus rhombeus
P
C
C
C C
C
P
7
Pristobrycon striolatus
P
P
P
Pa
P
P
P
7
Serrasalmus altuvei
P
P
P
P
4
Serrasalmus cf.
eigenmanni
P
P P
P
C
5
Total number of species
8
7
6 1
4
6 3
5
5
a = Single specimen from Atabapo River drainage was recorded by Machado-Allison et al. (1989).
VO

60
River, where Serrasaimus cf. eigenmanni was the most common piranha collected.
Pygocentrus caribe is the predominant piranha throughout most of the Llanos, and was
abundant in samples from the Apure River drainage although absent or uncommon in the
Cinaruco and Capanaparo. Pygocentrus caribe was rare in the upper Orinoco.
Serrasaimus irritans and 5. medinai were locally common in the low Llanos, but neither
was taken in the upper Orinoco. Serrasaimus manueli, although absent from much of the
Llanos, was commonly taken along with S. rhombeus in the Cinaruco River. Pristobrycon
striolatus, although widespread, was never common in any one drainage.
Species occurred in one to seven of the nine drainages sampled (Table 4-1); most
were found in several (mean = 4.1) drainages, with Serrasaimus rhombeus and
Pristobrycon striolatus (taken in seven drainages) being the most widespread. Several
species were absent from two middle drainages, the Sipapo and Atabapo rivers. Two
species were limited to single drainages. In the Orinoco River basin, Pristobrycon sp. is
known only from the Atabapo drainage. Serrasaimus medinai was represented only in
Apure River samples (although it is found in other Orinoco tributaries that fringe the
Llanos, drainages not included in this study).
The number of piranha species per drainage ranged from 1 to 8 (mean = 5.0)
(Table 4-1). Sipapo drainage samples yielded only one piranha species (Serrasaimus
manueli), whereas all other drainages were inhabited by three or more species. The Apure
had the highest number of species (eight), but it was also the largest and best sampled
drainage. There was a significant correlation between numbers of piranha species and size
of drainage area (Spearman rank correlation, rs = 0.67, one-tailed P < .05, n = 9; Table 4-
2, Fig. 4-2).
Species composition of piranha assemblages across drainages was highly variable;
CBR values ranged from 0 (i.e., no species in common) to 0.83 (Table 4-2). Adjacent
drainages often shared many of the same species (Table 4-3), but waterways that had
many species in common (i.e., high CBR) were not always those drainages that were

61
geographically close (Fig. 4-3, Table 4-2). For instance, the Mavaca and Cinaruco were
somewhat similar in terms of species composition (CBR = 0.73), yet the two drainages are
far apart geographically. Similarly, the Apure drainage had four species in common with
the Ocamo, even though these two rivers are separated by roughly 1000 km of waterway
(Fig. 4-1). As expected, there was a significant negative correlation between species
composition resemblance (i.e., CBR) and the distance between adjacent drainages (rs =
- 0.66, one-tailed P < .05, n = 8; Table 4-2, Fig. 4-3). However, the relationship was
not significant at the 0.05 level when plotting all possible combinations of drainage-pair
distances against their CBR values (rs = 0.23, one-tailed, .10 > P > .05, n = 36; Table 4-
2, Fig. 4-4).
Figure 4-5 summarizes results of a UPGMA cluster analysis showing affinities
among the nine drainages based on CBR similarity values given in Table 4-3. In addition
to similarity in species composition, most resulting groups of drainages were related by
either geographic proximity, characteristics of the drainage (e.g., water type), or some
combination of these two factors. The first major cluster consisted of the three savanna
drainages (Capanaparo, Cinaruco, and Apure) and one upper Orinoco tributary (Ventuari).
The Capanaparo and Cinaruco are adjacent drainages and both were classified as
blackwater, but each receives high input from Clearwater streams. The Apure River is a
whitewater river with many small blackwater and Clearwater tributaries. The Ventuari also
is mainly a whitewater river although it has several large blackwater and Clearwater
tributaries. The second major cluster was formed by three drainages in the upper Orinoco.
This cluster consisted of the Matacuni, Ocamo, and Mavaca; all are whitewater rivers and
geographically close. The remaining two drainages, the Sipapo and Atabapo, did not
cluster with any of the other drainages. They were blackwater rivers with relatively few
piranha species. Clustering based on the farthest neighbor strategy resulted in drainage
groupings identical to that of the UPGMA method.

62
Table 4-2. Distance between drainages and Coefficient of Biogeographic Resemblance
(in parenthesis) among nine sampled drainages in the Orinoco River basin. Distances
measured in kilometers between drainage mouths by way of Orinoco River main channel.
CBR values range from 0 (no species in common) to 1 (complete similarity in species
composition)
River Drainages
Low Llanos
Upper Orinoco
Apu
Cap
Cin
Sip
Ata
Ven
Mat
Oca
Mav
Drainage area
(km2 x 103)
167
35
25
13
9.4
40.5
10.1
9.8
5.3
Number of
piranha species
8
7
6
1
4
6
3
5
5
Apure
110
(0.80)
160
(0.57)
400
(0)
530
(0.33)
610
(0.57)
945
(0.36)
965
(0.62)
1000
(0.62)
Capanaparo
50
(0.77)
290
(0.25)
420
(0.55)
500
(0.77)
835
(0.20)
855
(0.50)
890
(0.50)
Cinaruco
240
(0.29)
370
(0.60)
450
(0.83)
785
(0.44)
805
(0.55)
840
(0.73)
Sipapo
130
(0.40)
210
(0.29)
545
(0)
565
(0)
600
(0)
Atabapo
80
(0.60)
415
(0)
435
(0.22)
470
(0.44)
Ventuari
335
(0.44)
355
(0.73)
590
(0.73)
Matacuni
20
(0.75)
55
(0.75)
Ocamo
35
(0.80)
Mavaca

63
CD
O)
CO
c
2
T3
u_
CD
Q.
C/3
QD
O
CD
Q.
CO
CO
JZ
c
co
1
CL
10-
8-
6-
4-
2-
0 +-
3.0
o
Mav
3.5
*Cap
Apu
Cin*
OOca
Ata
O
Mat
O
Sip
o
Ven
= Low Llanos
O = Upper Orinoco
T 1 1 1 r
4.0 4.5 5.0 5.5
Log drainage area (km 2)
6.0
Fig. 4-2. Scatter diagram showing relationship between number of piranha species per
drainage and log of the drainage area size (km2) for nine sampled drainages in
Orinoco River basin, Venezuela. Drainage abbreviations are: Apu = Apure,
Ata = Atabapo, Cap = Capanaparo, Cin = Cinaruco, Mat = Matacuni, Mav =
Mavaca, Oca = Ocamo, and Sip = Sipapo.

64
Table 4-3. Number of shared piranha species and Coefficient of Biogeographic
Resemblance (CBR) (in parenthesis) among nine sampled drainages in the Orinoco River
basin. CBR values range from 0 (no species in common) to 1 (complete similarity in
species composition).
River Drainages
Low Llanos
Upper Orinoco
Apu Cap
Cin
Sip
Ata
Ven
Mat
Oca
Mav
Number of
piranha species
8 7
6
1
4
6
3
5
5
Apure
6
4
0
1
4
2
4
4
(0.80)
(0.57)
(0)
(0.33)
(0.57)
(0.36)
(0.62)
(0.62)
Capanaparo
5
1
2
5
1
3
3
(0.77)
(0.25)
(0.55)
(0.77)
(0.20)
(0.50)
(0.50)
Cinaruco
1
2
5
2
3
4
(0.29)
(0.60)
(0.83)
(0.44)
(0.55)
(0.73)
Sipapo
1
1
0
0
0
(0.40)
(0.29)
(0)
(0)
(0)
Atabapo
2
0
0
1
(0.60)
(0)
(0.22)
(0.44)
Ventuari
2
4
4
(0.44)
(0.73)
(0.73)
Matacuni
3
3
(0.75)
(0.75)
Ocamo
4
(0.80)
Mavaca

Coefficient of Resemblance (CBR)
65
1.0i
0.8-
0.6-
0.4
0.2-
o 0
0.0 "I 1 1 T 1 1 1 1
0 100 200 300 400
Distance between adjacent drainages (km)
Fig. 4-3. Scatter diagram showing similarity in piranha species composition between
adjacent sampled drainages versus distance between adjacent drainages.
Similarity measure was Duellman's (1990) Coefficient of Biogeographic
Resemblance.

Coefficient of Resemblance (CBR)
66
Distance between drainage pairs (km)
Fig. 4-4. Scatter diagram showing similarities in piranha species composition between all
possible paired drainages and the distance between paired drainages. Similarity
values and distances are from Table 4- 2.

67
O
r
o
0.5
1.0
Water Types
Dominant
Vegetation
APURE W (B,C) S
CAPANAPARO B (C) s
CINARUCO B (C) S
VENTUARI W (B,C) F
MATACUNI W F
OCAMO W (B) F
M A VACA W (B) F
SI PAPO B (C) F
ATABAPO B F
I I I
0.5 1.0
Coefficient of Biogeographic Resemblance
Fig. 4-5. Dendrogram from cluster analysis depicting similarities among nine sampled
drainages of Orinoco River basin based on piranha species composition. Major
and minor (in parenthesis) water types, W = whitewater, B = blackwater, and C
= Clearwater; Dominant regional flora, S = savanna (low Llanos), and F = forest
(upper Orinoco). Similarity values are from Table 4-3. Clustering technique
was UPGMA, and similarity measure was Duellman's (1990) Coefficient of
Biogeographic Resemblance.

68
A summary of species occurrence by habitat type is given in Table 4-4. Most
species were found in a variety of environmental conditions, but relative abundances
differed among sites. Serrasalmus rhombeus and S. manueli were frequently taken in
riverine habitats; other piranhas were more common in floodplain habitats (e.g., lagoons or
old meanders) and in caos with slow currents. In those cases where piranhas were found
in large streams or rivers, they commonly congregated in adjoining slackwaters near the
interface between fast-flowing and still waters, for example near the mouths of sloughs or
deep caos.
Most piranhas were found in two or all of the three major water types (Table 4-4),
but greatest numbers occurred in whitewater habitats. Three species (i.e., Serrasalmus
manueli, Pygopristis denticulatus, and Pristobrycon sp.) were usually associated with low-
pH, blackwater habitats Nevertheless, most species seem to tolerate a wide range of
temperatures and pH, as shown by wild-caught juveniles of both S. manueli and P.
denticulatus that have survived nine months (to date) in aquarium water with pH as high as
8.5. Water temperatures at sample sites ranged from 24.5 to 38 C, and pH 4.5 to 7.2;
water transparency ranged from very turbid (10 cm as measured with a Secchi disk), to
very clear (>3 m).
Where piranhas occur, two or more species are commonly taken together. In the
low Llanos, juveniles and subadults of as many as five species (i.e., Pygocentrus caribe,
Serrasalmus altuvei, S. irritans, S. medinai, and S. elongatus) were occasionally taken in
single seine hauls in floodplain pools of the Apure drainage. In the upper Orinoco, adults
of as many as four species of piranha (e.g., Serrasalmus rhombeus, S. cf. eigenmanni,
Pygocentrus caribe, and Pristobrycon striolatus) were caught together in gill nets set during
evening twilight. Sites of highest species richness were characterized by a large amount of
instream cover or other protection, including mats of aquatic vegetation, adjacent flooded
forest, or deep water. Small juvenile piranhas (<40 mm SL) were only found in

69
microhabitats where there was high cover provided by herbaceous plants. In the Llanos,
small piranhas relied on water hyacinth or flooded grasses for shelter and as a foraging
place. In the upper Orinoco, young juveniles were limited to a few sites where there were
mats of flooded grasses (e.g., stream edges) or shallow waters with dense growths of
submergent plants, such as beds of the aquatic plant Elodea.

Table 4-4. Summary of species occurrence by habitat and water type, based on samples in Orinoco River basin, Venezuela. Physico
chemical data represent minimum-maximum values recorded for water at capture sites. Transparency measured with Secchi disk.
Species
Habitat Type
Water Type
Physico-Chemical Ranges
Big
River
Stream
Lagoon/
Oxbow
Flooded-
forest
Flooded-
savanna
While
Clear
Black
pH
Temperature
(C)
Transparency
(m)
Pygocentrus caribe
X
X
X
X
X
X
X
X
6-7
26-30
0.1->2.0
Pristobrycon striolatus
X
X
X
X
X
X
X
6-6.7
27.5-30.5
0.5-1.0
Pristobrycon sp.
X
X
X
4.5
27
~2
Pygopristis denticulatus
X
X
X
X
4.5-6
26-38
1-2
Serrasalmus altuvei
X
X
X
X
X
6-7.2
24.5-31
0.1-1.0
Serrasahnus cf.
X
X
X
X
X
X
X
6-7
25-33
0.5-0.9
eigenmanni
Serrasalmus elongatus
X
X
X
X
X
6-6.5
29-29.5
0.1->2.0
Serrasalmus irritans
X
X
X
X
X
X
6-7
27-29.5
0.1->2.0
Serrasalmus manueli
X
X
X
X
X
X
X
4.5-6.5
24.5-31
0.7-2.3
Serrasalmus medinai
X
X
X
X
X
X
6-7
27-33
0.1-1.0
Serrasalmus rhombeus
X
X
X
X
X
X
X
6-7.2
24.5-31
0. l->2.0
Note: Physico-chemical parameters not measured at all sites, therefore ranges given in many cases are probably conservative.
-J
o

CHAPTER 5
TROPHIC ECOLOGY OF SAVANNA PIRANHAS: THE APURE DRAINAGE
This chapter focuses on the diets of piranhas from the area around the Femando
Corrales ranch and research station of the University of the Western Llanos (UNELLEZ),
located in the Cao Caicara region, Apure River drainage, in the low Llanos (Fig. 5-1). I
give this drainage separate treatment because it is the only site where long-term sampling
(1979-1990) has been carried out (Taphom and Lilyestrom 1984, Nico and Taphom 1984,
1985, 1988, Nico 1990, Taphorn 1990). The existing data base on piranhas from the
Cao Caicara region is the most complete of any single locality or drainage in the Orinoco
basin. The seven species examined were Pygocentrus caribe, Serrasalmus altuvei, S.
medinai, S. elongatus, S. irritaos, S. rhombeus, and Pristobrycon striolatus (Fig. 5-2). I
also report on the diet of the serrasalmine Catoprion ment, a close relative of the piranhas.
Study Area
The study area is located in the low Llanos of Apure State (0725'50"N,
693530"W) about 80 km W of the town of Mantecal (Fig. 5-1). Several permanent
streams border the 12,600-ha ranch, caos Caicara, Maporal, and Guaritico. These low-
gradient streams have mostly silty bottoms, and are bordered by narrow gallery forests.
The ranch is maintained primarily for grazing of cattle and encompasses open flat savanna
with a very gradual sloping terrain west to east. Most of the savanna floodplain of the
ranch is surrounded by a 2.5 m high earthen dike constructed to control flooding during the
rainy season and hold water during the drier part of the year. During the rains most of the
71

Fig. 5-1. Location of Cao Caicara study area, Apure Drainage, in low Llanos of Apure State, Venezuela. (Arrow indicates
Fernando Corrales ranch and research station of UNELLEZ).
to

Fig. 5-2. General body form and major fin markings of seven piranha species (55-70 mm
SL) and Catoprion ment (Cm) from Cao Caicara study area, Apure Drainage,
in the low Llanos of Venezuela: Pc = Pygocentrus caribe; Pst = Pristobrycon
striolatus, Smd = Serrasalmus medinar, Sr = Serrasalmus rhombeus,
Sa Serrasalmus altuvei, Sir = Serrasalmus irritaos, and Sel = Serrasalmus
elongatus.

Pc
Pst
Sel

75
savanna becomes flooded, with low areas covered by as much as 2 m of water. Lower
areas and deeper borrow pits contain water throughout the year, but most permanent water
sites are reduced to less than 1 m depth during the dry season. The fish species
composition of borrow pits resembles that of natural lagoon habitats. Large free-floating
mats of vegetation, primarily Eichhomia crassipes and E. azurea, are common in streams
and savanna pools. During high water, fishes can move between the streams and the
interior of the diked areas through culverts or low sections of the dike, but this interchange
has been greatly reduced as dike stability has been achieved. During the late dry season
(January to early April), the streams have little or no flow and are often reduced to isolated
pools. Rainy season flow is continuous with depths to 5 m or more. Width ranges from 3
to 12 m during low water to over 30 m during peak flooding. Although the Apure River
itself is white water in character, streams of the study area are essentially blackwater
habitats with low transparency. The flooded savanna pools are white water habitats,
usually very turbid (<10 cm Secchi disk), but the larger pools often become quite clear (>1
m Secchi disk) late in the rainy season.
Species Accounts
In this section, I describe the general morphology, local distribution and habitat,
and the diets of the piranha species found in the Cao Caicara study area. Information on
the smallest size class of piranhas, juveniles less than 20 mm SL, were pooled; all were
tentatively identified as Pygocentrus caribe. Figure 5-3 is a summary of the diets by size
class (Group II and larger) of the seven piranhas and Catoprion ment from the Cao
Caicara area.

Fig. 5-3. Diets by size class of seven piranha species and Catoprion ment from Cao Caicara study area, Apure River drainage,
in the low Llanos of Venezuela. Size of segments represents percentage of adjusted volume (Va) of each prey type; n =
number of stomachs examined; numbers in parentheses represent diet breadth using formula of Levins (1968).

S.L. (mm)
PYGOCENTRUS SERRASALMUS
CARIBE RHOMBEUS
SERRASALMUS SERRASALMUS
ELONGATUS IRRITANS
SERRASALMUS SERRASALMUS PRISTOBRYCON
MEDINAI ALTUVEI STRIOLATUS
CATOPR ION
MENTO
20-39
40-79
80-159
>160
n=84 (5.92) n=15(1.52)
n=29 (1.06)
n=80 (4.13) n=53 (3.27)
Plant material
Decapoda
n=12 (1.62) n=i 08)
n=162 (1.76) n=58 (2.02) n=3 (2.00) n=1 (1.00) n=50(1.66)
n=146 (3.13) n=10 (3.42) n=5(2.91)
\ \
/ .
\ \
Microcrustacea
Aquatic Insects
n=3 (1.69)
-4

78
Pvgocentms caribe (Valenciennes 1849)
Pygocentrus caribe was the most abundant piranha in the Cao Caicara area,
occurring in both flooded savanna and flowing waters. This blunt-headed, heavy-bodied
species (Fig. 5-2) reaches approximately 300 mm SL. Stomach contents of 516 P. caribe
in the four larger size classes are given in Table 5-1 and Figure 5-3. Unlike most other
piranha species, fish fins and scales were of minor importance in stomachs of juveniles.
Group II fish fed most heavily on aquatic insects, followed by microcrustaceans, but for
Group in fish flesh was the most important food item, followed by plant material
(primarily vascular plant debris) and aquatic insects. Larger P. caribe of groups IV and V
took mostly fish flesh and whole small fish.
Thirty-two species of prey fishes (mostly characins) were identified from stomachs
of Groups IV and V P. caribe (Table 5-2). There were also several instances of
cannibalism by adults on small juveniles. In addition to fish, larger juveniles and adults
sometimes ate other vertebrates, perhaps as carrion. Different stomachs contained a chunk
of flesh from a small caiman (Caiman crocodilus), skin of a lizard (probably Ameiva), and
a small adult leptodactylid frog. Three individuals taken together had stomachs full of
feathers, flesh, and bone fragments of a white-faced whistling duck (Dendrocygm
viduata). Mammals were not found in P. caribe from the study area, but I have found flesh
and fur of small rodents in specimens from nearby localities.
Serrasalmus irritara Peters 1877
Serrasalmus irritans was very common, usually second only to P. caribe in
numbers of individuals at most sampling sites. My sample consisted of 271 specimens
(Table 5-3 and Fig. 5-3). It has a moderately pointed snout (Fig. 5-2) and is seldom
longer than 160 mm SL. My study shows that juvenile S. irritans (Groups II and III)
specialized on fins of other fishes. Stomachs of the young of this piranha were typically
packed exclusively with fins, mostly from fish smaller or similar in size to the predator.

Table 5-1. Food items of Pygocentrus caribe from the Apure River drainage (Cao Caicara area) by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 516.
Size class (mm, SL)
Number examined
Number empty
Food items
II (20-39)
110
l
%0 %D %Va
III (40-79)
84
5
%0 %D %Va
IV (80-159)
176
18
%0 %D %Va
V(>160)
146
46
%0 %D %Va
Plant material
17.4
1.8
1.1
43.0
25.3
23.5
29.7
8.7
5.4
41.0
15.0
8.8
Decapoda
-
-
-
10.1
7.2
7.4
3.8
1.2
1.2
9.0
4.7
3.0
Microcrustaceans
78.0
23.7
21.4
19.0
3.6
2.6
-
-
-
-
-
-
Aquatic insects
80.0
55.3
60.7
32.9
14.5
14.7
0.6
-
-
11.0
4.7
3.0
Other invertebrates
36.7
14.0
12.3
30.4
10.8
12.4
5.1
1.2
0.6
21.0
4.7
2.0
Small whole fish
0.9
0.9
1.1
2.5
1.2
1.8
29.1
22.0
24.1
51.0
41.1
51.0
Fish flesh
0.9
0.9
1.1
29.1
19.3
25.3
. 81.6
59.0
63.7
38.0
17.8
20.5
Fish fins
-
-
-
36.7
8.4
4.1
12.0
0.6
0.3
7.0
2.8
1.8
Fish scales
-
-
-
17.7
2.4
1.8
12.0
4.6
2.8
12.0
3.7
2.0
Other
3.7
3.5
2.4
10.1
7.2
6.5
5.1
2.9
1.9
9.0
5.6
7.8
MD

80
Table 5-2. List of vertebrate prey taxa identified from the stomach contents of the four
most common piranhas from the Cao Caicara area, Apure River drainage, in the low
Llanos of Venezuela.
Species
Vertebrate Prey
(frequency of occurrence)
Pygocentrus caribe
Fish (whole or flesh): Characidae Aphyocharax erythrurus (6), Astyanax
bimaculatus (1), Astyanax sp. (3), Charax sp. (2), Cheirodon
pulcher (1), Ctenobrycon spilurus (22), Gymnocorymbus thayeri
(15), Hemigrammus marginatus (5), Hemigrammus sp. (5),
Moenkhausia dichroura (2), Odontostilbe pulcher (7), Poptella
orbicularis (6), Pygocentrus caribe (6), and Roeboides qffinis (1),
Roeboides dayi (8), Roeboides sp. (3), Serrasalmus eigenmanni (1),
Serrasalmus sp. (1), Triportheus sp. (1); Curimatidae Curimata
metae (10), curimatids (14); Lebiasinidae Pyrrhulina cf. lugubris (2);
characoid (8); Cichlidae Microgeophagus ramirezi (2), Gyranotidae -
Gymnotus carapo 1); Stemopygidae Sternopygus macrurus (1), and
Eigenmannia spp. (10); Hypopomidae Hypopomus sp. (1);
Auchenipteridae Entomocorus gameroi (1) and Parauchenipterus
galeatus (1); Pimelodidae Pimelodella sp.(l); Callichthyidae -
Hoplosternum ¡inrale (1); Rivuiidae (1). Fins of Hypophthalmidae -
Hypophthalmus cf. edentatus (1); Characidae Triportheus sp. (1).
Reptiles: Flesh of Caiman crocodilus < 1); flesh of lizard, probably
Ameiva (1).
Amphibians: Small adult leptodactyiid frog.
Birds: Feathers and flesh of white-faced whistling duck (Dendrocygna
viduata) (3).
Serrasalmus irritans
Fish (whole or flesh): Characidae Ctenobrycon spilurus (1),
Odontostilbe pulcher (2), Hemigrammus sp.(l), small juvenile
Pygocentrus caribe (1); Curimatidae Curimata metae (1), curimad
(1); characoid (4); gymnotoid (1); Cichlidae Micro geophagus
ramirezi (1), cichlid (1). Fins of adult Pygocentrus caribe (2).
Serrasalmus medinai
Fish (whole or flesh): Characidae Aphyocharax erythrurus (1),
Hemigrammus marginatus (2), Hemigrammus sp. (1), and
Odontostilbe pulcher (2), characid (2); Curimatidae Curimata metae
(2), curimatid (1); Cichlidae Microgeophagus ramirezi (1);
gymnotoid (1); catifish (1); Fins from Loricariidae (1).
Serrasalmus rhombeus
Fish (whole or flesh): Characidae Astyanax bimaculatus and Charax
sp.(l), characid (1); characoid (1); Doradidae Agamyxis'l (3);
unidentified catfish (1); Fins of Characidae Pygocentrus caribe (/);
Erythrinidae? (1).
Amphibians: Small adult frog (1).

Table 5-3. Food items of Serrasalmus irritans from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 271.
Size class (mm, SL)
Number examined
Number empty
Food items
%o
II (20-39)
29
1
%D
%Va
%o
III (40-79)
162
7
%D %Va
IV (80-159)
80
10
%0 %D %Va
Plant material
10.7
3.6
1.4
1.9
-
-
18.6
8.3
5.0
Decapoda
-
-
-
0.6
0.6
0.3
1.4
-
-
Aquatic insects
-
-
-
3.2
-
-
1.4
-
-
Other invertebrates
-
-
-
0.6
-
-
1.4
1.4
0.4
Small whole fish
-
-
-
3.2
3.1
4.0
18.6
13.9
18.8
Fish flesh
-
-
-
21.9
17.5
21.0
28.6
25.0
37.1
Fish fins
92.9
92.6
97.3
81.9
73.8
72.3
37.1
22.2
21.3
Fish scales
10.7
-
-
23.2
3.1
1.3
37.1
23.6
14.2
Other
3.6
3.6
1.4
3.9
1.9
1.2
8.6
5.6
3.3
oo

82
It was usually not possible to identify the fins eaten, but the thick red anal fins of
Pygocentrus caribe were found in two individuals. Large S. irritans preyed mostly on
small whole fish, fish flesh, fins, and occasionally scales. Fishes eaten whole or in pieces
by S. irritans are given in Table 5-2. A small juvenile P. caribe was found in the stomach
of one individual. No nonfish vertebrate remains were found.
Serrasalmus medinai Valenciennes 1849
Serrasalmus medinai was the third most common piranha in the study area; 124
specimens were analyzed for diet (Table 5-4 and Fig. 5-3). It is a medium-sized piranha,
usually less than 160 mm SL with a head shape that is intermediate between the robust P.
caribe and species with pointed snouts (Fig. 5-2). Unlike Pygocentrus, but similar to
other Serrasalmus, it has a series of ectopterygoid teeth that is easily seen even in small
individuals (from about 25 mm SL). It is primarily a fin-eater when small (20-79 mm
SL). The largest individuals (Group IV) fed chiefly on fish flesh, fins and scales, and
small whole fish. Prey fish identified from the stomachs of S. medinai are given in Table
5-2. The only fin identified was from an armored catfish. Shrimp and crabs were also
eaten.
Serrasalmus rhombeus (Linnaeus) 1766
Serrasalmus rhombeus was uncommon in flooded savanna of the Cao Caicara
study area, although on several occasions adults were taken in large numbers by hook and
line at night in Cao Maporal. Juvenile Serrasalmus rhombeus have a somewhat elongate
body and sharp snout (Fig. 5-2). They resemble S. irritans in body form, but are slightly
more robust. Adults have heavy rhomboidal bodies. The body and fins of large
individuals, some well over 300 mm SL, are black or blue-black, and the iris is often deep
red. I examined the stomach contents of 51 S. rhombeus from the Cao Caicara area
(Table 5-5 and Fig. 5-3).

Table 5-4. Food items of Serrasalmus medinai from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 124.
Size class (mm, SL)
II (20-39)
in (40-79)
IV (80-159)
Number examined
13
58
53
Number empty
0
2
3
Food items
%o
%D
%Va
%o
%D
%Va
%o
%D
%Va
Plant material
7.7
7.1
3.2
16.1
1.7
1.6
26.0
5.8
2.9
Decapoda
-
-
-
1.8
1.7
2.4
8.0
1.9
2.9
Aquatic insects
7.7
7.1
9.7
-
-
-
-
-
-
Other invertebrates
-
-
-
5.4
1.7
0.8
4.0
-
-
Small whole fish
-
-
-
5.4
3.4
4.0
]
14.0
14.0
9.6
13.7
Fish flesh
7.7
7.1
6.5
23.2
15.3
46.0
36.5
48.0
Fish fins
84.6
71.4
77.4
80.4
62.7
68.4
66.0
30.8
20.1
Fish scales
-
-
-
44.6
11.9
8.0
36.0
15.4
12.3
Other
7.7
7.1
3.2
1.8
1.7
0.8
-
-
-
oo

Table 5-5. Food items of Serrasalmus rhombeus from the Apure River drainage (Cao Caicara area) by size class.
%0 = percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N 51.
Size class (mm, SL)
Number examined
Number empty
Food items
II (20-39)
18
1
%0 %D %Va
Ill (40-79)
15
0
%0 %D %Va
IV (80-159)
8
1
%0 %D %Va
V(>160)
10
1
%0 %D %Va
Plant material
-
-
-
20.0
-
-
42.9
25.0
27.3
11.1
-
-
Microcrustaceans
23.5
15.8
10.9
-
-
-
-
-
-
-
-
-
Aquatic insects
47.1
26.3
32.6
-
-
-
14.3
-
-
11.1
-
-
Other invertebrates
5.9
-
-
-
-
-
28.6
12.5
9.1
33.3
-
-
Small whole fish
-
-
-
6.7
5.9
8.6
-
-
-
44.4
33.3
36.9
Fish flesh
-
-
-
13.3
11.8
8.6
28.6
12.5
18.2
55.6
22.2
21.1
Fish fins
64.7
57.9
56.5
93.3
76.5
80.0
71.4
50.0
45.5
33.3
33.3
31.6
Fish scales
-
-
-
26.7
5.9
2.9
42.9
-
-
22.2
-
-
Other
-
-
-
-
-
-
14.3
-
-
11.1
11.1
10.5
OO
4^

85
Juvenile S. rhombeus in size classes II-IV specialized on fish fins. Aquatic insects,
mostly plecopterans, were packed in the guts of several specimens from Cao Guaritico.
The ten largest S. rhombeus (Group V) had taken almost equal volumes of whole small
fish, chunks of fish flesh, and fish fins. Fishes identified from the stomachs of larger S.
rhombeus are given in Table 5- 2. Three large S. rhombeus collected at night in Cao
Maporal contained entire or partial individuals of small 20-30 mm SL doradid catfishes.
One individual had eaten a small adult frog.
Serrasalmus elonaatus Kner 1860
Serrasalmus elongatus was rare to uncommon in my samples in the study area. It
is a pikelike piranha (Fig. 5-2), having the most elongate body, relative to body depth, of
all piranhas. I examined 42 individuals, including a few from the small size class (Group
II) from other locations in the Apure River drainage (Table 5-6 and Fig. 5-3). Stomachs of
three small juveniles (20-39 mm SL) were packed with fins of other small fishes, and one
also contained a nematode (possibly a parasite). Stomachs of large specimens contained
fish fins and many scales. In addition, small whole fish and chunks of fish flesh were
taken by the largest S. elongatus.
Serrasalmus altuvei Ramirez 1965
Serrasalmus altuvei was rare in the Cao Caicaia area, and was found in both
streams and floodplain pools. It is a medium-sized piranha; maximum length in my
samples was less than 200 mm SL, with a deep narrow body and a slender pointed snout
(Fig. 5-2). It has a silver body and a broad, black terminal band on its unpaired fins,
none of my specimens from the Apure drainage had any red on the body. I examined the
stomachs of ten of 17 individuals collected in Cao Maporal and the flooded savanna

Table 5-6. Food items of Serrasalmus elongatus from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence (nonempty stomachs); %D = percent dominance; and %Va = percent adjusted volume. N = 42.
Size class (mm, SL)
Number examined
Number empty
Food items
II (20-39)
3
0
%Q %D %Va
Ill (40-79)
13
0
%0 %D %Va
IV (80-159)
21
1
%0 %D %Va
V(>160)
5
0
%0 %D %Va
Plant material
-
-
23.1
-
-
30.0
5.0
4.5
40.0
-
-
Decapoda
-
-
-
-
-
5.0
5.0
2.3
-
-
-
Other invertebrates
33.3
-
-
-
-
15.0
5.0
4.5
-
-
-
Small whole fish
-
-
-
-
-
10.0
10.0
9.1
20.0
-
-
Fish flesh
-
-
15.4
12.5
15.6
35.0
30.0
40.9
80.0
40.0
25.0
Fish fins
100.0
100.0 100.0
76.9
50.0
57.8
.40.0
20.0
18.2
40.0
20.0
37.5
Fish scales
-
-
84.6
37.5
26.6
50.0
20.0
18.2
80.0
40.0
37.5
Other
-
-
-
-
-
5.0
5.0
2.3
-
-
-
OO
Os

87
(Table 5-7 and Fig. 5-3). Fish fins, scales, flesh and small whole fish were found in the
two size classes (HI and IV) represented in our samples.
Pristobrycon striplatus ( Steindachner) 1908
Pristobrycon striolatus was rare in the Cao Caicara study area, and was collected
only on several occasions from Cao Maporal. It is a medium-sized species (Fig. 5-2),
less than 200 mm SL; the largest specimen taken from the Cao Caicara region was 156
mm. Adults sometimes had a red-orange chest and occasionally a pattern of orange vertical
bars along the sides. Pristobrycon striolatus has a rather blunt snout, but smaller and
weaker jaws and jaw musculature than Pygocentrus caribe. The body is deep and strongly
compressed. Small juveniles are similar to young Serrasalmus rhombeus but are slightly
stouter, lack ectopterygoid teeth, and have little if any side spotting. The largest individual
collected in the study area was 159 mm SL. I examined the stomach contents of 16 of the
38 specimens collected. Food items by size class are given in Table 5-8 and Figure 5-3.
Specimens in Group II fed mostly on fish fins as did the one Group IE specimen
examined. Three adults from Group IV contained fish flesh, a few scales, shrimp
fragments, an adult aquatic beetle, an aquatic hemipteran and unidentified insect fragments.
Catoprion ment (Cuvier) 1819
Catoprion ment was common in many of the streams and savanna pools. It is a
small, deep-bodied species (Fig. 5-2) that is closely related to piranhas. Although
maximum size is around 120 mm SL, in the Apure drainage most specimens sampled were
under 80 mm SL, and none was greater than 100 mm. The teeth of C. ment are
somewhat everted and its long lower jaw swings open to more than 180 degrees, making it
well suited for scraping scales off other fish. The stomachs of all 104 specimens examined
contained fish scales (ranging up to 23 mm in diameter) (Table 5-9 and Fig. 5-3). Plant
material, primarily comprising vascular debris and root wads, and occasionally filamentous

88
Table 5-7. Food items of Serrasalmus altuvei from the Apure River drainage (Cao
Caicara area) by size class. %0 = percent frequency of occurrence; %D = percent
dominance; and %Va = percent adjusted volume. N = 10.
Size class (mm, SL)
m(40-79)
IV(80-159)
Number examined
3
7
Number empty
0
. 0
Food items
%0
%D
%va
%0
%D
%va
Plant material
-
-
-
28.9
-
-
Small whole fish
33.3
33.3
50.0
-
-
-
Fish flesh
33.3
-
-
42.9
30.0
50.0
Fish fins
66.7
66.7
50.0
71.4
40.0
31.3
Fish scales
-
-
-
42.9
30.0
18.8
Other
_
_
_
14.3
_
_

Table 5 8. Food items of Pristorbrycon striolatus from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N 16.
Size class (mm, SL)
Number examined
Number empty
Food items
%o
11 (20-39)
12
1
%D
%Va
%o
m(40-79)
1
0
%D
%Va
IV (80-159)
3
0
%0 %D %Va
Decapoda
-
-
-
-
-
-
66.7
33.3
28.6
Aquatic insects
27.3
18.2
13.3
-
-
-
66.7
-
-
Other invertebrates
3.9
-
-
-
-
-
33.3
33.3
28.6
Fish flesh
18.2
9.1
10.0
-
-
-
33.3
33.3
42.9
Fish fins
81.8
72.7
76.7
100.0
100,0
100.0
-
-
-
Fish scales
-
-
-
-
-
-
33.3
-
-

Table 5-9. Food items of Catopon ment from the Apure River drainage (Cao Caicara area) by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 104.
Size class (mm, SL)
II (20-39)
III (40-79)
IV (80-159)
Number examined
51
50
3
Number empty
0
0
0
Food items
%o
%D
%va
%o
%D
%Va
%0
%D
%Va
Plant material
25.0
2.0
2.1
50.0
19.0
16/1
33.3
33.3
28.6
Microcrustaceans
2.0
-
-
-
-
-
-
-
-
Aquatic insects
2.0
-
-
-
-
-
-
-
-
Other invertebrates
3.9
2.0
1.4
-
-
-
-
-
-
Small whole fish
-
-
-
4.0
3.4
5.0
-
-
-
Fish flesh
-
-
-
2.0
1.7
2.5
-
-
-
Fish fins
-
-
-
2.0
1.7
0.8
-
-
-
Fish scales
100.0
96.1
96/4
100.0
74.1
75.6
100.0
66.7
71.4

91
algae, was present in small amounts in many stomachs. Rare items included an aquatic
beetle larva, a cladoceran, and the head of a small characid fish {Aphy ochar ax erythrurus).
Small juvenile piranhas. Group I (10-19 mm SL)
Most piranhas spawn at the onset of the rainy season. Small juveniles inhabit the
flooded grasses and marsh habitats of the flooded savanna. The newly flooded savanna
acts as a prime nursery area for young fish since the flooded herbaceous vegetation
provides protection from predation and produces an abundant supply of invertebrates that
are utilized for food. The 114 stomachs of small juvenile piranhas contained mostly
microcrustaceans and aquatic insects (Table 5-10 ). As size increased within this group
there was a gradual switch from microcrustaceans to small aquatic insects. Primary food
items, in order of importance (high %Va and %D), were: cladocerans, chironomid larvae,
copepods, and ostracods.
Comparison of Diets
Fish (flesh, fins, scales and small whole fish) were the main component of diets of
all seven species of piranhas, both in terms of dominance and adjusted volume (Fig. 5-3).
Only in small juveniles of Group I and juvenile P. caribe less than about 80 mm SL (or
where sample sizes were small, e.g., Group IV P. striolatus) did non-fish items make up a
large proportion. Most juveniles had eaten fish fins. Major exceptions were P. caribe, a
generalist, and C. ment, a highly specialized scale-eater. Fins were usually from fishes
similar in size to the predator. Based on this observation, one may assume juvenile
piranhas were attacking small species or juveniles of other fishes. Whereas fish were the
predominant food resource used by savanna populations, other vertebrates (i.e., mammals,
birds, reptiles, and amphibians) were only of minor importance (Table 5-2).

92
Table 5-10. Food items of small juvenile piranhas (Size Class 1,10-19 mm SL),
tentatively identified as Pygocentrus cabe, from the Apure River drainage (Cao
Caicara area). %0=percent frequency of occurrence (nonempty stomachs); N = mean
number per nonempty gut; %D = percent dominance; and %Va = percent adjusted
volume.
Number examined
Number empty
Food items
%0
N
114
3
%D
%Va
Plant material
5.4
nda
-
-
Microcrustaceans
91.0
27.5
54.8
58.1
Aquatic insects
73.0
3.4
37.9
36.9
Other invertebrates
12.6
0.2
4.0
2.3
Other
7.2
nda
3.2
2.7
a Not determined/not applicable

93
I rarely found evidence of seed-eating by piranhas in the Cao Caicara site, with the
few seeds eaten being very small and probably taken incidentally along with intended prey
items. Although other plant material, such as bits of leaves, grass blades, root wads, tiny
flowers, and filamentous algae, was ingested, these items were usually of minor
importance in terms of dominance and volume. Of hundreds of specimens examined, not
one stomach contained many seeds. Most of the low Llanos, including gallery forests, do
not produce many large fruits or big seeds. By way of comparison, stomachs of the
herbivorous adults of Mylossoma sp. and Metynnis sp., taken in the Cao Caicara study
area, were typically full of filamentous algae, masticated small seeds, and nonwoody
vascular plant debris.
Diets and diet breadth usually changed with age. Diet breadth values were typically
higher for the larger size classes (Fig. 5-3 and 5-4), but C. ment (the highly specialized
scale-eater) had low diet breadth values (1.08 to 1.69) for all size groups. Group III P.
caribe, with 5.92, had the widest breadth.
Table 5-11 is a matrix showing the diet overlap values for piranhas, by size class,
from the Cao Caicara area. Cluster analysis of the Table 5-11 data produced four major
trophic groupings (Fig. 5-5). Cluster I consisted of small juvenile piranhas that fed on
small invertebrates, mostly microcrustaceans and aquatic insects. Cluster II contained
seven species and three different size classes grouped together based on their high degree
of piscivory. These piranhas frequently fed by cutting out chunks of flesh from other fish;
however, diets also included an assortment of small fish taken whole, fish fins, and fish
scales. Cluster HI represented fin-eating piranhas. It included six species, and most were
in size classes that included individuals between 20 and 80 mm SL. The only exception
was adult Serrasalmns elongatus in the >160 mm SL size range. Cluster IV was composed
of scale-eaters and represented by the three size classes of Catoprion ment. As a reflection
of the intraspecific changes or shift in diet with age or size, most species were divided
among two or more of the different cluster groupings.

94
6n
5-
S2 4-
*'
TD
CO
CD
0)
Q 2-
1 -

20-39 mm
fl
40-79 mm

80-159 mm

>160 mm
i! /
fSf /
i /
m/
Ms
ms
l
P. caribe S. rtiombeus S. elongatus S. irritans S. medin S. altuvei P. striolalus C. ment
Species
Fig. 5-4. Diet breadths estimated for eight piranha species, by size class, from the Cao
Caicara area of the low Llanos, Apure River drainage, Orinoco River basin,
Venezuela. Diet breadth calculated using formula of Levins (1968). Most
species not represented in all size classes. Size ranges are standard length.

Table 5-11. Matrix of diet overlaps among different size classes of piranhas from Cao Caicara area, Apure River drainage, low Llanos.
Overlap index is that of Schoener (1970); SL = Standard Length; JV = small juveniles; see Table 3-1 for species abbreviations.
Species and
Size Range
(mm SL)
PC
2039
PC
4079
PC
80159
PC
£160
SR
2039
SR
4079
SR
80159
SR
£160
SEL
2039
SEL
4079
SEL
80159
SEL
£160
SIR
2039
SIR
4079
SIR
80159
SMD
2039
SMD
40-79
SMD
80159
PST
2039
PST
4079
PST
80159
CM
2039
CM
4079
CM
80159
SA
4079
SA
80159
JV
1019
PC 20-39
100
35.2
5.75
10.7
43.6
2.1
11.2
4.5
0
1.05
10.05
1.05
2.4
3.3
6
14.25
4.85
3.3
14.35
0
13.3
2.5
3.25
1.05
1.05
1
62.9
PC 40-79
100
38.25
49.2
21.35
16.2
54.8
33.4
4.05
21.45
46.55
30.85
6.8
29.6
41.6
26.65
27.25
38.8
27.35
4.05
45
5.3
22.95
25.25
5.85
31.1
22.25
PC 80-159
100
56.05
0.3
20.25
24.45
47.35
0.3
18.7
61.3
28.1
3.05
28.05
66.25
11.9
25.3
68.95
10.3
0.3
28.1
5.55
16
8.2
24.4
53.05
2.5
PC £160
100
4.85
21
30.8
67
1.85
19.45
44.55
24.35
4.6
29.1
51.8
17.75
27.45
43.9
14.85
1.85
25.5
5.6
19.15
10.85
70.55
24.3
7.75
SR 20-39
100
56.45
45.45
31.55
56.5
56.5
18.2
37.5
56.45
56.45
21.25
66.2
56.5
20.15
69.8
56.5
0
0
0.8
0
0
31.25
43.5
SR 40-79
100
54
48.7
79.95
69.25
38.25
48.95
79.9
86.1
41.3
83.85
83.85
40.2
85.25
79.95
8.5
2.9
11.15
2.85
58.55
42.7
0
SR 80-159
100
39.2
0
15.55
54.45
24.95
46.8
63.6
60.2
18.75
19.55
62.1
19.05
0
42.8
2.1
23.55
27.25
18.15
45.4
2.25
SR £160
100
31.55
47.15
50.65
52.65
32.9
57.7
64.4
41.25
50.35
54.9
41.55
31.55
21
0
8.25
0
68.45
52.3
2.7
SEL 20-39
100
57.8
18.2
37.5
97.25
72.25
21.25
77.4
68.4
20.1
<-7
100
0
0
0.8
0
50
31.3
0
SEL 40-79
100
52
79.7
57.75
74.65
51.05
64.3
79.8
48.05
{ 8
57.8
15.55
26.65
29.9
26.6
50
65.65
0
SEL 80-159
100
64.8
20.95
20.95
85.75
30.2
49.7
85.75
28.2
18.2
47.65
21.75
31
22.7
27.3
77.25
4.6
SEL £160
100
37.45
59.75
60.45
44
59.5
57.45
47.5
37.5
24.95
37.5
40.8
37.5
37.5
75.05
0
SIR 20-39
100
73.4
24
80.15
70.55
21.5
76.65
97.25
0
1.4
2.15
1.35
49.95
31.2
1.4
SIR 40-79
100
48.7
79.95
88.75
46.7
82.27
72.3
21.2
1.3
8.55
1.25
53.95
53.5
1.15
SIR 80-159
100
34.15
50.05
86.1
31.25
21.3
37.4
16.7
27.45
19.15
40.05
72.5
3.05
SMD 20-39
100
77.3
29.55
92.9
77.4
6.45
2.15
6.5
3.2
50
37.75
12.4
SMD 40-79
100
50.15
78.4
68.4
17.15
10.45
16.9
9.6
54
53.25
1.6
SMD 80-159
100
30.15
20.1
45.8
14.5
23.55
15.25
33.85
80.4
0.05
PST 20-39
100
76.7
9.95
0
3.3
0
50
41.25
13.3
PST 40-79
100
0
0
0.8
0
50
31.3
0
PST 80-159
100
1.4
2.45
0
0
42.8
2.25
CM 20-39
100
77.75
73.55
0
18.8
1.4
CM 40-79
100
87.5
5.8
22.05
0
CM 80159
100
0
18.75
0
SA 4079
100
31.25
0
SA 80-159 100 0

96
O
r
25
-r~
50
~T~
75
r
L.
0
25 50 75
Percent diet similarity
100
1
General
Piscvoros
H
JV 10-19 J_ Aquatic Insects/
PC 20-39 _T Microcrustaceans
PC 40-79 _
SR 80-159
PC 80-159
SEL 80-159
SIR 80-159
SMD 80-159
SA 80-159
PST 80-159
PC >160
SA 40-79
SR >160 _J
SR 20-39
SR 40-79
SIR 40-79
SMD 40-79
SMD 20-39
PST 20-39
SEL 20-39
PST 40-79
- Fin Eaters
SIR 20-39
SEL 40-79
SEL >160 J
CM 20-39
CM 40-79
CM 80-159 J
- Scale Eaters
100
Fig. 5-5. Dendrogram from cluster analysis depicting similarities among diets of piranhas
and related species (by size class) from the Cao Caicara area of the low Llanos,
Apure River drainage, Orinoco River basin, Venezuela. Similarity values are
from Table 5-11, dendrogram UPGMA-generated using overlap index of
Schoener (1970). Size ranges are in mm Standard Length. Species
abbreviations are as follows: PC = Pygocentrus caribe; PST = Pristobrycon
striolatus; SMD = Serrasalmus medinai; SR = Serrasalmus rhombeus, SA =
Serrasalmus altuvei, SIR = Serrasalmus irritaos, SEL = Serrasalmus elongatus,
and CM = Catoprion mento\ JV = small juveniles.

CHAPTER 6
TROPHIC ECOLOGY OF PIRANHAS FROM THE UPPER ORINOCO
This chapter focuses on the trophic ecology of piranhas and related species from the
upper Orinoco River basin of southern Venezuela, a region characterized by extensive
lowland forests that undergo seasonal flooding. I also provide information on the diets of a
few savanna populations not reported in the previous chapter, and compare feeding patterns
of serrasalmine fishes from savanna with those from forested regions. Finally, I examine
the relationship between intestine length and serrasalmine diets.
There have been few studies of the fishes inhabiting the upper Orinoco River
region. To date, published works have dealt mainly with descriptions of new species or
reports of species distributions as part of broader investigations on South American fish
zoogeography. The research presented here is the first field study of fishes from the
southern region of Venezuela aimed at understanding fish feeding patterns. Although
feeding behaviors among certain piranha species are somewhat similar, the diets of several
species have not been reported previously. The eight species of piranhas examined from
the upper Orinoco are Serrasalmus rhombeus, S. manueli, S. cf. eigenmanni, S. altuvei,
Pygocentrus caribe, Pygopristis denticulatus, Pristobrycon striolatus, and an undescribed
Pristobrycon sp. (Fig. 6*1). I also report on the diets of several other serrasalmine fishes,
focusing primarily on Catoprion ment, Myleus asterias, M. schomburgkii, and M.
torquatus.
97

Fig. 6-1. Eight piranha species from the upper Orinoco River basin of Venezuela.
Sm = Serrasalmus manueli, Sr = S. rhombeus, Seg = S. cf. eigenmanni,
Sa = S. altuvei, Pst = Pristobrycon striolatus, Pc = Pygocentrus caribe,
Pyp = Pygopristis denticulatus, and Psp = Pristobrycon sp.

99

100
Species Accounts
Figure 6-2 is a summary of the diets by size class of the eight piranha species taken,
in the upper Orinoco. A partial listing of prey items identified from the stomachs of the
common piranhas is given in Table 6-1. In this section I describe the general morphology,
local distribution and habitat, as well as the diets for each of the upper Orinoco piranhas
and several other serrasalmine fishes.
Serrasalmus rhombeus (Linnaeus 1766)
Serrasalmus rhombeus was the most abundant piranha in most samples from the
upper Orinoco River. Greatest numbers were found in whitewaters such as the Ocamo and
Paru rivers where they typically inhabited main channel borders. Serrasalmus rhombeus
(Fig. 6-1) was also the largest piranha species taken, reaching well over 350 mm SL. Like
many piranhas, it varies ontogenetically in both body form and coloration. Juveniles have
a moderately elongate body and pointed snout, whereas adults are robust with a relatively
deep body. Juvenile body color is silver with black spotting, and the caudal fin has a
terminal black band. The body and fins of large adults are darkly pigmented, typically
gray or blue black.
Serrasalmus rhombeus was one of the most carnivorous of the upper Orinoco
piranhas (Fig. 6-2 and Table 6-2). Individuals from 40-159 mm SL (Groups ni-IV) fed
mostly on fish flesh and fins, and the largest specimens examined (>160 mm) had fed
mainly on small fish. Only a few of the prey fish ingested could be identified (Table 6-1).
A large S. rhombeus contained the skeletal remains of an adult toad identified as Bufo
marinas, but overall they rarely preyed upon non-fish vertebrates. Plant material was also
relatively unimportant in their diet, small quantities being found in stomachs of only 11 of
the 83 specimens and accounting for less than 5% of the total food volume. Most or all of
these plant items were probably ingested incidentally .while attacking other prey. Plant

Fig. 6-2. Diets by size class (> 40 mm SL) of eight piranha species from the upper Orinoco River basin, Venezuela. Size of
segments represents percentage of volume (%V) of each prey type; n = number of stomachs examined; numbers in
parentheses represent diet breadth using formula of Levins (1968).

S.L. (mm)
20-39
40-79
80-159
^ 160
SERRASALMUS SERRASALMUS SERRASALMUS SERRASALMUS PYGOCENTRUS PRISTOBRYCON PRISTOBRYCON PYGOPRISTIS
RHOMBEUS MANUELI cf. EIGENMANNI ALTUVEI
CARIBE STRIOLATUS
SP.
n=2 (1.47) n=18(1.83)
n=52 (2.99) n=42(1.99)
BMasticated Seeds
Other Plant Material
Microcrustaceans
Decapoda
n=7 (2.10)
n=8 (1.82) n=1 (1.11)
n=5 (1.08)
DENTICULATUS
n=1 (1.07)
o
K>

103
Table 6-1. List of laxa identified from the stomach contents of the three most common
piranha species from upper Orinoco River drainages, Venezuela.
Species
Food Item
(frequency of occurrence)
Serrasalmus rhombeus
Fish remains (small whole fish or flesh): Ctenoluciidae Boulengerella
sp. (1); catfish: Callichthyidae Corydoras sp. (1); Auchenipteridae
(1); Pimelodidae (1); Doradidae (probably Liphodoras).( 1); unidentified
catfish remains (2); Cichlidae (2), other fish (32).
Bird; fragments of feather and bone (1).
Amphibians: skeletal remains of adult toad Bufo marinus.il).
Invertebrates: Decapoda: crab(l); Arthropoda- terrestrial beetle (1),
adult beetle Gyrinidae (1), insect larva (1), unidentified insect (1),
terrestrial insect (1), Orthopteran leg (1); Gastropoda snail (1).
Plant Material: Filamentous algae (1); unidentified flower (1); leaf or leaf
fragments (2); woody twigs (1); root fibers (5), seed fragments? (2)
Serrasalmus manueli
Fish (whole fish or flesh): characoid ( ); Cichlidae juvenile Cichia
temensis.{\)\ gymnotoid eel remains (1); catfish remains (Doradidae
or Auchenipteridae) (2), catfish remains (1), unidentified fish (24).
Reptiles: Lizard remains (1).
invertebrates: Decapoda: Macrobrachium olfersi (1), unidentified shrimp
(2), decopod leg fragment (1); terrestrial insect (3), unidentified insect
(1).
Plant Material: small flowers of a Lecythidaceae Gustavia sp.? (1);
Palmae fruit of Bactris gasipaes ? (2); unidentified masticated seeds
(9); leaf fragments (3); unidentified pieces of fruit (exocarp and
mesocarp) (1); vascular plant material (2).
Serrasalmus cf. eigenmannii
Fish (whole fish or flesh): unidentified fish remains (7).
Plant Material (all unidentified): flowers fregments (2); masticated seeds
(mostly endocarp) (35).

Table 6-2. Food items of Serrasalrnus rhombeus from the upper Orinoco River basin by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %V = percent volume. N = 83.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
HI(40-79)
2
0
%D
%V
%o
IV(80-159)
29
7
%D
%M
%0
V(>160)
52
16
%D
%V
Plant material
-
-
-
18.2
4.6
5.1
13.9
5.3
1.9
Decapoda
-
-
-
-
-
-
2.8
2.6
5.2
Aquatic insects
-
-
-
4.6
4.6
0.7
-
-
-
Other invertebrates
-
-
-
13.6
-
1.5
5.6
2.6
0.7
Small whole fish
4.6
4.6
3.4
8.3
5.3
33.3
Fish flesh
50.0
50.0
80.0
40.9
36.4
49.8
58.3
50.0
46.3
Fish fins
50.0
50.0
20.0
59.1
40.9
31.0
13.9
13.2
3.8
Fish scales
-
-
-
22.7
9.1
8.6
25.0
15.8
3.0
Other
-
-
-
-
-
-
8.3
5.3
5.9

105
materials eaten by four Group FV fish consisted of a small leaf, fine roots, and a small
amount of filamentous algae, while five large adults (>160 mm SL) had fed on an
unidentified flower, a leaf fragment, woody twigs, and some small root fibers.
My samples of Serrasalmus rhombeus from the upper Orinoco did not include
individuals less than 40 mm SL. Juveniles found in the low Llanos frequently take fins, as
is probably true also for young S. rhombeus inhabiting the upper Orinoco. IL/SL ranged
from 0.9 for a 158-mm SL fish, to a high of 1.7 for a 233-mm SL adult.
Serrasalmus manueli Femandez-Yepez and Ramirez 1967
Serrasalmus manueli was the most abundant piranha in many of the blackwater
rivers, such as the Atabapo and the Sipapo. It was also found together with S. rhombeus
in a few of the larger whitewater rivers, including the upper Orinoco main stem and the
Ventuari. Serrasalmus manueli (Fig. 6-1) was the second largest piranha found in the
upper Orinoco basin; individuals over 270 mm SL were fairly common, and one specimen
from the Atabapo drainage was 340 mm SL. The shape of the body is similar to S.
rhombeus. Young are relatively elongate and sharp-snouted, whereas large adults have a
fairly deep, thick body, and broad, powerful jaws. The body of S. manueli has many
elongated vertical and irregularly-shaped dark markings, and black coloring is found along
the base of the caudal fin. Large juveniles and adults have a large, black humeral spot, and
the cheek and breast of adults are sometimes red-orange. The body color of S. manueli
changes from silvery to almost black with age as is true also for 5. rhombeus. However,
like many neotropical fish, those inhabiting blackwaters are darker or more heavily
pigmented than individuals taken in turbid whitewaters. Unique among piranhas, the first
few anterior rays of the dorsal fin have filaments that may be greatly elongated in older
juveniles and adults, but most individuals lose this ornamentation to other fin-eating fishes.
The diet of Serrasalmus manueli has never before been reported. Diets of
specimens from the upper Orinoco are given in Figures 6-2 and Table 6-3. Large S.

106
manueli (>160 mm SL) preyed heavily on fishes, but plant material was occasionally taken
in mass, with plant matter occurring in 12 of 42 Group V stomachs and accounting for
25% of total food volume. Five of six adult S. manueli (>160 mm SL), caught with hook.
and line in the Sipapo River during high water, contained large amounts of masticated
seeds, primarily endocarp, and the sixth was packed with small flowers of a Lecythidaceae,
possibly Gustavia sp. Seven specimens from other forest sites had fed on leaf fragments
and pieces of fruit (exocarp and mesocarp); some of the fruit was identified as the palm
Bactris gasipaes (Palmae). Prey fishes and other items identified from stomachs are given
in Table 6-1. IL/SL ranged from 0.7 for a 52-mm SL juvenile, to 2.2 for a 250-mm SL
adult.
In addition to the 78 large specimens, I examined five small Serrasalmus (<40 mm
SL) that I tentatively identified as juveniles of S. manueli. These small fish, together with
young of Pristobrycon striolatus, were taken from a clump of macrophytes near the banks
of the lower Yureba River, a blackwater tributary of the Ventuari. All five fish had a
prominent black spot on the dorsal fin and well-developed ectopterygoid teeth. The
stomach of a single individual less than 20 mm SL (Group I) contained aquatic insects
(Fig. 6-3), while those of four Group II individuals were packed with fins of other small
fishes (Fig. 6-3, Table 6-3). IL/SL of these small juveniles was less than 1.0.
Serrasalmus cf. eigenmanni Norman 1928
Serrasalmus cf. eigenmanni was the third most common piranha in samples from
the upper Orinoco. It was the most abundant piranha taken in the Mavaca River drainage,
was relatively common in the Ocamo and Matacuni drainages, and a single individual was
taken from the Paru River of the lower Ventuari. All of the above are basically whitewater
rivers. Serrasalmus cf. eigenmanni (Fig. 6-1) is a medium-sized piranha, the largest
specimens collected being two gravid females of 180 mm SL. It has a somewhat blunt
snout, and in terms of body shape, most resembles S. medinai, a species found in the

Table 6-3. Food items of Serrasalmiis manned from the upper Orinoco River basin by size class. %0 percent frequency of
occurrence; %D = percent dominance; and %V = percent volume. N = 82.
Size class (mm, SL) 11 (20-39) III (40-79) IV (80-159) V(>160)
Number examined 4 18 18 42
Number empty 0 5 7 16
Food items
%o
%D
%v
%o
%D
%V
%o
%D
%V
%o
%D
%V
Masticated seeds
-
-
-
-
-
-
9.1
-
0.1
30.8
19.2
9.5
Plant material
-
-
-
15.4
7.7
1.5
27.3
18.2
13.1
15.4
11.5
15.1
Decapoda
-
-
-
-
-
-
-
-
-
15.4
3.8
2.9
Aquatic insects
-
-
-
-
-
-
9.1
-
0.01
-
-
-
Other invertebrates
-
-
-
7.7
-
0.8
18.2
18.2
1.0
11.5
7.7
1.2
Fish flesh
-
-
-
38.5
30.8
68.2
45.5
40.9
81.8
69.2
46.2
68.5
Fish fins
100.0
100.0
100.0
28.7
57.7
28.7
27.3
22.7
4.1
3.8
3.8
1.4
Fish scales
-
-
-
7.7
-
0.1
-
-
-
11.5
-
0.3
Other
_
_
_
7.7
3.8
0.8
-
-
-
11.5
7.7
1.0
Note: Stomach contents of a single specimen of Group I size class (10-19 mm SL) consisted of aquatic insects.
o
-j

Fig. 6-3. Diets of selected small juvenile piranhas (10-19 mm SL) from upper Orinoco River drainages and the low Llanos,
Venezuela. Size of segments represents percentage of volume of each prey type; n = number of stomachs examined;
numbers in parentheses represent diet breadth using formula of Levins (1968).

UPPER ORINOCO
LLANOS
S.L. (mm)
SERRASALMUS PRISTOBRYCON PYGOPRISTIS
MANUELI STRIOLATUS DENTICULATUS
PYGOCENTRUS
CARIBE
n = 114(2.11)

Other Plant Material
I
Other Invertebrates
Microcrustaceans
Fish Fins
\ \ V
/ / /
\ N \
Aquatic Insects
Other

110
Llanos. Individuals of all sizes are silver-colored and have numerous irregularly-shaped
dark spots, with the number and shape of the spots being quite variable. Adults have a
rather faint black humeral spot The base of the caudal fin is black, which in older fish
covers nearly the entire tail except for a terminal hyaline band. Parts of the cheek and
breast, as well as the pectoral and anal fins, are reddish orange. Although Serrasalmus cf
eigerunanni may involve a species complex (W. Fink, personal communication), I
distinguished only one species in my samples.
The diet of this species has not been reported previously. All larger 5. cf.
eigenmanni were primarily seed predators (Fig. 6-2 and Table 6-4). Masticated seeds,
mostly endocarp, were found in 35 of 46 Group IV and V specimens and accounted for
75% of total food volume. The only other plant materials found were fragments of mature
flowers in two stomachs. Unfortunately none of the seeds or flowers could be identified.
Although its natural diet consisted primarily of seeds, as in other piranhas, adult 5. cf.
eigenmanni readily take hooks baited with fish flesh. The stomachs of two young juveniles
(48 and 76 mm SL) examined were packed exclusively with fins of other small fishes.
IL/SL ratio (n = 32) ranged from 0.9 for a 48-mm SL juvenile, to 3.4 for a 129-mm SL
adult.
Serrasalmus altuvei Ramirez 1965
Serrasalmus altuvei was uncommon in samples from the upper Orinoco. It is a
medium-sized piranha, with a slender pointed snout and a deep body that is more laterally
compressed than that of most other piranhas (Fig. 6-1). The body is silvery, and the sides
are covered with black spots that are vertically elongated in most juveniles and some adults.
Large juveniles and adults have a dark humeral spot and a black terminal band on the caudal
fin. Live S. altuvei from the Mavaca River were found to have a partly red iris, which was
less intense than that of 5. rhombeus. I collected 12 fish (119-169 mm SL), from the
Mavaca, Ocamo and Matacuni rivers, and examined the stomach contents of 9 specimens

Table 6-4. Food items of Serrasalmus cf. eigenmanni from the upper Orinoco River basin by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %V = percent volume. N =4 8.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
m(40-79)
2
0
%D
%v
%0
IV(80-159)
40
2
%D
%V
%o
V (>160)
6
0
%D
%V
Masticated seeds
-
-
-
78.9
63.2
74.4
83.3
83.3
76.4
Plant material
-
-
-
5.3
-
0.9
-
-
-
Aquatic insects
-
-
-
2.6
-
0.4
-
-
-
Other invertebrates
-
-
-
7.9
2.6
1.1
-
-
-
Fish flesh
-
-
-
15.8
13.2
11.6
33.3
-
12.4
Fish fins
100.0
100.0
100.0
39.5
18.4
7.6
16.7
-
1.6
Fish scales
-
-
-
26.3
-
3.6
33.3
16.7
9.5
Other
-
-
-
2.6
-
0.4
-
-
-

112
(Table 6-5 and Fig. 6-2). Fins were the most important food item, accounting for 63.9%
of total food volume; scales were second in importance, 25.9% by volume. IL/SL ratio
(n = 8) ranged from 0.65 to 1.02 (mean = 0.87).
Pygocentrus caribe (Lutken 1874)
Although it was the most abundant piranha in many fish communities in the low
Llanos, Pygocentrus caribe was uncommon in samples from the upper Orinoco, and was
restricted to more lentic habitats such as abandoned river meanders and floodplain lakes.
Pygocentrus caribe (Fig. 6-1) is a robust, heavy-bodied species with broad and powerful
jaws; individuals reach about 300 mm SL. The body is silvery, and the cheek and venter
are often bright reddish orange, usually with a prominent black humeral spot. Based on
observations of P. caribe collected in other parts of Venezuela, the body and fins of large
adults in breeding condition turn almost black.
My samples showed that Pygocentrus caribe is primarily a piscivore. Examination
of stomach contents of 11 specimens (135-235 mm SL) from the upper Orinoco (Fig. 6-2)
indicated that fish flesh was the main prey in terms of frequency of occurrence, volume,
and dominance. Food items were as follows (%0-%D-%V): Group IV (n=3)-other
invertebrates (66.7-0-0.7), fish flesh (100.0-100.0-88.4), fish fins (66.7-0-8.3), fish
scales (66.7-0-2.7); Group V (n=8, 3 empty)-plant material (80.0-40.0-9.4), fish flesh
(80.0-60.0-71.8), fish fins (20.0-0-0.7), fish scales (20.0-0-15.5), other (20.0-0-2.7).
Plant material consisted of leaf fragments and woody material, which most likely was taken
incidental to attacking or ingesting other prey. No small juveniles of P. caribe were found
in the upper Orinoco. IL/SL was low, ranging from 0.7 to 1.4 for the 11 specimens
examined.

113
Table 6-5. Food items of Serrasalmus altuvei from drainages of the upper Orinoco River
basin, by size class. %0 = percent frequency of occurrence; %D percent dominance;
and %V = percent volume. N = 9.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
IV (80-159)
7
1
%D
%V
%0
V(>160)
2
1
%D
%v
Plant material
-
-
-
100.0
-
12.5
Aquatic insets
33.3
-
2.5
-
-
-
Other invertebrates
16.7
-
0.2
-
-
-
Fish flesh
50.0
33.3
7.0
-
-
-
Fish fins
66.7
50.0
63.1
100.0
100.0
75.0
Fish scales
66.7
16.7
27.0
100.0
-
12.5
Other
16.7
_
0.2
-
-
-

114
Pristobrycon striolatus (Steindachner 19081
Pristobrycon striolatus was rare in my samples from the upper Orinoco. It is a
medium-sized piranha found in both the Llanos and in southern Venezuela. The body is
silvery, partly covered with very small black spots, and has black along the base of the
caudal fin. The cheek and breast are typically reddish orange. My upper Orinoco sample
consisted of five adult specimens (106-165 mm SL), all taken during low water, four from
Cao Jenita of the Ocamo River, and one from a lagoon of the Mavaca River. The
stomachs of all five adults were packed with unidentifiable crushed seeds (Fig. 6-2 and
Table 6-6), which accounted for 84% of total food volume. Other plant material included
small stems and flower fragments. EL/SL ratio of the five specimens ranged from 1.5 to
2.8.
In addition to the larger fish, I also examined 38 small Pristobrycon juveniles (<40
mm SL), tentatively identified as P. striolatus. Characteristic of the genus, they had a
preanal spine (Fink, personal communication), but lacked ectopterygoid teeth. All were
taken from a mat of aquatic vegetation near the shore of the Yureba River, a blackwater
tributary of the Ventuari. Those of 10 to 19 mm SL fed heavily on the larvae of aquatic
insects (7.2 insects per stomach), mostly small chironomids, trichopterans and
ephemeropterans (Fig. 6-3). Food items of these Group IP. striolatus (n = 16) were as
follows (%0-%D-%V): microcrustaceans (18.8-0-1.7), aquatic insects (93.8-93.8-90.0),
and fish fins (12.5-6.3-8.3). Stomachs of fish 20-39 mm SL (n = 22, 2 empty) had fed
mostly on fins (55.3% by volume) and aquatic insects (44.3%) (Fig. 6-2). Aquatic insects
(3.1 per stomach) identified from stomachs comprised chironomids, ephemeropterans, and
coleopteran larvae and pupae. Mean IL/SL for small juveniles was less than 1.0.
Pristobrycon sp.
Pristobrycon sp. is a rare species. My sample consisted of only five adult fish
(182-245 mm SL) all taken in November during high water from flooded forest along Cao

Table 6-6. Food items of Pristobrycon striolatiis from the upper Orinoco River basin by size class. %0 = percent frequency of
occurrence; %D = percent dominance; and %V = percent volume. N = 43.
Size class (mm, SL)
Number examined
Number empty
Food items
1(19-20)
16
0
%0 %D %V
II (20-39)
22
2
%Q %D %V
IV (80-159)
4
0
%0 %D %V
%o
V(>160)
1
0
%D
%v
Masticated seeds
-
-
-
-
-
-
75.0
60.0
71.8
100.0
100.0
95.0
Plant material
-
-
-
-
-
-
50.0
20.0
5.7
100.0
-
4.5
Microcrustaceans
18.8
-
1.7
-
-
-
-
-
-
-
-
-
Aquatic insects
93.8
93.8
90.0
50.0
50.0
44.3
-
-
-
-
-
-
Other invertebrates
-
-
-
5.0
-
0.4
25.0
-
2.9
-
-
-
Fish flesh
-
-
-
-
-
-
25.0
20.0
12.0
-
-
-
Fish fins
12.5
6.3
8.3
50.0
50.0
55.3
50.0
-
6.7
-
-
-
Fish scales
-
-
-
-
-
-
-
-
-
100.0
-
0.5
Other
_
-
-
-
-
-
25.0
-
1.0
-
-
-

li
Chimita, Atacavi River, with gill net and handlines. The only other specimen known is that
of a single fish taken from a tributary of the blackwater Pasimoni River in the upper Rio
Negro drainage of Venezuela (W. Fink, personal communication). The species is currently
being described as new by W. Fink and A. Machado-Allison, and the five fish reponed on
here will be part of the type series. Pristobrycon sp. is a medium to large-sized piranha
with a rounded snout and a fairly robust body that is covered with irregularly-shaped black
markings (Fig. 6-1). It is known locally as "caribe colorado" (a name sometimes applied to
Pygocentrus caribe) because of the bright red-orange color that marks most of the lower
body and the lower fins. Intensity of body coloration is probably related to breeding
condition. Three of the specimens were females, of which one had the gonads almost
completely developed indicating that spawning takes place near the end of the rainy season.
Curipaco Indians collect adults in the flooded forest by pole fishing using small hooks
baited with earthworms; they maintain that the young of Pristobrycon sp. move from the
flooded forests into streams during low water where they are easily caught with nets or
killed with fish poisons derived from plants (barbasco).
Pristobrycon sp. is a seed predator (Fig. 6-2); stomachs of all five specimens were
packed with unidentified crushed seeds, mostly endocarp plus some exocarp and
mesocarp. Food items were as follows (%0-%D-%V; all Group V); masticated seeds
(100.0-100.0-96.4), plant material (leaf fragment of a palm) (20.0-0-0.4), other
invertebrates (winged insects and fragments of a spider) (60.0-0-1.4), and fish scales (20-
0-1.8). Intestines were very long for piranhas, ranging from 630 to 800 mm; IL/SL ranged
from 2.7 to 4 for the five specimens examined.
Pvgopristis denticulams Muller and Troschel 1845
Pygopristis denticulams (Fig. 6-1) was uncommon in my samples. I collected only
one adult (175 mm SL) from the upper Orinoco, taken from Cao Cuchakn of the
blackwater Atabapo River. I also preserved 80 small juvenile P. denticulatus (15-37 mm

117
SL) taken from a shallow, blackwater oxbow lake covering several hectares in the forested
floodplain of the Mavaca River; several additional fish were transported alive for later
observation. The species is the only representative of the genus Pygopristis, and closely
resembles Pristobrycon striolatus in both body form and markings. Pygopristis
denticulatus is the only piranha with five cusps (pentacuspid) on the jaw teeth, whereas
adults of all other piranhas have only three (tricuspid) (Machado-Allison 1985). The body
is deep, the snout is somewhat rounded, and the jaws are relatively small compared with
that of S. rhombeus. The body is typically silvery and sometimes dark, and parts of the
cheek and breast, as well as most fins, are red-orange. Juveniles are silvery, and parts of
unpaired fins are reddish orange. From about 25 mm SL, the sides are marked by a series
of about ten brownish, vertical bars, narrow and somewhat irregularly shaped; the bars
become faint with age. Unpaired fins are marked with a thin, blue-white terminal border.
Results of stomach content analysis are given in Figure 6-2 and Table 6-7. The
stomach of the single adult examined was full of masticate,! seeds (96.8% by volume)
along with a few fish scales (1.6%) and the remains of two small invertebrate larvae
(1.6%) (Fig. 6-2). L/SL was 1.9. I examined the stomach contents of 24 of the 80
preserved juveniles (Table 6-7). Both Group I (Fig. 6-3) and II (Fig. 6-2) had fed heavily
on aquatic insects, mostly chironomid and ephemeropteran larvae, and odonata nymphs.
Upon reaching a SL of about 40 mm SL a single juvenile that had survived in an aquarium
began stalking and chasing other fishes and clipping out pieces of fins.
Other Serrasaimine Fishes
In addition to piranhas, there are several other genera of the subfamily
Serrasalminae that occur in the upper Orinoco basin. Catoprion, a monotypic genus, is a
fin eater widely distributed in South America. All other genera of serrasaimine fishes, a
group in dire need of taxonomic revision, are primarily herbivores and all have relatively

Table 6-7. Food items of Pygopristis denticulatus from the upper Orinoco River basin by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %V = percent volume. N = 25.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
1(10-19)
4
0
%D
%v
%o
II (20-39)
20
0
%D
%V
%0
V (>160)
1
0
%D
%v
Masticated seeds
-
-
-
-
-
-
100.0
100.0
96.8
Plant material
-
-
-
20.0
-
1.7
-
-
-
Microcrustaceans
100.0
-
15.2
5.0
5.0
3.7
-
-
-
Aquatic insects
100.0
100.0
84.8
95.0
95.0
94.1
-
-
-
Other invertebrates
-
-
-
5.0
-
0.7
100.0
-
1.6
Fish scales
-
-
-
-
-
-
100.0
-
1.6
Other
-
-
-
5.0
-
<0.1
-
-
-

119
long intestines. The diets of several of the more commonly encountered species are
presented in Figure 6-4.
Catoprion ment (Cuvier 18191 Although locally abundant in parts of the low
Llanos, C. ment was uncommon in my samples from southern Venezuela, where it was
limited to lentic, back-water areas. It is a small species; those taken in the upper Orinoco,
all over 90 mm SL, were some of the largest I saw in all of Venezuela. The body is
silvery, cheek usually marked with reddish orange. Both males and females may have long
filaments extending from the first rays of dorsal fin. The seven large adults examined (99
to 128 mm SL) contained mostly fish scales (81.7% by volume) and a small amount of
plant material (10.4%) (pieces of leaves, and some filamentous algae), and aquatic insects
(8.0%) (Fig. 6-4). IL/SL ratio (n=7) ranged from 0.7 to 0.9.
Myleus species. The genus Myleus is represented by several species of deep
bodied, laterally compressed fishes. Jaw teeth are essentially molariform, with high cusps
that are adapted for cutting and possibly crushing plant material. The sexes exhibit striking
differences in body color and fin morphology; the males sometimes develop bright colors
and long fin filaments that are most pronounced during the breeding season. Three species
of Myleus were common in my samples from the upper Orinoco, Myleus asteias, M.
schomburgkii, and M. torquatus.
Myleus asterias was the most common species of this genus encountered. My
largest specimen was 185 mm SL, although maximum size may be much larger. It is a
silvery fish, with the bodies of males often spotted with variable hues of purple and
yellow. The anal fin of the male consists of two lobes with very small hooks present
during the breeding season. In contrast, the anal fin of females forms single a long lobe.
Most of the 37 specimens examined (98-185 mm SL) contained leaves that had been
clipped or sliced into small fragments (Fig. 6-4). Food items were as follows (%0-%D-
%V): Group IV (n=31, 2 empty)-masticated seeds (24.1-12.1-10.9), leaves/flowers

Fig. 6-4. Diets by size class (>80 mm SL) of four serrasalmine species from the upper Orinoco River basin:
Catoprion ment, Myleus asterias, M. schomburgkii, and M. torquatus. Size of segments represents
percentage of volume of each prey type; n = number of stomachs examined; numbers in parentheses
represent diet breadth using formula of Levins (1968).

S.L. (mm) MYLEUS
ASTERIAS
MYLEUS
SCHOMBURGKII
MYLEUS
TORQUATUS
CATOPRION
MENTO
80-159
>160
n=6 (1.04)
n=3 (1.08)
n=20 (2.24)
Masticated Seeds
\ \ N '
/ / /
S \ S '
/ *
\ \ \ '
Aquatic Insects
Fish Fins
Leaves/Flowers
Other Invertebrates
Fish Scales
Other Plant Material
Fish Flesh
Other ^

122
(93.1-74.1-84.4), other plant material (24.1-13.8-4.6), fish scales (3.4-0-0.1); Group V
(n=6)-masticated seeds (16.7-0-2.2), leaves/flowers (100.0-100.0-97.8). Several of the
flowers could be identified: one stomach was packed with small whole flowers of a
Machaerium sp. (Papilionaceae), and a second contained flower fragments of a
Campsiandra sp. (Caesalpiniaceae). Four fish collected in an abandoned meander of the
Putaco River with dense aquatic vegetation had fed on flowers and leaves of the water
lettuce Pistia stranotes (Araceae).
Myleus torquatus was taken along the main channels of rivers and streams, but not
in backwater areas. It is a medium-sized fish. The body coloration is silver, and there is a
black border on the caudal fin that may vary widely in intensity. A few males had long
dark filaments extending from the dorsal-fin rays. My examination of the stomachs of 24
individuals (109-192 mm SL) (Fig. 6-4) indicated that the species is highly opportunistic in
its feeding behavior. Many stomachs contained either crushed seeds or well-digested fruit;
one was full of cooked white rice (having fed on our discarded camp food); the stomachs
of several specimens were packed with large scales. Because scales of serrasalmine fishes
are small, scale eating was not the result of intraspecific aggression. Unlike other members
of the genus examined, Myleus torquatus has a unique "overbite", the upper jaw extending
past the lower jaw, causing several of the upper teeth to be exposed. Other scale-eating
fish are known to ram their victims and use their projecting teeth to dislodge scales
(Sazima and Machado 1982, Sazima 1983); the exposed teeth of M. torquatus could be
used for the same purpose. Food items were as follows (%0-%D-%V): Group IV (n=4, 2
empty) plant material (50.0-50.0-21.1), fish fins (50.0-0-5.3), fish scales (50.0-50.0-
73.7); Group V (n=20, 2 empty) masticated seeds (77.8-61.1-50.4), leaves/flowers
(27.8-27.8-43.6), other plant material (5.6-5.6-1.0), other invertebrates (11.0-0-0.2), fish
flesh (5.6-0-0.2), fish scales (22.2-0-3.9), and other (5.6-5.6-0.7). IL/SL ranged from
2.6 to 3.2.

123
Myleus schomburgkii. M. schomburgkii, possibly a species complex (Machado-
Allison, personal communication), is fairly common and widespread in the upper Orinoco,
and is also found in the Capanaparo and Cinaruco rivers of the Llanos. Maximum size is
over 300 mm SL. Myleus schomburgkii is silvery, with a single large black marking that
runs vertically on each side of the body that gives the appearance of having been stroked
with a paint brush. In breeding males the dorsal fin develops many long black filaments,
and large parts of the body may be covered with various combinations of bright reddish
orange, dark red, and black. I examined the stomachs of nine specimens (87-310 mm SL)
(Fig. 6-4). Common food items included seeds (masticated), filamentous algae, and
fragments of leaves of a bryophyte. IL/SL ranged from 2.3 to 3.8. Seeds were also the
most important food item in eight M. schomburgkii collected in the Llanos during the dry
season.
Summary of Upper Orinoco Trophic Patterns
Table 6-8 presents a matrix giving the diet overlap values, calculated by size class
for eight piranhas and four related species from the upper Orinoco River basin. Cluster
analysis of the Table 6-8 data produced six major trophic groupings or feeding guilds (Fig.
6-5): general piscivore, aquatic insectivore, scale-eater, fin-eater, seed-predator, and
folivore. Cluster I includes the general piscivores, predators that bit out chunks of flesh
from other fishes or ate small fish whole; this guild consisted of three species in the three
larger size classes (>40 mm SL). Cluster II were fin eaters and consisted of four piranha
species and four different size classes. Cluster IE, the seed-predator guild, consisted of
fish that fed mostly on seeds, which they bit into small fragments before ingesting. Seed-
predators were represented by six species in the two larger size classes. Cluster IV were
scale-eaters, represented by two species. Cluster IV were folivores, fish that fed on leaves
and flowers, usually by clipping them into small fragments; this group was limited to two

Table 6-8. Matrix of diet overlaps among different size classes of serrasalmine fishes from upper Orinoco River drainages. Overlap
index is that of Schoener (1970). (SL = Standard Length, see Table 3-1 for species abbreviations).
Species and
Size Range (SL, mm)
SR
40-79
SR
80-159
SR
>160
SM
40-79
SM
80-159
SM
>160
SEG
40-79
SEG
80-159
SEG
>160
PC
80-159
PC
>160
PST
80-159
PST
>160
PSP
>160
PYP
>160
SR 40-79
100
69.75
50.05
88.16
84.05
69.95
20
19.2
14.05
88.25
72.45
18.65
0
0
0
SR 80-159
100
59
80.79
59.91
57.8
31
25.15
22.6
61.4
64.1
25.2
4.95
3.55
3.05
SR >160
100
53.09
52.6
54.5
3.8
20.35
17
53.4
54.5
19.3
2.35
2.85
2.25
SM 40-79
100
74.51
72.79
28.7
21.34
14.09
77.19
71.19
21.71
1.54
1.24
0.84
SM 80-159
100
84.1
4.1
17.66
14.1
86.5
81.8
22.8
4.55
1.45
1.05
SM >160
100
1.4
25.25
23.7
70.9
79.9
30.8
14.35
11.45
11.05
SEG 40-79
100
7.6
1.6
8.3
0.7
6.7
0
0
0
SEG 80-159
100
91.25
22.55
17.15
92.45
75.8
77.7
77.1
SEG >160
100
16.7
22.6
85.4
76.95
78.25
78.05
PC 80-159
100
75.1
19.3
0.5
2.45
2.25
PC >160
100
19.3
4.95
2.15
1.55
PST 80-159
100
76.25
73.55
73.35
PST >160
100
95.9
95.5
PSP >160
100
99.4
PYP >160
100

Table 6-8continued.
Species and
Size Range (SL, mm)
SA
80-159
SA
>160
MYA
80-159
MYA
>160
MYS
80-159
MYS
>160
MYT
80-159
MYT
>160
CM
80-159
SM
10-19
SM
20-39
PST
10-19
PST
20-39
PYP
10-19
PYP
20-39
SR 40-79
27
20
0
0
0
0
5.3
0.2
0
0
20
20
20
0
0
SR 80-159
47.45
44.65
5.15
5.05
5.6
6.45
18.95
9.35
14.3
0.7
31
8.95
32.05
0.7
2.9
SR >160
14.15
8.65
1.95
1.85
4.4
8.05
8.65
5.95
4.8
0
3.8
3.75
7.1
0
2.3
SM 40-79
36.14
30.24
1.54
1.46
2.31
2.34
6.84
2.64
1.49
0
28.7
8.3
29.06
0
2.1
SM 80-159
11.26
16.55
12.65
13.15
13.11
7.05
17.15
13.55
10.31
0.01
4.1
4.06
4.46
0
2.3
SM >160
9.15
14.25
24.75
17.35
16.2
19.85
16.85
26.05
10.7
0
1.4
1.45
1.85
0
2.4
SEG 40-79
63.1
75
0
0
0
0
5.3
0
0
0
100
8.3
55.3
0
0
SEG 80-159
19
12.1
11.9
3.1
1.75
49.2
9.8
55.7
4.85
0.4
7.6
8.3
22.1
0.4
1.9
SEG >160
18.15
11.15
11.05
2.25
0
47.25
11.15
54.55
9.5
0
1.6
1.4
1.4
0
0
PC 80-159
18.15
10.95
0.1
0
0
0.95
7.95
3.05
2.6
0
8.3
8.3
8.7
0
0.5
PC >160
23.35
22.55
9.45
9.35
11.9
6.25
25.55
14.15
24.8
0
0.7
0.7
0.7
0
1.6
PST 80-159
14
12.35
16.55
7.85
6.7
53.65
10.95
57.15
5.6
0
6.7
6.7
7.1
0
2.3
PST ¡>160
0.5
5
15.5
6.7
4.55
51.7
5
55.4
4.95
0
0
0
0
0
1.6
PSP >160
2
2.2
11.4
2.6
0.45
48.7
2.2
52.8
2.15
0
0
0
0.4
0
1.0
PYP >160
1.8
1.6
11
2.2
0
48.3
1.6
52.2
1.6
0
0
0
0.4
0
0.6

Table 6-8continued.
Species and
Size Range (SL, mm)
SA
80-159
SA
160
MYA
80-159
MYA
>160
MYS
80-159
MYS
>160
MYT
80-159
MYT
>160
CM
80-159
SM
10-19
SM
20-39
PST
10-19
PST
20-39
PYP
10-19
PYP
20-39
SA 80-159
100
75.6
0.1
0
0.75
0.5
32.3
4.5
29.45
2.5
63.1
10.8
58
2.5
2.6
SA >160
100
12.6
12.5
12.55
6.3
30.3
16.4
22.85
0
75
8.3
55.3
0
1.6
MY A 80-159
100
91.2
89.05
17
21.1
55.6
10.45
0
0
0
0
0
1.6
MYA >160
100
96.95
8.2
21
46.8
10.35
0
0
0
0
0
1.6
MYS 80-159
100
6.05
21.05
45.35
10.9
0.55
0
0.55
0.55
0.6
2.2
MYS >160
100
6.3
53.4
6.25
0
0
0
0.4
0
2.3
MYT 80-159
100
24.9
84.05
0
5.3
5.3
5.3
0
1.6
MYT >160
100
14.25
0
0
0
0.2
0
1.8
CM 80-159
100
8
0
7.95
7.95
8.0
9.5
SM 10-19
100
0
90
44.3
84.8
94.0
SM 20-39
100
8.3
55.3
0
0
PST 10-19
100
52.6
86.5
91.6
PST 20-39
100
44.3
44.6
PYP 10-19
100
88.4
PYP 20-39
100

Fig. 6-5. Dendrogram from cluster analysis depicting similarities among diets of piranhas
and related species (by size class) from the upper Orinoco River basin,
Venezuela. Similarity values are from Table 6-7, dendrogram UPGMA-
generated using overlap index of Schoener (1970) and eleven resource
categories. See Table 3-1 for species abbreviations.

128
O 25 50 75 100
i \ 1 i
SR 40-79
PC 80-159
SM 80-159
SM £160
PC 2160
SR 80-159
SM 40-79
SR 2160 -
SEG 40-79*
SM 20-39
SA 80-159 -
SA2160
PST 20-39 -
SEG 80-159*
PST 80-159
SEG 2160
PST 2160
PSP2160
PYP2160
MYT2160
MYS2160 -
MYA 80-159
MYA2160 -
MYS 80-159_
MYT 80-159*1
CM 80-159 J
SM 10-19 -
PYP 20-39
PST 20-39
PYP 10-19.
General
Piscivores
Fin Eaters
Seed
Predators
Leaf
Eaters
Scale
Eaters
Insect ivores
0 25 50 75 100
Percent diet similarity

129
of the three Myleus species. Cluster VI was comprised of insectivores and consisted of
small juvenile piranhas that fed on the larva of small aquatic insects.
Of the six different feeding guilds recognized for serrasalmine fishes from the upper
Orinoco, piranhas were represented in four. None of the piranhas was considered to be
leaf-eaters or scale-eaters. My results indicate that most piranhas eat scales on occasion,
but none did so consistently, or to any great degree. Only in the non-piranha
serrasalmines, Catoprion memo and Myleus torquatus (80-159 mm SL), did scales make
up a high proportion of total diet volume. Adults of a few Orinoco piranhas were
considered to be truly herbivorous, and these fed mostly on seeds. Nevertheless, most
species exhibit some flexibility in feeding behavior, species considered to be primarily
herbivorous occasionally took animal prey, and the more carnivorous species sometimes
fed on plant material in bulk. In contrast to seed-eating piranhas, other primarily
herbivorous serrasalmine fishes exploited a more varied plant diet, frequently feeding on
leaves and flowers, in adddition to seeds and fruits.
Diet width measures diversity and evenness of resource use. Diet breadth usually
changed with age (Fig. 6-6), but there was no consistent pattern among species. The
lowest diet breadth values were found in both small and large size classes of piranhas.
Serrasalmus rhombeus >160 mm SL, Group V, had the highest diet breadth (i.e., 2.99).
In summary, of the eight piranha species found in the upper Orinoco River basin:
the adults of four species (Serrasalmus rhombeus, S. manueli, S. altuvei, and Pygocentrus
caribe) fed heavily on fish or fish fins: and adults of the other four piranha species
(Serrasalmus cf. eigenmanni, Pygopristis denticulatus, and two Pristobrycon species) were
basically seed predators, biting seeds into small fragments before ingesting them. Of the
three most abundant species in my samples (,Serrasalmus rhombeus. S. manueli, and S. cf.
eigenmanni), two were primarily piscivores, but S. manueli, though primarily a fish-eater,
occasionally took seeds or fruits in mass. All drainages in the upper Orinoco are heavily

130
"O
co
03
b
3 ~\
2-
1 ~
0
ill
s -y
pi
h4
i X
I:: -
:y*y
?:
1P
|p
rip
i
i
i
Si 7
lp
i
lp
i
10-19 mm

20-39 mm

40-79 mm
z
80-159 mm

>160 mm
S. rhombeus S. maiueli S. eigenmanni S. atuvei P. caribe P. strioiaus Prist, sp. P. denticulatus
Species
Fig. 6-6. Diet breadths estimated for eight piranha species, by size class, from the upper
Orinoco River basin, Venezuela. Diet breadth calculated using formula of
Levins (1968). Most species not represented in all size classes. Size ranges are
standard length (mm).

131
forested and I found evidence of herbivory (i.e., seed-eating) by piranhas in all six
drainages studied.
Data on diets of the smaller size class piranhas from the upper Orinoco is
incomplete. Stomach contents of five species (<80 mm SL), supplemented by my
observations on feeding behavior of wild-caught juveniles of Serrasalmus nianueli and
Pygopristis denticulatus kept in aquaria, suggest that most species in the upper Orinoco
pass through a growth stage, between 20 and 80 mm SL, when fin-eating is common or
even their predominant mode of feeding. Smaller juveniles (< 30 mm SL) taken in the
upper Orinoco had fed heavily on small aquatic insects; microcrustaceans only accounted
for a small part of their diets. Young piranhas rarely ate seeds or other plant matter.
Comparison with Savanna Populations
Much of my original data on the trophic patterns of savanna populations comes
from the low Llanos of the Apure River basin. As seen in the previous chapter,
information on the Cao Caicara area, an Apure River tributary, contrasted sharply with my
findings on adult piranhas from the upper Orinoco. Fish (flesh, fins, and small whole fish)
was the main component of adult diets of all seven species of piranhas from the Cao
Caicara region. I rarely found evidence of seed-eating by piranhas in the Cao Caicara
site. The few seeds eaten were very small and probably were taken incidentally along with
intended prey items. Of hundreds of specimens examined, not one stomach contained
many seeds. Other plant material, such as bits of leaves, grass blades, root wads, tiny
flowers, and filamentous algae, was ingested, but was of minor importance in terms of
dominance and volume. Pristobrycon striolatus was a seed predator in the upper Orinoco,
but none of the 16 P. striolatus from the Apure drainage had fed on seeds; however, most
specimens examined were juveniles that had fed heavily on fins. A 84-rrtm SL juvenile,
collected in Cao Maporal and kept in an aquarium, fed on small seeds and fish fins while

132
in captivity (Pygopristis denticulatus, another herbivorous piranha, is extremely rare in the
Apure River drainage and has not been taken in Cao Caicara).
Fin eating was also common among juveniles in the Llanos. In the Cao Caicara
area, the young of at least five of the seven piranha species present (i.e, Serrasalmus
rhombeus, S. elongatiis, S. irritans, S. medinai, and Pristobrycon striolatus) fed heavily
on fins. The smallest juveniles (10-19 mm SL) examined from the two regions are
compared in Figure 6-3. Small juvenile Pygocentrus caribe from the low Llanos fed on
small aquatic insects and microcrustaceans in roughly equal amounts (Fig. 6-3).
The Cinaruco and Capanaparo River Drainages
Long-term research in the Cao Caicara area suggested that savanna populations of
piranhas do not depend on plant material. However, my later study of fishes from savanna
areas where gallery forests are more extensive suggest that differences in trophic patterns
between the upper Orinoco and low Llanos are not always distinct. Although uncommon,
three of the four seed-eating piranhas found in the upper Orinoco (i.e., Pristobrycon
striolatus and Pygopristis denticulatus, Serrasalmus cf. eigenmanni) also occur in the
Cinaruco or Capanaparo river drainages of the low Llanos. Based on a limited number of
specimens taken during the dry season, stomach content analysis indicated adult piranhas
of the herbivorous species feed on plant material when available in savanna situations
(Fig.6-7). A description of their diets follows.
Pristobrycon striolatus was collected in both the Cinaruco and Capanaparo rivers.
Two juveniles (42 and 44 mm SL) contained mostly fish fins (80% of total volume); other
items included some plant material (leaf fragment and small stem) and a few scales. Larger
P. striolatus from these two rivers were seed predators (%0-%D-%V): Group IV (n = 8, 1
empty) masticated seeds (85.7-57.1-64.8), other invertebrates (28.6-0-2.0), fish fins
(28.6-0-5.4), fish scales (57.1-42.6-21.0), other (14.3-0-6.8).

Fig. 6-7. Diets by size class (>40 mm SL) of three piranha species from the Cinaruco and
Capanaparo river drainages of the low Llanos, Orinoco River basin, Venezuela.
Size of segments represents percentage of volume of each prey type; n = number
of stomachs examined; numbers in parentheses represent diet breadth using
formula of Levins (1968).

S.L. (mm)
40-79
80-159
>160
PYGOPRISTIS SERRASALMUS
DENTICULATUS cf. EIGENMANNI
PRISTOBRYCON
STRIOLATUS
n = 2
m
Masticated Seeds
Fish Flesh
i
:
Other Plant Material
Fish Fins
7 7
N N S
/ s
\ \ \
/ / !
Aquatic Insects
n
Fish Scales
1
Other Invertebrates
i
Other

135
I examined the stomach contents of 11 P. denticulatus (19-195 mm SL) taken from
the Capanaparo River drainage during low water (Fig. 6-7). Two small juveniles (19 and
28 mm SL) contained mostly microcrustaceans (ostracods, cladocerans, and copepods);
other food items included aquatic insect fragments (e.g., odonata nymph) and a few
diatoms. Masticated seeds were found in the stomachs of five of the eight specimens
greater than 40 mm SL; food items were as follows (%0-%D-%V): Group HI (n = 3) -
masticated seeds (100.0-66.7-95.0), and fish scales (66.7-33.3-5.0); Group IV (n=3)-
masticated seeds (66.7-66.7-55.0), aquatic insects (adult coleptera) (66.7-33.3-27.5),
fish flesh (33.3-0-17.2), and fish scales (33.3-0-0.3); Group V (n = 3) masticated seeds
(33.3-0-22.7), plant material (woody fiber and twigs) (66.7-33.3-22.7), aquatic insects
(adult coleptera) (66.7-0-6.8), fish scales (66.7-33.3-36.4), and other (soil) (33.3-33.3-
11.4).
Serrasalmus cf. eigenmanni occurs in the Cinaruco River of the Llanos. It appears
to be scarce, however, and I only examined three specimens (155-198 mm SL) (Fig. 6-7).
Two stomachs contained small amounts of leaf fragments. Other items included a few
large fish scales and some fish flesh.
Spatial Variation: Herbivorv versus Carnivory
Based on floristic differences between the two regions, I predicted that populations
in the upper Orinoco would be more herbivorous than their savanna counterparts. Table 6-
9 compares the incidence of herbivory among all piranhas (specimens >80 mm SL) from
the upper Orinoco to those from the low Llanos. With the exception of Serrasalmus
manueli, the proportion of piranhas containing plant matter was not significantly different
between the two regions. However, comparisons combining all species, and combining all
members of the genus Serrasalmus were significant in chi-square tests (Table 6-.9).

136
Table 6-9. Incidence of herbivory in piranhas (> 80 mm SL) as associated with the low
Llanos and upper Orinoco.
Taxon
Low Llanos
Upper Orinoco
# With
# Without
# With
# Without
Pristobrycon sp.
5
0
Pristobrycon striolatus
8
2
5
0
s
II
O
4^
Pygocentrus caribe
88
170
4
4
f (X2 = 0.31)
Pygopristis denticulatus
4
2
1
0
t (P = 0.71)
Serrasalmus alluvei
2
5
2
7
t (P = 0.61)
S. cf. eigenmanni
2
1
36
8
t (X2 = 0)
S. manueli
2
22
16
21
** (X2 = 6.93)
S. rhombeus
4
12
9
49
f (X2 = 0.26)
S. elongatus
8
17
S. irritans
13
57
S. medinai
13
37
All Serrasalmus
44
151
63
85
** (X2 = 14.77)
All piranhas
144
325
78
89
** (X2 = 13.18)
* P < 0.05, ** P < 0.01, t not significant
Note: Analysis was limited to individuals > 80 mm SL; each specimen containing food
in its stomach was considered a sample point and scored as to whether or not it contained
any plant matter. To test that upper Orinoco populations were more herbivorous than their
counterparts from the low Llanos, a 2 x 2 contingency table X2 test (one tailed, X2 value
given) was used where appropriate; if N < 40 then a Fisher exact probability test (one
tailed, P value given) was applied.

137
Many piranhas feed on small amounts of plant material, therefore using frequency
of occurrence as a measure of herbivory tends to over-emphasize the importance of small
plant items that in reality may not contribute much to the overall diet To overcome this
possible bias. Figure 6-8 summarizes the diet data in terms of the degree of herbivory using
three different diet measures including percent adjusted volume (%Va), percent dominance
(%D), and percent frequency of occurrence (%0) (for explanation of determination see
Chapter 3). Based on the data given in Figure 6-8, one-tailed Mann-Whitney U-tests were
used to determine whether forest piranhas (> 80 mm SL), as a group, were more
herbivorous than their savanna counterparts (Table 6-10). In each case (i.e., using %Va,
%D, and %0) the resulting probability (P) values fell between 0.07 and 0.05. As
previously mentioned, seven of the eleven piranha species were found in both the Llanos
and the upper Orinoco. In five of these seven wide-ranging piranha species, plant material
(in terms of %Va, %D, and %0) was greater in upper Orinoco populations than those from
the Llanos (Fig. 6-8). Four species (including three herbivorous species) showed fairly
substantial differences between regions. Serrasalmus rhonibeiis was the only species in
which samples from forest populations contained less plant food than those from savanna
sites.
Although primarily a carnivore, Serrasalmus manueli was one of the few Orinoco
species that was relatively common in both the low Llanos (i.e., Capanaparo River
drainage) and the upper Orinoco (e.g., Sipapo and Atabapo rivers) and also fed to some
extent on seeds. Figure 6-9 summarizes and compares diets of S. manueli Llanos
populations with samples from the upper Orinoco. Considering only individuals > 80 mm
SL having food in their stomachs, two of 24 S. manueli examined from the Llanos
contained plant material whereas 16 of 37 individuals taken in the upper Orinoco contained
seeds or other plant remains. The two Llanos S. manueli containing plant material in their
stomach were larger than 160 mm SL.

Fig. 6-8. Comparison of the proportion of plant material in the diets of carnivorous and
herbivorous piranha species (> 80 mm SL) from the low Llanos to those from
upper Orinoco River drainages in terms of percent adjusted volume (%Va),
percent dominance (%D), and percent frequency of occurrence (%0).
Carnivorous species abbreviations are: Pc = Pygocentrus caribe; Sa =
Serrasalmus altuvev. Sel = S. elongatus; Sir = S. irritans; Sm = S. manueli: Smd
= S. medinai; and Sr = S. rhombeus. Herbivorous species abbreviations are:
Pst = Pristobrycon striolatus; Psp = Pristobrycon sp.; Pyp = Pygopristis
denticulatus; and Seg = Serrasalmus cf. eigenmanni. Psp was found only in the
upper Orinoco; Sel, Sir, and Smd were found only in the Llanos.

139
CARNIVORES
HERBIVORES
40-
30-
%D 20'
10-
0-
Low Llanos Upper Orinoco

140
Table 6-10. One-tailed Marm-Whitney U-test results testing the prediction that piranha
species (> 80 mm SL) from upper Orinoco River drainages are more herbivorous than
those from the low Llanos. Diet measures are percent adjusted volume (%Va), percent
dominance (%D), and percent frequency of occurrence (%0) (see Chapter 3 methods for
explanation). Ni = number of piranha species from upper Orinoco; N2 = number of
piranha species from low Llanos. See Table 6-9 for number of specimens examined for
each species.
Diet Measure
Ni
n2
u
Mean
SD*
z value*
P
%va
8
10
23
40
11.22556
- 1.514402
0.0655
%D
8
10
22.5
40
11.21973
- 1.559752
0.0594
%0
8
10
23
40
11.21556
- 1.514402
0.0655
* Corrected for ties

Fig. 6-9. Diets by size class (>40 mm SL) of Serrasalmus manueli comparing Llanos
(Cinaruco River drainage) and upper Orinoco populations. Size of segments
represents percentage of volume of each prey type; n = number of stomachs
examined; numbers in parentheses represent diet breadth using formula of Levins
(1968).

142
SERRASALMUS MANUELI
S.L. (mm)
40-79
80-159
>160
LLANOS
UPPER ORINOCO
o = 5 (3.90)
n = 22 (1.96)
n = 18(1.83)
n = 18 (1.45)
n = 42 (1.99)
Masticated Seeds
Other Plant Material
Decapoda
Aquatic Insects
Other Invertebrates
Small Whole Fish
Fish Flesh
Fish Fins
Fish Scales
Other

143
Ecomorphological Correlates: Intestine Length and Diet
In general, intestine length (IL) was positively correlated with standard length (SL),
that is, the IL/SL ratio typically increased with greater body size, or age, in most species.
Small juvenile piranhas tended to have fairly low IL/SL, usually less than 1.0. To reduce
the effect on variability due to body size the following comparisons were limited to larger
specimens, those >80 mm SL. Relative intestine length (IL/SL) among the serrasalmine
fishes (> 80 mm SL) examined ranged from less than 1.0 to greater than 3.0. Differences
among species were correlated with adult diet (Fig. 6-10). The association between
intestine length and degree of herbivory among species (> 80 mm SL) was significant
(Spearman rank correlation, rs = 0.79, P < .001, n = 35; Fig. 6-11); carnivorous species
have a short intestine (<1.5 IL/SL) and all herbivorous species have a relatively long
intestine (usually >1.5). In a few cases data seemed to indicate differences in IL/SL
between populations of the same species, but such variation was usually associated with
small sample size or body size effects.
Large sample sizes for the three most common piranhas in the upper Orinoco (i.e.,
(,Serrasalmiis rhombeus, S. manueli, and S. cf.eigenmanni) permitted a more detailed
analysis of IL, SL, and diet relationships (Fig. 6-11). Serrasalmus cf. eigenmanni, a
species that fed heavily on seeds, had the longest relative IL; its IL/SL ratio was
significantly greater than that of the other two species (ANCOVA; F = 21.44 and 26.09,
P = 0.0001). Serrasalmus rhombeus, the most carnivorous of the three, had the relatively
shortest intestine, whereas S. manueli had an intermediate intestine length. The latter
species occasionally takes seeds or fruit in large quantity. Although slopes of the IL/SL
regression lines did not differ between S. rhombeus and S. manueli (F = 3.24, P =
0.0741), the IL of the two species differed after adjusting for differences in SL (F = 33.89,
P = 0.0001); S. rhombeus had a shorter intestine, as expected from its diet. My data show
that adult S. manueli from the upper Orinoco fed more on plant material than conspecific

144
savanna populations (Table 6-10, Figs. 6-8 and 6-9). However, in examining possible
geographic variation in the EL/SL of S. manueli, I found no significant difference in the
slopes of the EL and SL regression lines (F = 0.67, P = 0.4157) between forest and
savanna populations (Fig. 6-12).

145
O)
c
0)
-D
CC
~o
c
ce
-i '
en
O)
c
a>
0)
c
c
ce
(D
3-
1 -
0
Pst
'Mys
Seg
PsP0
My O
Mys o
Mag Md H
Mya
O O
Pst Pyp
Smss
SrO
Smd _
SaC
a Pn
Sir Sr
o.Jkk "
' Pn
Sel
Ocm
Osm
'Cm
1 Pyp
Standard length >80 mm
o Upper Orinoco
B Llanos
r i i i i 1 i i 1 i i 1 i
0 10 20 30 40 50 60 70 80
% Volume plant material in diet
90 100
Fig. 6-10. Scatter diagram showing relationship between mean intestine length/standard
length (not adjusted for SL) and percent volume of plant material in diet for
selected serrasalmine fish (>80 mm SL). Piranha species: Pyp = Pygopristis
denticulatus', Sa = Serrasalmus altuvei; Seg = S. cf. dgenmannv, Sel = S.
elongatus; Sir = S. irritans: Sm S. manueli; Smd = S. medinai; Sr = S.
rhombeus', others: Cm Catoprion ment-, Mag = Metynnis argenteiis\
Mya = Myleus asterias-, Mys = M. schomburgki; Myt = M. torquatus; and
Md = Mylossoma duriventris.

Fig. 6-11. Scatter diagram showing relationship between intestine length (IL) and standard
length (SL) for the three most common piranhas in samples from the upper
Orinoco River basin of Venezuela. Regression lines are as follows: S. manueli
IL = -64.09 + 1.86SL (r2 = 0.908, n = 60), S. rhombeus IL = -76.07 +
1.66SL (r2 = 0.857, n = 70), S. cf. eigenmanni EL = -137.88 + 3.44SL (r2 =
0.733, n = 32). Lines fitted by the above linear regression equations, r =
Pearson correlation coefficient. See Appendix B for ANCOVA analyses.
Fig. 6-12. Scatter diagram showing relationship between intestine length (IL) and standard
length (SL) for Serrasalmus manueli comparing upper Orinoco and Llanos
populations. Regression lines are as follows: Upper Orinoco EL = -64.09 +
1.86SL (r2 = 0.908, n = 60), Llanos IL = -94.32 + 2.00SL (r2=0.864, n =
20). Line fitted by the above linear regression equation, r = Pearson
correlation coefficient See Appendix B for ANCOVA analyses.

Intestine length (mm) Intestine length (mm)
147

CHAPTER 7
ANALYSIS OF NUTRIENT VALUES OF PIRANHA PREY
Piranhas and their close relatives exploit a broad range of food resources, including
arthropods, fishes and other vertebrates, fish fins and scales, carrion, seeds, fruits, leaves,
and flowers (Goulding 1980, Sazima 1983, Sazima and Guimaraes 1987, Nico and
Taphorn 1988, Winemiller 1989a, Sazima and Machado 1990). These diverse food items
differ in terms of protein, lipid, carbohydrate and caloric content, offering piranhas a range
of foods that differ in nutrient quality and digestibility. The nutrient value of a particular
type of food item, along with its relative availability and digestibility, is an important factor
in food preference or selection.
My results from the chemical analysis of scales, fin.->, and small whole fish are
given in Table 7-1 and Figure 7-1. I also present some information from the literature on
the energy contents and chemical components of other types of general food items, for
example insects and various types of plant material.
Animal Matter
Ssaks
Scale-eating, or lepidophagy, is known for several unrelated freshwater fishes of
South America (Roberts 1970, Sazima 1983). Many of the serrasalmine species that I
examined took scales in small quantities, but Catoprion ment was the only species in
which individuals of all sizes fed heavily on scales. The stomachs of several specimens of
My lens torquatus of size class IV were packed with scales, but the few specimens available
148

Table 7-1. Estimates of the lipid, protein, ash, carbohydrate, and caloric contents of fins, scales, and whole fish
for two taxa of typical piranha prey fish. Energy expressed as kJ/g of dry mass, all others given as percent of
dry mass. Where number of replicates exceeds one, values represent mean standard error with number of
replicates in parentheses.
kJ/g
(dry mass)
%
Protein
(dry mass)
%
Ash
(dry mass)
%
Lipids
(dry mass)
%
Carbohydrate
(dry mass)
Cichlidae
Whole fish
14.8 .0.01 (2)
50.7 0.05 (2)
33.3
7.01 0.02 (2)
0.1 0.03 (2)
Scales
9.0.0.01 (2)
43.5 0.05 (2)
48.7
1.1 0.18 (2)
5.7 1 0.00 (2)
Fins
9.2 .0.00.(2)
35.9 0.05 (2)
56.2
3.3 1 0.03 (2)
0.5 1 0.03 (2)
Curimatidae
Whole fish
14.9 .0.00.(2)
52.210.10 (2)
33.7
6.0 1 0.01 (2)
0.8 1 0.03 (2)
Scales
10.2 .0.00.(2)
44.2 0.38 (2)
48.3
0.7 1 0.01 (2)
6.3 1 0.03 (2)
Fins
10.9 .0.00.(2)
34.0 0.60 (2)
57.8
2.1 1 0.03 (2)
2.5 1 0.01 (2)
Combined
Whole fish
14.9 0.03 (4)
51.510.44 (4)
33.5 1 0.20 (2)
6.5 1 0.30 (4)
0.5 1 0.19 (4)
Scales
9.6 0.36 (4)
43.9 1 0.24 (4)
48.5 1 0.20 (2)
0.910.14 (4)
6.010.17 (4)
Fins
10.1 0.48 (4)
34.9 1 0.60 (4)
57.0 1 0.80 (2)
2.7 1 0.37 (4)
1.5 0.58 (4)

150
Prey items
Fig. 7-1. Bar graph comparing the dry mass composition of small whole fish, scales, and
fins. Energy expressed as kJ/g of dry mass, all others given as percent of dry
mass. Vertical bars represent 2 SE.

151
made it difficult to determine if such behavior is widespread. Scales eaten were all large,
thereby eliminating the possibility of intraspecific aggression since all Myleus species have
fairly small scales.
Scale-eating fishes probably have less difficulty in digesting scales than other fish
parts, for instance bone. Because I rarely found whole scales in the posterior parts of the
their intestine, it suggests that ingested scales are broken down into their component parts
in the foregut. Although scales are a common food item, there have been no published
reports on the nutrient value of scales of South American freshwater fishes. My results
from analysis of scales from cichlid and curimatid fishes generally agree with previous
findings (Table 7-1, Fig. 7-1). Whitfield and Blaber (1978) reported that scales from the
mugilid Mugil cephalus, a wide-ranging species of both marine and fresh waters, had a
caloric value of 8.5 kj/g. Scales that have been studied were found to contain 40-85%
protein (van Oosten 1957). The mucus that coats fish scales is rich in proteins (Wessler
and Wemer 1957) and lipids (Lewis 1970). In salmon, the protein content of the mucus is
62% of the dry weight (Harris and Hunt 1973). The mineral proportion, calcium
phosphate, of a teleost scale ranges from 16% to 59%, depending on species (Whitear
1986). Sazima (1983) thought that scale eaters must augment their diet with other kinds of
food. Goulding et al. (1988) found that 100 of 250 fish species from the Rio Negro fed on
scales, usually in small quantities, and they argued that occasional scale eating may act to
supplement diets for those fishes inhabiting rivers that are poor in calcium and
phosphorous (e.g., blackwater habitats).
Fins
Fin eating is common among piranhas and several other South American fishes.
Most fishes taken in the low Llanos are missing pieces of their caudal or dorsal fins during
both high and low water periods. On the other hand, my observations seem to indicate that
the incidence of fin eating is much less in the upper Orinoco (L. Nico, unpublished data).

152
There have been no previous studies of the nutrient content of fins as relates to fin-eating
fishes. My results show that the energy and protein content of fins and scales are very
similar, about 10 kj/g and approximately 34% protein (Table 7-1, Fig. 7-1). Like scales,
the fins of fishes are covered with protein-rich mucus; similar to scales they probably also
contain a significant amount of calcium phosphate.
Fish and Fish Flesh
Many adult piranhas prey heavily on fishes, either biting out chunks from larger
fishes, sometimes as carrion, or taking small fish whole or almost whole. Compared with
feeding only on fins or scales, the nutrient advantages of such behavior are obvious
because the predator gets a combination of fins, scales, and flesh. The energy, protein,
and lipid contents of entire small fish are higher than those of either fins or scales (Table 7-
1, Fig. 7-1). Smith (1981:90), citing Junk (1977), presented a list of the fat, protein, and
ash content of 21 medium and large-sized Amazonian food fishes from a floodplain lake at
low water. Protein (12.4 to 20.2%) and ash (1.0 to 5.2%) contents did not vary much;
however, fat content showed wide variation among species, ranging from 0.2 to 28.8%.
Fat contents also show seasonal differences since many species accumulate fat after feeding
during the high-water season (Smith 1981). My values for small prey fishes showed a
much higher protein content (51.5%) and ash content (33.5%) than Smith reported for
large fishes, with a fat content (6.5%) within the lower part of his reported range.
Arthropods
Insects and other invertebrates are some of the richer foods in terms of nutrient
value per mass. Bell (1990) reported that the dry mass composition of an average insect is
59.5% protein, 15.5% fat, 5.0% ash and 7.2% carbohydrate, and yields approximately 22
kJ/g dry mass through combustion. Ranges of 5.3 to 85.4% fat, and 12 to 29.7% kJ/g
were reported, with highest values often associated with larval forms (Cummins and

153
Wuycheck 1971, Davis and Warren 1971, Bell 1990). The lipid and energy content of
insects is much higher than that of other animal food items eaten by piranhas.
Microcrustaceans, similar to insects, also yield over 20 kJ/g of dry matter (Cummins and
Wuycheck 1971).
The small juveniles (usually <40 mm SL) of several piranhas were found to feed on
aquatic insects, mostly ephemeropterans and chironomid larvae. Pygocentrus caribe,
which feeds heavily on aquatic insects and some fish flesh when young, has a faster
growth rate than other piranhas, such as Serrasalmns irritans, which feed heavily on fins as
juveniles (Nico, unpublished data).
Plant Matter
There are, to my knowledge, no data available on the chemical composition of the
seeds, fruits, and leaves eaten by serrasalmine fishes. As a rule, plant matter tends to be
high in carbohydrates whereas animal matter is high in proteins. Nevertheless, nutrient and
energy content varies considerably among different plant species and different plant parts.
Plants typically accumulate nutrients and energy reserves in seeds and fruits. Seeds are
particularly rich in lipids in the form of oils. My study suggests that piranhas prefer seeds
and hard fruits over other plant parts (e.g., fleshy fruit, leaves, flowers). Goulding et al.
(1988) felt that herbivorous fishes prefer fruits and seeds to leaves because leaves are less
nutritious and frequently contain toxic compounds.
Okeyo (1989) compiled information on the composition of foods found in
alimentary tracts of a wide range of herbivorous fishes showing that aquatic plants vary
greatly in terms of ash, protein, lipid, carbohydrate, and energy content. Previous studies
investigating nutrient quality of plant matter as it relates to animal diets in the neotropics
have focused primarily on mammals and birds. Snow (1981) presented food values of
fruits from 20 tropical and subtropical plant species, reporting protein, fat, and

154
carbohydrate contents. Giving nutrient content values as a percentage of the dry mass
composition of the fruit pericarp, Snow reported ranges of 1.9 to 21.6% protein, 0.6 to
67.0 % fat, and 10.8 to 90.9% carbohydrate. Worthington (1989) found that the fleshy
parts of fruits eaten by manakins, a group of neotropical frugivorous birds, typically had
low nutrient concentrations. However, the energy content of fruit pulp ranged from 15 to
17 kJ/g of dry pulp. Similarly, Kerley and Erasmus (1991) reported a range of 17 to 20
kJ/g dry mass for seeds commonly eaten by African rodents.
In conclusion, because of their high sugar and oil content, the energy yield of seeds
and fruits is frequently higher than that of fish flesh. Nevertheless, herbivorous species
probably need to supplement their diets with animal matter. Sugars supply only calories
rather than essential nutrients (see Karasov and Diamond 1988). From his research on the
Gray's monitor lizard, Auffenberg (1988) concluded that fruits alone, being low in both
proteins and calcium, forces vegetarian reptiles to include other items such as land snails in
their diet.

CHAPTER 8
DISCUSSION AND CONCLUSIONS
In this work, I have attempted to describe the diets and trophic ecology of piranhas
from contrasting environments of the Orinoco River basin. The main questions addressed
in this study are: (1) Do the same species of piranhas occur in both savanna and forested
regions? (2) Do diets differ, and, if so, are fish from populations in forested habitats
significantly more herbivorous than their savanna counterparts? (3) How do ontogenetic
changes in diet compare among species and do they correlate with regional environments?
(4) Is intestinal length of piranhas and other serrasalmine fishes correlated with diet?
(5) What are the nutritional benefits associated with different diets or food preferences?
(6) How do diets of piranhas compare with those of other serrasalmine species? (7) What
is the relationship between piranha ecology and serrasalmine phylogeny? In this final
chapter, I briefly reexamine these questions in view of my results and I speculate on the
findings in relation to mechanistic, ecological, and evolutionary issues.
Composition of Piranha Assemblages
It it difficult to determine with certainty the precise effect ecological conditions have
had on current piranha abundance and distribution patterns. Gilbert (1980) considered both
historical and ecological elements as being equally important in interpreting the
geographical distributions of most freshwater fishes. Along these same lines. Burr and
Page (1986) suggested that similarities in fish faunal compositions among North American
streams were dependent upon several factors, for instance drainage size and proximity,
155

156
geological history, and the physical and biological characteristics of the individual
drainages. A combination of all these factors has probably helped to shape the distribution
patterns observed for Orinoco piranhas.
Several recent studies in different parts of the Orinoco River basin have examined
patterns of fish distribution and species composition. Based on long-term collecting, much
of it in the Apure River drainage. Taphorn (1990) felt that altitude (lowland versus
montane) and water type (i.e., clear and black versus white) were the two basic
environmental parameters governing fish species distribution. He found that many species
(47 of 103 characiform fishes) living in black waters seemed to be restricted to that type of
habitat, whereas relatively few species were limited to just white waters (15 of 77
characiform species). In a study of fish communities from 20 floodplain lakes in the lower
Orinoco, Rodriguez and Lewis (1990) found that differences in species composition
between lakes might be best explained in terms of variation in small-scale factors (e.g.,
water type, lake morphology, and vegetation), and that apparent differences among regions
might be averaged out and disappear if many sites (i.e., habitats) from each region were
included in a comparison. Chemoff et al. (1991) rejected both ecological segregation and
the possibility of sampling artifact and concluded that historical events, or vicariance, better
explained the seemingly disjunct distribution patterns seen with some Orinoco fish species.
I examined and compared piranha distribution patterns among regions and
drainages to reveal any associations existing between species composition and habitat. My
interest in habitat-dependent piranha distribution revolved around their relationship to
piranha trophic ecology. Although piranhas exhibit a fair amount of flexibility in what they
eat, my study documents the fact that Orinoco piranhas, in terms of adult diets,
nevertheless fall into two general categories: species that are largely carnivorous, and
others that axe primarily herbivorous (Table. 8-1). Given this apparent dichotomy in
feeding preferences, a close association between piranha distribution patterns and habitat
type might be predicted. Herbivorous species should.be much more common in the

157
forested upper Orinoco drainages where plant foods, especially fruits and seeds, are an
abundant and fairly reliable resource; and carnivorous species should predominate in the
grassland savannas of the low Llanos where fish biomass is high but plant food availability
extremely seasonal and therefore a less dependable resource.
Low Llanos versus Upper Orinoco
During this study, eleven piranha species were recorded from the two regions of the
Orinoco River basin: ten from the low Llanos, and eight from the upper Orinoco. Seven
species were found to inhabit both regions. Thus, even though the Llanos and upper
Orinoco have very different vegetation, they are very similar in their overall piranha species
composition. The high similarity in species make-up suggests that, in terms of piranhas,
there are really no distinct savanna versus forest species assemblages. These results at first
seem contrary to the already mentioned possibility that piranhas are distributed based on
their feeding preferences (i.e., carnivorous species in the Llanos and herbivores in the
upper Orinoco). However, a few exceptions to the prevailing species overlap should be
noted. Four of eleven species were limited to one or the other region: Pristobrycon species
is a seed-eating piranha known only from forested blackwater habitats of southern
Venezuela: and Orinoco Serrasalmus elongatus, S. irritans, and S. medinai, all highly
carnivorous, were taken only in the Llanos.
My findings on the relative abundance of species in the two regions suggested
patterns not evident from analysis of presence-absence data alone. Several species are
much more common in one region than the other. These differences were associated, in
part, with differences in food resources. For example, the seed-eating S. cf. eigenmanni
was rare in samples from the Llanos but common in several drainages in the upper Orinoco:
the carnivorous Pygocentrus caribe is abundant throughout much of the Llanos but
uncommon in the upper Orinoco. Overall, herbivorous species were only really common

158
Table 8-1. Orinoco River basin piranhas categorized by adult diet (L = Llanos; U = upper
Orinoco).
Largely Carnivorous
Largely Herbivorous
Pygocentrus caribe (L, U)
Serrasaimus altuvei (L, U)
Serrasalmus elongatus (L)
Serrasaimus ini tans (L)
Serrasalmus manueli (L, U)
Serrasaimus medinai (L)
Serrasalmus rhombeus (L, U)
Pygopristis denticulatus (L, U)
Serrasalmus cf. eigenmanni (L, U)
Pristobrycon striolatus (L, U)
Pristobrycon sp. (U)

159
the upper Orinoco. Carnivorous piranha species were abundant in both the upper Orinoco
and the low Llanos, but they were more common in the Llanos.
Ecological Considerations
There seems to be no single habitat parameter that will reliably predict the makeup
of piranha assemblages in given areas. Nevertheless, local ecological conditions are
probably more important than regional differences in determining species abundance and
local species composition. Various ecological factors, both physical (e.g., water
temperature, clarity, pH, stream gradient) and biological (e.g., vegetation, availability of
food, spawning requirements, symbiotic interactions with other organisms) can be
considered as potentially limiting numbers and kinds of piranhas. Some of these factors
have already been touched upon briefly in the preceding sections.
Most Orinoco piranha species, in addition to being widespread, are found in a
variety of lowland habitats (e.g., rivers, streams, floodplain lagoons and oxbow lakes)
over a wide range of environmental conditions (Table 4-4). If numbers of individuals can
be used as an indicator of habitat quality, then the preferred habitats of most species are
lentic white waters. Serrasalmus cf. eigenmanni is the most common herbivorous species
in the upper Orinoco, and it was found in both whitewater streams and cutoff meanders.
Carnivorous piranha species seem more able than herbivorous species to adapt to
perturbation. For example, several of the more carnivorous species occur in great numbers
in reservoirs: Serrasalmus rhombeus and Pygocentrus caribe in the Orinoco (personal
observations), 5. rhombeus, S. spilopleura, and P. nattereri in Brazil (Table 1-1). To my
knowledge, those species that I have categorized as largely herbivorous (Table 8-1) are
never found in reservoirs. Still, many species are apparently able to maintain smaller
populations in what might be described as less desirable habitats.
Several species are widely distributed but seem to be uncommon throughout their
ranges (e.g., Serrasalmus altuvei. Pristobrycon stiiolatus, Pygopristis denticulatus).

160
Serrasalmus altuvei has been found recently in the Rio Negro of the Amazon basin where,
as in the Orinoco, it is also considered quite rare (Jgu and Santos 1987, Jgu et al. 1991).
Explanations for the noted natural rarity of these species may be found, perhaps, in their
having more specific habitat requirements (see Gilbert 1980). Some of the more
uncommon species of piranhas seem to have somewhat specialized diets as adults, and a
narrow food preference might account for their low numbers. For example, adult S.
altuvei are basically fin eaters, and some of the other rare piranha species are mainly
herbivorous. (See later discussion of dietary specialization).
Species closely related to piranhas (e.g., Colossoma, Piaractus, Mylossoma) are
known to make long seasonal migrations of many hundreds of kilometers for purposes of
tracking food resources or for reproduction (Lowe-McConnell 1964, Goulding 1980). In
contrast, migratory movements by piranhas seem limited to lateral movements across the
floodplain and to short seasonal journeys between more permanent waters (large streams
and lagoons) and their floodplains. Field researchers have yet to observe piranhas
spawning in the wild or even identify precisely where eggs are deposited (but see Lowe-
McConnell 1964). In all likelihood, spawning sites are located in aquatic vegetation. My
unpublished data on the reproductive condition of adults and monthly differences in body
size indicate that spawning takes place mainly during the early part of the rainy season.
Small juvenile piranhas are always found in flooded vegetation and it has been shown that
they use macrophytes for both shelter from predators and as a foraging area (Menezes et al.
1981, Sazima and Zamprogno 1985, Nico and Taphom 1988, Nico 1990, this study). The
upper Orinoco has few habitats with large areas of aquatic macrophytes and this scarcity
may limit piranha numbers in that region.
In addition to regional differences, differences in species composition and
abundance among habitats within regions also seem to be associated, at least in part, with
differences in types and availability of food resources. Perhaps the clearest example is that
from the Llanos. Earlier work in the Cao Caicara area suggests that all Orinoco savanna

161
piranhas are basically carnivorous (Nico and Taphom 1988, Winemiller 1989a, see
Chapter 5). However, my later research of piranhas in other low Llanos drainages gave
evidence of seed eating by adults of two, and perhaps three, savanna species. The savanna
drainages studied (Apure, Cinaruco, and Capanaparo) are all located in the low Llanos of
Apure State; but study sites in the Cinaruco and Capanaparo drainages differed somewhat
from the Cao Caicara site of the Apure River drainage in having large gallery forests.
Similar to the flooded forests of the upper Orinoco, savanna regions having extensive
gallery forests provide a significant amount of edible plant material during high-water
periods when fishes are able to move across their floodplains; but plant foods are rarely
available to savanna fishes during the dry season when water levels have dropped. This
fact alone may explain why the more herbivorous piranha species are not very common in
savanna drainages. Admittedly, quantitative studies of availability of food resources across
a range of habitats are still required.
The possibility that South American fishes might segregate according to water type
is an attractive idea, only partly supported by recent field work (e.g., Taphom 1990,
Rodriguez and Lewis 1990). Nine of the 11 Orinoco piranha species studied were either
found in two or in all three major water types (Table 4-4). Nevertheless, as found by
Taphom (1990) in his study of Apure River fishes, blackwater habitats have a more unique
fish fauna than whitewater habitats due to a fairly high proportion of endemics or core
species. Even though few species are restricted to a particular water type, there do appear
to be consistent differences in relative abundance between water types for those species that
inhabit both black and white waters. Whereas most piranha species reach their greatest
numbers in whitewater habitats, several Orinoco species (i.e., Serrasalmus manueli,
Pygopristis denticulatiis, Pristobrycon sp.) are apparently restricted to, or much more
common in, black waters. In my study, cluster analysis of drainages based on species
composition also tended to group drainages that were similar in habitat (e.g., water type),
as well as by their geographic proximity.

162
Given the complex situation of various water types superimposed onto both
savanna and forested regions, excepdons to any generalizations can be found.
Nevertheless, although additional studies are needed, some general trends are apparent that
are obviously important in understanding the trophic ecology of serrasalmine fishes. On
average, it seems safe to assume that aquatic primary production is greater in the Llanos
than in the upper Orinoco (see Saunders and Lewis 1988), and is greater in white water
than in either blackwater or Clearwater situations (Fittkau et al. 1975, Saunders and Lewis
1988, Goulding et al. 1988). Of course, white waters are much more common in the
Llanos than in the upper Orinoco. Furthermore, my observations indicate that white waters
in the upper Orinoco are less turbid and correspondingly less productive than those of the
Llanos. In any case, South American fishes inhabiting highly productive waters feed more
on autochthonous foods (e.g., aquatic insects, fishes, and so on), whereas fishes
inhabiting nutrient-poor waters depend more on allochthonous material for food (e.g.,
fruits, seeds, leaves, and terrestrial and arboreal insects).
Historical Perspective
It is interesting to speculate as to what effects past climatic changes might have had
on the distribution and abundance of piranhas and other serrasalmine fishes. Herbivorous
serrasalmine fishes existed more than 15 million years ago during the Miocene, long before
the start of the Quaternary (Lundberg et al. 1986). As described in Chapter 2, the
equatorial lowland regions of South America experienced dryer and hotter climates during
major glaciations resulting in an expansion of savanna and open-land environments.
Because humid forests would have contracted in size, herbivorous serrasalmines would
either have had to adjust to changes in food, or been forced either to retreat to the remaining
forested regions or to maintain close ties to rivers with large gallery forests. On the other
hand, interglacial or pluvial periods were wetter and relatively cooler, contributing to the
expansion of humid forests, a situation clearly favoring herbivorous fishes.

163
Based on the fossil record and the proposed phylogenetic relationships among
serrasalmine fishes (Lundberg et al. 1986; Fig. 1-1), no less than a proto-piranha existed
before the start of the Pleistocene. If this "first piranha" entered the Quaternary unchanged,
subsequent radiation might have been in the form of adaptive responses to the dramatic
changes wrought by glacial events. In this scenario, herbivorous piranhas would have
evolved in forested areas and perhaps certain carnivorous forms in savanna regions.
However, given evolutionary stasis (see Lundberg et al. 1986) and the possibility that
piranhas, as we now know them, had already evolved well before the climatic events of the
Pleistocene, piranha lifestyles would still have been dramatically altered by the climatic
cycles, and these fishes would have had to respond behaviorally, if not morphologically, to
large cyclical changes in food resources.
Trophic Patterns
Trophic Groupings
Based mostly on stomach content analysis, I identified six general trophic groups
among the serrasalmine fishes and size classes studied; four of these six feeding guilds
included piranhas. In order to compare the Low Llanos and the upper Orinoco groupings,
I attempt a general assessment in the following pages. Information on minor food items
not included in these discussions can be found in species account sections presented earlier.
1) Piscivores. The adults of at least seven Orinoco piranhas (Serrasalmus and
Pygocentrus; Table 8-1) are largely carnivorous, feeding mainly on fishes by either biting
out pieces of flesh or taking small fish whole. In addition to actively preying on other
fishes, piscivorous piranhas are opportunistic and scavenge on dead or dying fish (as well
as other vertebrates) (see Sazima and Guimaraes 1987, Nico and Taphom 1988).
Goulding (1980) reported that the dominant Amazonian piranha, S. rhombeus, preyed
most heavily on common fishes of about its own size by removing chunks of flesh. I

164
found that Orinoco piranhas, particularly in low Llanos where there is greater fish biomass,
frequently attack small fish.
As a group, piscivorous piranhas are often the predominant predators in lowland
habitats throughout the Orinoco River basin. Even in the upper Orinoco, I found that
carnivorous species (i.e., S. rhombeus and 5. manueli) outnumber individuals of the more
herbivorous species in most areas. The best information on numbers and biomass of
Orinoco piranhas comes from two studies in the Llanos. Based on rotenone sampling in a
savanna lagoon during the dry season, Mago-Leccia (1970) reported that piranhas (mostly
Pygocentrus caribe) accounted for 14 % of the total number of individuals and 26% of the
total fish biomass. In their study of flooded savannas in the Cao Caicara area, Taphom
and Lilyestrom (1984) found that the biomass of P. caribe was greater than any other fish
predator in both dry season and wet season samples. Their rotenone sampling of a dry
season pool showed that piranhas made up 14% of total fish biomass.
2) Fin Eaters. Stomach content analysis, supplemented by my observations on
feeding behavior of wild-caught juveniles, showed that most piranha species pass through
a growth stage, between 20 and 80 mm SL, when fin-eating is common or the predominant
mode of feeding. Fin-eating seems to be common in young of three of the four piranha
genera (all except juvenile Pygocentrus), and includes juveniles of both herbivorous and
carnivorous species from the Llanos and the upper Orinoco. At least two wide-ranging
species, Serrasalmus altuvei and S. elongatus, feed heavily on fins as adults (Roberts
1970, Goulding 1980, Nico and Taphom 1988, this study). Even though fins apparently
do not provide the nutritional benefits of fish flesh (see Chapter 7), many species may eat
fins because fins are an abundant and rapidly renewable resource (Northcote et al. 1987,
Nico and Taphom 1988). In cropping fins instead of eating the whole animal, piranhas
resemble herbivores that condnually exploit their food resource without eliminating it.
Reproduction of piranhas is closely correlated with the reproductive cycle of most other
fishes, thus there is an abundance of small prey available to young fin-eating piranhas.

165
Various tactics for successfully nipping fins from other fish have been described including
aggressive mimicry (Nico and Taphom 1986, 1988, Sazima and Machado 1990). Where
piranhas are abundant, many fishes have missing or damaged fins (Northcotte et al. 1987,
Nico and Taphom 1988) making the physical condition of fishes a useful indicator of
piranha density.
Defense by prey fish against fin-eating piranhas is an interesting topic and probably
includes both morphological and behavioral adaptations. The fins of several South
American fishes are nearly transparent in water, for instance those of the anostomid
Abramites hypselonotus Although there is no experimental evidence, the near
transparency of their fins probably provide them protection from predation by fin eaters.
Winemiller (1990) presented evidence that the caudal eyespot of the cichlid Astrononis
ocellatus acts as a deterrent against fin predation. However, behavioral adaptations against
fin-eating piranhas do not require a long history of coevolution. For example, I sometimes
give live bluegill (Lepomis macrochirus) and other native North American fish to young
aquarium-kept piranhas. In a large aquarium, small fast-sw imming fishes are able to avoid
predation; however, most bluegill are rapidly attacked and soon killed. Nevertheless, I
have observed that a few individuals survive weeks in a large tank with a single piranha.
Because fin-eating piranhas normally attack from behind and toward the rear of their prey,
these longer-surviving bluegill apparently learn to protect themselves by facing the piranha
and backing into dense vegetation or crevices. Thus they prevent attacks from the rear as
well as possible crippling injury to their caudal fin.
3) Scale Eaters. Scale-eating, or lepidophagy, is known for several unrelated South
American freshwater fishes (Roberts 1970, Sazima 1977, 1983, Sazima and Machado
1982, Goulding et al. 1988). The possible nutritional benefits of scales have already been
briefly discussed in Chapter 7, and like fins, scales can be thought of as a renewable
resource. Many of the serrasalmine species in both the Llanos and the upper Orinoco take
scales in small quantities, but the non-piranha Catoprion ment is the only species in which

166
individuals of all sizes fed heavily on scales. It was common in the low Llanos but rare in
samples from the upper Orinoco. Catoprion ment is a widely distributed species and its
scale-eating habits are well documented (Roberts 1970, Vieira and Gry 1979, Sazima
1983, 1988, Nico and Taphom 1988). The stomachs of several specimens of Myleus
torquatiis from the upper Orinoco were packed with scales; this is an unusual behavior not
previously reported for members of this generally herbivorous genus. Although most
studies suggest that adult Serrasalmus elongatus are primarily fin eaters (Roberts 1970) or a
general piscivore (Nico and Taphorn 1988, this study), Goulding (1980) reported that adult
Serrasalmus elongatus in the Madeira River drainage of Brazil preferred scales to fins.
Based on stomach content analysis alone, it is difficult or impossible to determine which
prey species are most frequently attacked. Certain species are obviously more vulnerable to
having scales removed than others. For instance, while the scales of some fish are firmly
attached to the body (e.g.,cichlids), the scales of others (i.e., many characoids) are easily
dislodged and these fish are probably more prone to attack by scale-eaters.
4) Predation on Invertebrates. Like the young of most freshwater fishes, small
juvenile piranhas (less than about 40 mm SL) commonly feed on immature aquatic insects
and microcrustaceans. Most major groups of small freshwater crustaceans were
represented in their diet, including cladocerans, copepods, ostracods, and conchostracans.
Most aquatic insects eaten by young piranhas were immature forms of cnironomids,
ephemeropterans, odonates, and plecopterans. The smallest piranhas in the Llanos fed
almost equally on insects and microcrustaceans, whereas small juveniles taken in
blackwater areas of the upper Orinoco preyed mainly on insects. Earlier it was emphasized
that there is a common association between young piranhas and aquatic vegetation. In
addition to providing some protection from predators, aquatic macrophytes are home to a
large number of invertebrate prey. Based on observations of wild-caught piranhas in
aquarium, Sazima and Zamprogno (1985) described how young juveniles pick
chironomids and ostracods from the roots of water hyacinths. Invertebrates are also taken

167
on occasion by adult piranhas, mostly terrestrial and flying insects, and shrimp and crabs.
Braga (1954) reported that shrimp were the main prey of adult Serrasalmus rhombeus
inhabiting a man-made lake.
5) Seed Predators. Many serrasalmine species feed on seeds and the hard parts
surrounding the seed (mainly endocarp). The term "seed predator" was used by Goulding
(1983) to refer to fishes that destroy seeds by mastication or other digestive processes.
This is in contrast to several other basically herbivorous serrasalmids (most often
Colossoma macropomum and Piaractus brachypomus) which, in addition to masticating
seeds, occasionally act as seed dispersal agents by swallowing and passing whole seeds
(Gottsberger 1978, Goulding 1980, 1983, personal observation). Four piranhas
representing three genera (Table 8-1) were largely herbivorous and all were primarily seed
predators. Myleus species from the upper Orinoco also sometimes feed on seeds that they
bite into small fragments. Llanos piranhas rarely eat seeds, but seed predation was
common among piranhas in all six upper Orinoco drainages. Goulding et al. (1988)
reported that Myleus switch from seed-eating to folivory during low water when fruits and
seeds are in shorter supply, this may be the case with Orinoco Myleus as well (see next
section on folivores), but I found that herbivorous piranhas continued to feed on seeds
even during the dryer season. Herbivorous fishes are known to gather around trees that are
dropping their fruit (Goulding et al. 1988). A few carnivorous serrasalmine species are
somewhat territorial (Sazima 1988, personal observation). Like their carnivorous relatives,
herbivorous piranhas can be very aggressive at times and it is conceivable that they
maintain feeding territories around fruiting trees during the low water season, driving away
other herbivorous fishes that might compete for a limited number of seeds.
Several authors list examples of the seeds and fruits eaten by various South
American fishes, including a few serrasalmine species (Gottsberger 1978, Goulding 1980,
Smith 1981, Goulding et al. 1988). I was unable to identify the crushed seeds found in the
stomachs of Orinoco piranhas, but a large Piaractus (560 mm SL) from the upper Orinoco

168
had its stomach and intestine full of what were probably palm seeds; about half the seeds
had been masticated and the remainder, about twenty seeds (about 30 mm long) had been
swallowed whole. Machado-Allison and Garcia (1986) reported that juveniles of several
piranha species from a savanna marsh fed on the tiny seeds of sedges (Cyperaceae), but
they did not give number of seeds eaten nor their percentage of the overall volume of food
(Table 1-1).
6) Leaf Eaters. None of the Orinoco piranhas were considered to be folivores, but
small bits of leaves or even flowers were eaten by all species on occasion. Of the
serrasalmine species studied, only Myleus feeds heavily on leaves. Piaractus will also take
leaves in bulk (personal observation). Folivorous serrasalmine fishes seem to restrict
themselves to feeding on live leaves that they clip into small fragments before swallowing.
Similar behaviors have been reported for leaf-eating fishes of the Amazon (Goulding 1980,
Goulding et al. 1988). Goulding et al. (1988) hypothesized that folivory by Amazonian
fishes is limited by the toxic chemicals in the leaves. Their studies suggest no specialized
folivores among herbivorous fishes, but rather that frugivorous fishes become leaf eaters
only when fruits and seeds are scarce, for instance during periods of low water. Most of
the Myleus that I examined were captured during the low water period; therefore, I cannot
rule out such a seasonal shift in diet. Nevertheless, the stomachs of herbivorous piranhas,
netted together with Myleus taken in the upper Orinoco during the drier part of the year,
were full of seeds, suggesting some sort of food resource partitioning.
Ontogenetic Changes in Diet
My study approach has been to emphasize dietary differences among different size
classes as well as among species. The differences found therefore tend to support the
contention of Stoner and Livingston (1984) that ecological studies of fishes should employ
the "ontogenetic trophic unit" concept rather than grouping a taxonomic species as a single
functional ecological unit. Changes in diet with age have been documented for many of the

169
Orinoco species found in the Llanos (Machado-Allison and Garcia 1986, Nico and Taphom
1988, Winemiller 1989a, Nico 1990) and for Serrasalmus spilopleura from a reservoir in
southern Brazil (Sazima and Zamprogno 1985) (Table 1-1). In general, piranhas change
their preferred prey as they grow from invertebrates as small juveniles, to fins as large
juveniles, and finally to a diet of mainly fish or plant matter. The size at which individuals
switch from one mode of feeding may be species specific, related to food resource
availability, or more likely, a combination of both of these factors. All juveniles less than
about 20 mm SL specialize on invertebrate prey (i.e., microcrustaceans and aquatic insect
larvae), some not switching to fins until about 40 mm SL. Fin eating is most common in
juveniles between 40 and 80 mm SL, but I found that juveniles as small as 20 mm SL
(e.g., Serrasalmus manueli) already begin feeding on fins taken from Other small fishes.
Although data are incomplete on several species, Pygocentrus caribe is the only common
piranha that does not feed on fins to any great extent as a juvenile (but see Machado-Allison
and Garcia 1986). Although some species continue to feed heavily on fins as adults, larger
individuals of most species switch to a diet consisting primarily of fish or seeds.
Herbivory among piranhas seems to be mainly an adult trait, whereas the young of other
serrasalmine fishes (e.g., Metynnis) will frequently feed on plant matter. In contrast to the
findings of Machado-Allison and Garcia (1986), young piranhas that I studied rarely ate
seeds or other plant matter.
Camivorv versus Herbivorv
Although adult piranhas may be classified as either largely carnivorous or largely
herbivorous (Table 1-1), my results suggest that they can adjust their diets to changes in
food resources. There is a certain amount of omnivory in both groups. However, when
specimens of both groups were taken together, diets were usually distinctly different. In
the upper Orinoco, when finding two or more piranha species in the same gill net, then-
stomachs were either full of seeds or fish flesh. Such partitioning of food resources was

170
usually predictable according to species. For the most part, occasional bits of plant material
in the stomachs of typically carnivorous species were considered the result of accidental
ingestion when these fish were attacking prey fish. However, underwater observations in
the Pantanal of Brazil reported by Sazima and Machado (1990) suggested that primarily
carnivorous species Serrasalmus spilopleura and Pygocentriis nattered actively feed on
leaves of aquatic plants while scanning for aquatic insects and small crustaceans.
A hypothetical model for describing piranha responses to differing environmental
conditions is presented in Figure 8-1. This model shows trends and not absolute values.
All piranhas exhibit a certain amount of trophic flexibility. The model shows diets of
carnivorous and herbivorous piranhas to be most different when conditions provide for a
roughly equal amount of plant (i.e., mainly seeds) and animal food (i.e., mainly fish), or
when neither type of food is in limited supply. The vertical broken line of Figure 8-1
shows a situation I frequently encountered when both carnivorous and herbivorous species
were taken together in the upper Orinoco. Like any model, it does not take into account all
possible variables or conditions, but it does explain many of the findings of the present
study.
During extreme conditions both trophic groups might be expected to adjust their
diets, resulting in high dietary overlap (e.g., P. striolatus in the Apure drainage). When the
availability of edible plant materials (primarily seeds) is low, there is a corresponding shift
by herbivorous fishes to a more omnivorous diet. Dietary shifts by adult piranhas are
likely to be associated either with temporal changes, such as from highwater to lowwater
conditions, or with spatial changes, such as from a forest habitat to one that is more typical
of savannas. An obvious case where such a shift might occur is a savanna lagoon during
the onset of the dry season; as the pool shrinks, prey fish densities rise (at least
temporarily), but the input of plant resources into the system becomes negligible. On the
other hand, largely carnivorous piranhas might shift to a more omnivorous diet when the
availability of plant materials increases, such as the change from low water to flood

171
Axis of Habitat Variables
Forest Habitat < > Savanna Habitat
Wet Season < > Dry Season
High Water < > Low Water
Low Perturbation < > High Perturbation
Low
Relative
Amount of
Fish
in Diet
High
High Plant Material < > Low Plant Material
Low Fish Prey < > High Fish Prey
Axis of Food Availability
Fig. 8-1. Proposed hypothetical model showing the dietary responses of carnivorous
versus herbivorous piranha species to changes in various habitat parameters and
food resources. Dashed vertical line indicates the condition where both plant
material and prey fish are in approximate equal supply and relatively abundant
(see Table 8-1 for list of piranha species involved).

172
conditions, especially in forested habitats. Perhaps the best examples of carnivorous
piranhas adjusting its diet to local conditions are individuals of Serrasalmus manueli that
had fed on seeds and fruits in the flooded forests of the Sipapo River.
Generalist versus Specialist
In his analysis of avian diets, Sherry (1990) discussed the subject of specialist
versus generalist from both ecological (i.e., tactical) and evolutionary (i.e., strategic) points
of view, also taking into account other closely related dichotomies (e.g., stereotypy vs.
plasticity, monophagy vs. polyphagy, specialized vs. opportunistic). Ln a study of insects,
Fox and Morrow (1981) found that many herbivorous species have generalized diets over
their entire geographical ranges but that they may function as specialists with restricted diets
in specific areas.
Diet breadth, as estimated by Levins' index (see Chapter 3), measures the diversity
and evenness of resource use. Thus, diet breadth is actually a quantitative attempt to
measure the degree of dietary specialization (i.e., the resulting value being lower for a
dietary specialist and higher for a dietary generalist). Unlike many dominant predators
found in freshwater communities, piranhas are little limited by gape size (i.e., not gape-
limited predators sensu Zaret 1980) because they use their teeth to cut out bite-size pieces
even from fairly large food items. Nevertheless, because larger piranhas are able to attack
or ingest a wider range of food sizes than smaller conspecifics, it would be expected that
diet breadth would increase with increasing fish size.
Although I found that diet breadth among piranhas usually changed with age, there
was no consistent pattern among species. The lowest diet breadth measured during my
study were for species and size classes considered to be scale eaters and fin eaters, fairly
specialized types of feeding behaviors. Nevertheless, species or size classes that specialize
on the fins or scales of other fishes can choose to attack many different fish species and
select from a wide range of prey fish sizes. In most instances, it was not possible to

173
identify a prey species based only on fin fragments or scales found during examination of
stomach contents. However, my observations of feeding by captive fishes indicate that fin-
eating and scale-eating serrasalmine fishes are capable of successfully attacking individuals
of many fish species. Fin-eating piranhas use several basic tactics to approach prey fish,
for instance ambushing, stalking, and active chase. Although particular species appear to
be better suited morphologically for employing one tactic over another (e.g., the stream
lined S. elongatus for active pursuit; narrow deep-bodied species such as S. altuvei for
stalking) (Nico and Taphom 1988, Sazima and Machado 1990), my observations indicate
that the particular tactic used by individuals of a given species can vary widely and seems to
depend on several factors, for example, the amount and type of cover, the density and type
of prey fish, and water clarity. In nature, juvenile Serrasalmns irritans-use aggressive
mimicry to approach other fish (Nico and Taphom 1986, 1988). However, in large
outdoor tanks I have seen individuals use both ambush and pursuit. In the first case, an
individual hides among rocks and ambushes passing fish; in other instances they leave their
hideaway and actively pursue fish in open water over distances of more than a meter. I
have kept a young wild-caught Pygopristis denticulatus for nearly a year in a large
aquarium; it slowly stalks novel prey fish, but it will immediately chase small fish that are
not novel. Based on the size of fins in their stomachs, small juveniles in nature attack fish
that are about their own size; however, large fin-eating piranhas will prey on the fins of fish
much larger than themselves, for example the pimelodid catfishes Brachyplatystoma and
Phractocephalus.
In the Orinoco and elsewhere, studies are needed to determine to what extent
herbivorous fishes specialize on particular seeds or leaves. The method of diet analysis
used here, scoring plant foods as masticated seeds versus other plant material, gives low
diet width values for herbivorous fishes that may be misleading. Goulding (1980, 1983)
and Goulding et al. (1988) reported that herbivorous fishes in the Amazon River basin
exploit a wide range of plant species, but they seem to prefer fruits and seeds of a few

174
common species (e.g., seeds from rubber trees and palms). Goulding (1980) was able to
identify only a few seeds eaten by Amazonian piranhas. Similarly, because I could not
identify the seeds and most other plant materials in the diets of Orinoco herbivorous species
(i.e., adults), I cannot adequately assess their degree of specialization. Snow (1981)
distinguished between specialized frugivorous birds and unspecialized or opportunist
frugivores. The former typically feed on fruits rich in fats and proteins, whereas the latter
mosdy take fruits that provide mainly carbohydrates and less nutritious overall.
Although serrasalmine species or size classes were assigned to particular trophic
guilds, all exhibited a certain amount of plasticity in their diets. Because most foods do not
supply all the nutrients needed by an animal, a certain level of diet flexibility is probably a
requirement. An assessment of the balance between benefits and costs of piranha particular
modes of feeding and prey choice lies beyond the scope of the present study. Analysis of
energy and nutrient content suggests that certain types of foods are generally more
beneficial than others (e.g., fish flesh and insects over fish fins and scales, fruits and seeds
over leaves), but it ignores the possible costs of foraging, and that proportion of a food
item that is actually assimilated by the consumer. Each of these determinations would
require further study. Comparing aquatic versus terrestrial feeding modes, Liem (1990)
hypothesized that fish, by nature of their being designed for life in the water, have a much
more versatile feeding apparatus (i.e., mouth and jaw structures) than terrestrial
vertebrates. Based on this "built-in versatility", one of Liem's predictions was that fish
should be highly opportunistic in their feeding, thereby exhibiting both high dietary overlap
and extensive prey switching.

175
Ecomorpholoeical Correlates
Ecomorphology examines correlations between organism morphology and selective
demands of its external environment Keast and Webb (1966) were among the first to look
closely at possible relationships between fish trophic morphology and fish diets.
Piranhas have interspecific variation in body height, body width, shape of snout
and maximum size; general body shape also changes dramatically during growth in several
species, for example in Serrasalmus rhombeus as described and figured by Gry (1972).
Nico and Taphom (1988) thought that piranhas with sharp snouts (Serrasalmus irritaos and
S. elongatus) were more adapted for nipping fins or taking scales but found that even a few
species with somewhat blunt snouts (S. medinai and Pristobrycon strioiatus) fed heavily on
fins. Sazima and Machado (1990) also suggested that particular piranha body
morphologies were associated with particular predatory tactics: the low profile and
powerful tail of Pygocentrus nattered for giving short chase, and the high fins and narrow
body (in addition to a greenish body color) of the fin-eating S. marginatus for hiding in
vegetation while stalking its prey.
Particular types of morphology or behavior can preadapt animals to their current
ecological niches. For example, Futuyma (1986:424) described how a New Zealand
parrot, the kea (Nestor notabilis), uses its beak to rip through the skin of sheep and feed on
the fat beneath. The beak is similar to that of normal seed- and fruit-eating parrots, but its
form presumably preadapted the kea to invade the sheep-eating niche. Piranhas have a
single row of sharp, somewhat triangular teeth in both jaws used for rapid puncture and
shearing. Dental morphologies exhibit only slight variation among species, and are
sufficiently unspecialized that individuals are able to exploit a broad range of food. As
such, the unique dentition and strong jaw musculature of piranhas preadapts them for
feeding on hard seeds and fruits. This statement presumes, possibly incorrectly, that
camivory is the "primitive" ecological character state within piranhas.

176
Other morphological features related to feeding, for instance intestine length, show
much more variation among the different piranha species. Previous investigators have
noted that carnivorous fish (like many terrestrial vertebrates) have relatively shorter
intestines than herbivorous fish (see Ribble and Smith 1983), suggesting a correlation
between length of the gastrointestinal tract and the feeding ecology of a species (but see
Smith 1989). A longer intestinal tract provides a greater surface area for digestion and
absorption of difficult to digest plant material. Several researchers have even reported large
intraspecific differences in intestine length among fishes. For example, Odum (1970)
compared two populations of mullet (Mugil cephaliis) and reported that the gastrointestinal
tract was nearly twice as long in those fish living in a marsh habitat and feeding on hard-to-
digest items such as plant detritus and blue-green algae when compared to mullet inhabiting
an area where the predominant food consisted of benthic and epiphytic diatoms, a food
more easily digested. Luengo (1965) noted the relationship between the carnivorous diet of
Pygocentrus caribe (identified as Serrasalmus nattereri) and its relatively short intestine.
My study showed that intestinal length in Orinoco piranhas varies interspecifically
and is closely correlated with diet. Dental morphology, on the other hand, is a relatively
conservative character within the four piranha genera, although relative jaw width and
degree of musculature vary. This contrasts with the situation present in other serrasalmine
fishes, which exhibit a much more diverse dental morphology, indicating a more labile
evolutionary past (Lundberg et al. 1986). The adults of most non-piranha serrasalmines
are herbivorous (e.g., Mylens, Mylossoma, and Metynnis) and have relatively long
intestines. Catoprion ment is an exception because it eats scales and has a short intestine.
In addition, studies with other vertebrates indicate that features other than length (e.g.,
cellular anatomy or biochemical composition) also determine function of the digestive tract,
and these characters may also show inter- and intraspecific differences (e.g., Karasov and
Diamond 1988). However, I found no evidence to suggest that the intestine length of
individual fish changes in response to shifts in diet.

177
A Phylogenetic Perspective
In order to synthesize information concerning ecology and evolution, biologists
commonly superimpose ecological or behavioral results onto hypothesized phylogenies
derived from gross morphology or biochemical systematics (Brooks and McLennan 1991).
These types of analyses are preferred because they attempt to establish correlations between
the evolutionary history of organisms and present-day patterns of morphology, behavior,
and ecology. Nevertheless, as Losos (1990) has suggested, meaningful analysis in a
phylogenetic context requires that the group under study has radiated extensively and that
the phylogenetic relationships are relatively well understood. Although piranhas and their
close relatives have undergone moderate radiation, their taxonomy, particularly at the
species level, is still fluid and phylogenetic relationships of serrasalmine fishes are only
partly understood. Using morphological characters, Machado-Allison (1985) provided the
most current analysis of relationships of the subfamily Serrusalminae (Fig. 1-1). His
phytogeny is to genus level only, and its utility for this study is further limited because
most species are in the trophically diverse genus Serrasalmus.
My study provides information on the diets for nine of the 13 serrasalmine genera.
Using data on trophic groupings, I have superimposed my findings onto Machado-
Allison's phytogeny (Fig. 8-2) following the methods of Langtimm and Dewsbury (1991).
It gives a consistency index of 0.5 suggesting that trophic groupings and intestine length
are somewhat consistent with a phytogeny derived from strictly morphological characters.
Because much of the variation in trophic characters within the genus Serrasalmus was due
to the inclusion of Serrasalmus cf. eigenmanni, if this herbivorous species is not included
in the analysis then the consistency index is much higher (i.e., 0.67). Fink (1988)
emphasized the need for future studies on piranha ecology and behavior in addition to
systematic and phylogenetic analyses. Admittedly, my study on serrasalmine trophic
ecology has not answered all the questions. Nevertheless, it will be interesting to see how

178
the conclusions drawn here fare when they are re-evaluated in light of a well understood
phytogeny of the piranhas.

Fig. 8-2. Diets and intestine length mapped onto the proposed phylogeny of Machado-Allison (1985) for genera of the subfamily
Serrasalminae. The four piranha genera are highlighted. Orinoco taxa not examined during this study are not included
in tree. Jv = juvenile trait; ad = adult trait

Piscivores O M S3
Fin eaters (jv) D Hi Hi Hi
Fin eaters (ad) CD O CD S3
Scale eaters ES Bl CU
Herbivores M M M'm Hi S3
Long Intestine £ # # # O O
Piaractus Mylossoma Myleus Metynnis Catoprion Pygopristls Pygocentrus Prlstobrycon Serrasatmus

APPENDIX A
MATERIAL EXAMINED
Specimens examined are deposited at the Museo de Ciencias Naturales (MCNG) at
UNELLEZ, Guanare, Venezuela, and the Florida Museum of Natural History (UF),
Gainesville, Florida. Catalogued specimens are designated by MCNG or UF numbers and
uncataloged specimens by field collection numbers (PIMA, DCT or LN). Total number of
fish in that series and number of specimens in which gut contents were examined, or
intestine measured, is given in parentheses. Small juveniles (jv) are specimens less than 20
mm Standard Length.
Pristobrvcon strinlatus
Llanos
Apure River drainage: Cao MaporaL-1980: MCNG 9102 (1-0); MCNG 11373
(1-0). 1981: MCNG 9178 (2-0); MCNG 10127 (1-0); MCNG 10247 (6-3); MCNG
11371 (8-5); MCNG 11372 (5-3). 1983: MCNG 10073 (2-1). 1984: MCNG 11347 (6-
2); MCNG 11360 (5-1); MCNG 15736 (1-1?). 1985: MCNG 11511 (2-1). 1989:
MCNG 19454 (1-1).
Cinaruco River drainage: 1986: MCNG 1793 (1-1). 1987: MCNG 17157 (4-4).
1989: MCNG 21805 (1-1); MCNG 20018 (1-1);
Capanaparo River drainage: 1989: MCNG 20283 (4-4);
Other: 1987: MCNG 17387 (2-2).
181

182
Upper Orinoco
Ventuari River drainage: 1989: MCNG 22054 (38jv-38).
Mavaca River drainage: 1991: MCNG 25335 (1-1); Ocamo River drainage: 1990:
MCNG 22249 (4-4)
Pristobncon sp
Upper Orinoco
Atabapo River drainage: 1989: MCNG 21757 (5-5) (note: these five specimens
will be paratypes and divided among several museums, MCNG 21757 [2-2], MBUCV #
[1-1], and UMMZ # [2-2]).
Pvqocentrus caribe
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 3547 (1-1); MCNG
7686 (1-1); MCNG 8313 (4-4); MCNG 8342 (1-0); MCNG 9421 (2-2). 1980: MCNG
1776 (1-1); MCNG 4440 (1-1); MCNG 5899 (8-7); UF 37063 (2-0). 1981: MCNG 1996
(6-0); MCNG 2036 (5-5); MCNG 2076 (2-2); MCNG 2160 (7-7); MCNG 2166 (7-7);
MCNG 2188 (5-5); MCNG 2215 (1-1); MCNG 2298 (2-2); MCNG 2357 (4-4); MCNG
2379 (25-25); MCNG 2461 (4-4); MCNG 2482 (1-1); MCNG 3693 (2-2); MCNG 3728
(3-3); MCNG 3754 (1-1); MCNG 3842 (3-3); MCNG 3873 (1-1); MCNG 3888 (9-9);
MCNG 4006 (3-3); MCNG 4023 (145-30); MCNG 4049 (13-7,6jv); MCNG 4058 (2-2);
MCNG 4074 (3-1,2jv); MCNG 4119 (7-7); MCNG 4135 (6-6); MCNG 4153 (47-47);
MCNG 4168 (1-1); MCNG 4200 (2-2); MCNG 4217 (2-2); MCNG 4284 (3-3); MCNG
4309 (2-2); MCNG 4491 (1-1); MCNG 4557 (2-2); MCNG 4689 (2-2); MCNG 4715 (1-
1); MCNG 4737 (1-1); MCNG 4757 (2-2); MCNG 4777 (1-1); MCNG 4796 (1-1); 4901
(7-7); MCNG 4925 (5-5); MCNG 5030 (2-2); MCNG 5168 (1-1); MCNG 7881 (57-57?);

183
MCNG 10418 (2-1,ljv); MCNG 10419 (20-19, ljv); DCT 81-157 (2-1); DCT 81-159 (2-2);
DCT 81-160 (20-20); PIMA 18-25 (5-4); PIMA 18-26 (1-1); PIMA 18-27 (6-6); PIMA 18-
30 (3-3); PIMA 18-33 (5-5); PIMA 18-36 (7-7); PIMA 18-37 (1-1); PIMA 18-44 (4-4);
PIMA 18-46 (7-6); PIMA 18-49 (1-1); PIMA 18-78 (1-1); PIMA 18-90 (14-14); PIMA 18-
91 (1-1); uncatalogued student collection (11-10). 1982: MCNG 5075 (1-1); PIMA 18-96
(2-2); PIMA 18-98 (3-3); PIMA 18-99 (4-4). 1983: MCNG 10322 (77-71). 1984:
MCNG 10709 (18-18); MCNG 11325 (72-14); 11367 (4-4?); LN 84-7 (14-14); LN 84-8
(8-8); LN 84-76 (71-55?); DCT 84-13 (7-7). 1988: LN 88-23 (12-12); LN 88-24 (13-13);
LN 88-26 (43-43); LN 88-27 (17-17); LN 88-28 (11-11); LN 88-29 (11-11); LN 88-30
(16-16). 1989: LN 89-171 (5-2); LN 89-170 (6-6); LN 89-173 (1-1); LN 89-176 (9-9).
Other: MCNG 20751 (7-7); MCNG 8790 (1-1?).
Juveniles less than 20 mm SL.tentatively identified as P. caribe. UNELLEZ
module.-1981: MCNG 3949 (59-27jv); MCNG 3956 (21-20jv); MCNG 4006 (2-2);
MCNG 4023 (145-29jv); MCNG 4049 (13-6jv); MCNG 4< ¡74 (3-2jv); MCNG 4075 (1-1);
MCNG 4119 (7-3); MCNG 4135 (5-ljv); MCNG 4258 (1-1); MCNG 7881 (57-24jv);
MCNG 10418 (2-ljv); MCNG 10419 (20-ljv); MCNG 10424 (1-1).
Upper Orinoco
Ventuari River drainage: .1989: MCNG 22974 (2-2); MCNG 22247 (1-1); LN 89-
166 (2-2); LN 89-167 (2-2).
Ocamo River drainage: .1990: MCNG 22269 (2-2); MCNG 22295 (2-2); LN 90-
20 (1 1).
Pvqopristis denticulatm
Llanos
Apure River drainage: 1981: MCNG 3243 (3-1); UF 36177 (1-0).

184
Cinaruco River drainage: 1987: MCNG 17157 (4-0?); 1989: MCNG 20018 (2-2);
MCNG 20110 (1-1).
Capanaparo River drainage: 1989: MCNG 21885 (4-4); MCNG 17776 (3-3); UF
84183 (1-1).
Upper Orinoco
Venturari River drainage: 1981: MCNG 7874 (2-0);
Atabapo River drainage: 1989 MCNG 21881 (1-1);
Mavaca River drainage: 1991: LN 91-19 (33-9); LN 91-45 (47-15).
Serrasalmus altuvei
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 9147 (1-1). 1981:
MCNG 3619 (4-4). 1984: MCNG 10713 (5-5). 1985: MCNG 12470 (1-0). Cao
Maporal.-1981: MCNG 9356 (1-0); MCNG 11018.(1-0): UF 31859 (2-0). 1983:
MCNG 10075 (2-0). 1988: MCNG 21241 (1-1).
Upper Orinoco
Matacuni River drainage: 1990: MCNG 22126 (3-0); MCNG 22417 (1 1).
Mavaca River drainage: 1991: MCNG 25336 (7-7); MCNG 25410 (1-1).
Serrasalmus elongatus
Llanos
Apure River drainage: UNELLEZ module.-1980: MCNG 5902 (2-1). 1981:
MCNG 2044 (1-1); MCNG 4560 (1-1); MCNG 4736 (1-1). 1984: MCNG 10711 (9-8).
1985: MCNG 11382 (13-13); MCNG 11539 (2-2). 1989: MCNG 23139 (1-1); MCNG
23156 (1-1); MCNG 23179 (1-1); MCNG 23164 (7-7); MCNG 23386 (1-1); MCNG
23169 (9-9). 1990: MCNG 23384 (2-2). Cao Maporal.- 1980: MCNG 6067 (3-2);

185
MCNG 9101 (2-1). 1981: MCNG 11015 (2-2); UF 31858 (1-0); UF 77722 (1-0). 1984:
MCNG 11361 (8-4); MCNG 11350 (1-1) 1988: MCNG 21242 (2-2). Cao Caicara:
1990: MCNG 23382 (3-3). Other.-1979: MCNG 1193 (1-1); MCNG 9683 (2-2); MCNG
12588 (1-1).
Capanaparo River drainage: 1989: MCNG 20229 (1-0).
Serrasalmus cf. eigenmanni
Llanos
Cinaruco River drainage: 1989: MCNG 21380 (1-1); MCNG 20156 (2 2).
Upper Orinoco
Ventuari River drainage: 1989: MCNG 22116 (1-1).
Ocamo River drainage: 1990: MCNG 22415 (1-1); MCNG 22410 (1-1); MCNG
22260 (8-8); MCNG 22287 (1-1); MCNG 22289 (1-1); MCNG 22290 (2-2); MCNG
22250 (3-3); MCNG 22406 (4-4).
Matacuni River drainage: 1990: MCNG 22125 (5-5); MCNG 22129 (9 9).
Orinoco main stem: 1990: MCNG 21850 (1-1).
Mavaca River drainage: 1991: MCNG 25409 (4-4); MCNG 25361 (2-2); MCNG
25364 (4-4); MCNG 25337 (3-3).
Other
Caura River drainage: 1989: MCNG 21047 (3-3); ;MCNG 21593 (3-3); MCNG
21929 (6-6).
Serrasalmus irritans
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 7685 (4-4); MCNG
8409 (1-1); MCNG 9443 (2-2). 1980: MCNG 4439 (1-1); MCNG 5901 (13-13). 1981:

186
MCNG 1995 (6-6); MCNG 2046 (28-28); MCNG 2122 (6-6); MCNG 2162 (4-4); MCNG
2189 (3-3); MCNG 2216 (2-2); MCNG 2336 (1-1); MCNG 2359 (9-9); MCNG 2377 (15-
15); MCNG 3645 (1-1); MCNG 3729 (6-6); MCNG 3843 (1-1); MCNG 3889 (1-1);
MCNG 3984 (1-1); MCNG 4092 (3-3); MCNG 4154 (2-2); MCNG 4166 (7-7); MCNG
4199 (4-4); MCNG 4218 (1-1); MCNG 4233 (1-1); MCNG 4308 (4-4); MCNG 4341 (3-
3); MCNG 4543 (1-0); MCNG 4558 (2-2); MCNG 4583 (1-1); MCNG 4688 (2-2);
MCNG 4735 (1-1); MCNG 4776 (1-1); MCNG 4795 (1-1); MCNG 4927 (1-1); MCNG
4974 (20-20); UF 36153 (2-0); UF 77721 (1-0). 1982: MCNG 6325 (1-1). 1984:
MCNG 10712 (50-50); MCNG 11324 (2-2); MCNG 11364 (31-31); MCNG 11366 (1-1);
MCNG 11370 (1-1); LN 84-8 (1-0); DCT 84-68 (4-4). 1985: MCNG 11383 (17-17);
MCNG 11540 (1-0?); MCNG 12471 (6-5). 1989: MCNG 23387 (17-9); MCNG 23134
(6-6); MCNG 23141 (14-7); MCNG 23151 (6-1). 1990: MCNG 23385 (8-8). Cao
Caicara: 1989: LN 89-22 (1-1).
Serrasalmus 'marine I i
Llanos
Cinaruco River drainage: 1982: MCNG 5629 (3-3); 1986: MCNG 17954 (1-1).
1987: MCNG 17156 (8-8). 1989: MCNG 22185 (2-2); MCNG 20180 (2-2); MCNG
21764 (8-8); MCNG 21759 (2-2).
Capanaparo River drainage: 1989: MCNG 20064 (1-1).
Upper Orinoco
Sipapo River drainage: 1989: MCNG 21972 (6-6); LN 89-71 (4-4); LN 89-61
(1-1).
Atabapo River drainage: 1989: MCNG 21957 (6-6); MCNG 21795 (5-5); MCNG
22023 (1-1); MCNG 21889 (2-2); MCNG 21890 (1-1); MCNG 22019 (2-2); MCNG

187
21957 (6-6); MCNG 22020 (1-1); MCNG 21795 (5-5); MCNG 21966 (6-6); LN 89-153
(3-3); LN 89-154 (2-2); LN 89-161 (4-4); LN 89-165 (16-16).
Ventuari River drainage: 1989: MCNG 21969 (3-3); MCNG 21837 (2-2 ): MCNg
22128 (2-2); MCNG 21972 (1-1); MCNG 21982 (1-1); MCNG 21980 (2-2); MCNG
21969 (3-3); MCNG 22022 (5-5); MCNG 22115 (1-1); Small juveniles tentatively
identified as Serrasalmus manueli: MCNG 22053 (5-5jv).
Orinoco main stem: 1989: LN 89-92 (1-1). 1990: MCNG 21849 (2-2). 1991:
MCNG 25408 (3-3); MCNG 25396 (3-3); LN 91-50 (1-0).
Serrasalmus medinai
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 7684 (1-1); MCNG
8408 (1-1); MCNG 11311 (1-1). 1980: MCNG 5900 (16-16). 1981: MCNG2124(4-
4); MCNG 2165 (1-1); MCNG 2285 (2-2); MCNG 2299 (1-1); MCNG 2358 (3-3);
MCNG 2378 (8-8); MCNG 3887 (1-1); MCNG 3918 (1-1): MCNG 4167 (1-1); MCNG
4340 (1-1); MCNG 4559 (2-2); MCNG 4778 (2-2); MCNG 4881 (1-1); MCNG 4926 (4-
4); MCNG 4975 (4-4); MCNG 10421 (1-1); MCNG 10422 (1-1); UF 31458 (1-0); UF
36156 (3-0). 1984: MCNG 10710 (20-20); MCNG 11365 (1-1). 1985: MCNG 11384
(21-21); MCNG 12472 (3-3); MCNG 12561 (6-6). 1989: MCNG 23171 (7-7); MCNG
23142 (5-5); MCNG 23152 (5-5); MCNG 23157 (4-4); MCNG 23162 (1-1); MCNG
23155 (1-1); LN 89-20 (1-1). Cao Maporal.-1980: MCNG 9099 (1-1). 1981: MCNG
10126(1-1); MCNG 10244(2-2); MCNG 11017 (1-0). 1983: MCNG 10072 (1-1).
1984: MCNG 11351 (2-0); MCNG 12562 (1-1). Other.-1979: MCNG 9684 (14-6);
MCNG 9751 (1-1). CaoCaicara: 1990: LN 90-62 (2-2).

188
Serrasalmus rhombeiis
Llanos
Apure River drainage: UNELLEZ module.-1979: MCNG 8267 (1-1); MCNG
8314(3-3). 1981: MCNG 4137 (1-1); MCNG 10420 (1-1); MCNG 10423 (1-1); MCNG
10464(1-1); MCNG 11330 (1-1); MCNG 11331 (1-1); (1-1); DCT 81-157 (3-3). 1984:
MCNG 11345 (1-1); MCNG 11368 (1-1); MCNG 11377 (1-1). 1988: 19070 (1-1); LN
89-12 (1-1). 1989: MCNG 23389 (2-2). Cao Maporal.-1981: MCNG 10168 (1-1);
MCNG 10246 (1-1); MCNG 10288 (7-7); UF 77723 (2-0). 1984: MCNG 11362 (7-6);
MCNG 11348 (1-1); MCNG 11376 (2-2). Other.-1979: MCNG 9752 (13-4). 1984:
MCNG 1927 (1-1); MCNG 11378 (4-4); MCNG 12933 (6-6).
Upper Orinoco
Orinoco main stem: 1989: MCNG 22503 (2-2); LN 89-92 (1-1). 1991: MCNG
25397 (1-1)
Ventuari River drainage: 1989: MCNG 22021 (1-1); MCNG 21970 (1-1); MCNG
21981 (1-1); MCNG 21968 (3-3); LN 89-111 (5-5); MCNG 21926 (1-1); MCNG 22021
(1-1); MCNG 22503 (2-2);
Matacuni River drainage: 1990: MCNG 22507 (3-3); MCNG 22127 (14-14);
Ocamo River drainage: 1990: MCNG 22109 (1-1); MCNG 22102 (1-1); MCNG
22114 (5-5); MCNG 22130 (1-1); MCNG 22131 (1-1); MCNG 22270 (3-3); MCNG
22294 (2-2); MCNG 22411 (1-1); MCNG 22412 (4-4); MCNG 22416 (5-5); MCNG
22420 (1-1); MCNG 22251 (1-1); MCNG 22261 (2-2); MCNG 22923 (1-1); LN 90-12
(5-5); LN 90-14 (6-6); LN 90-19 (1-1); LN 90-21 (1-1); LN 90-22 (1-1); LN 90-26 (2-2);
LN 90-27 (3-3); LN 90-33 (1-1); LN 90-42 (7-7); LN 90-37 (4-4); LN 90-38 (2-2): LN
90-45 (2-2); LN 90-46 (2-2); LN 90-49 (1-1);
Mavaca River drainage: 1991: MCNG 25365 (1-1).

189
Other Serrasalmine Fishes
Catoprion ment
Llanos: UNELLEZ module.-1979: MCNG 9422 (2-2). 1980: MCNG 4428 (1-
1); MCNG 5897 (10-10); UF 37061 (1-0). 1981: MCNG 1986 (1-1); MCNG 2055 (5-5);
MCNG 2179 (1-1); MCNG 4866 (1-1). 1984: MCNG 10708 (31-31). 1985: MCNG
11385 (78-5). Cao Maporal.-1980: MCNG 6070 (6-6); MCNG 9111 (8-8). 1981:
MCNG 5765 (5-5); MCNG 7655 (6-6); MCNG 9179 (1-1); MCNG 9358 (1-1); MCNG
10219(1-1); UF 77720 (1-0). 1982: MCNG 7046 (3-3). 1983: MCNG 10071 (13-13).
1984: MCNG 11374 (2-2); MCNG 11375 (1-1). 1989: MCNG 23388 (1-1)
Upper Orinoco: Ocamo River drainage: 1990: MCNG 23415 (2-2). Mavaca River
drainage: 1991: MCNG 25403 (1-1); MCNG 25404 (1-1); MCNG 25362 (1-1); MCNG
25353 (1 1); UF 85217 (1-1).
Metvnnis spp.
Llanos: Apure River drainage: 1984: LN 84-7 (1-1). 1985: MCNG 11508 (17-
3). 1989: MCNG 23174 (6-1); MCNG 23145 (3-1); MCNG 23178 (1-1); MCNG 23161
(1-1).
Upper Orinco: Mavaca River drainage: 1991: MCNG 25333 (1-1); MCNG 25360
(1-1); MCNG 25411 (2-2); MCNG 25363 (1-1); LN 91-19 (2-1); LN 91-45 (1-1).
Mylens asterias
Upper Orinoco: Mavaca River drainage: 1991: UF 85212 (2-0); MCNG 25334
(11-2). Matacuni River drainage: 1990: MCNG 23381 (1-1); MCNG 23379 (1-1);
Ocamo River drainage: 1990: MCNG 23380 (8-8); MCNG 22288 (5-4); MCNG 22412
(4-3); MCNG 22413 (1-1); MCNG 22408 (2-2); MCNG 23416 (16-14).

190
Mvleus schomburgkii
Llanos: Capanaparo River drainage: 1989: MCNG 20067 (2-2); MCNG 20086
(3-3). Cinaruco River drainage: 1989: MCNG 20173 (1-1). Riecito River drainage:
1982: MCNG 6209 (2-2).
Upper Orinoco: Orinoco main stem: 1991: MCNG 25399 (1-1). Ventuari River
drainage: 1989: MCNG 22885 (2-2). Atabapo River drainage: LN 89-162 (2-2). Ocamo
River drainage: 1990: MCNG 22407 (1-1); Mavaca River drainage: MCNG 25401 (1-1)
Casiquiare: 1985: MCNG 12354 (1-1).
My lens torquatus
Upper Orinoco: Orinoco main stem: 1991: MCNG 25398 (2-2); LN 91-3 (4-4).
Ocamo River drainage: 1990: MCNG 23378 (1-1). Ventuari River drainage: 1989:
MCNG 22884 (4-3). Mavaca River drainage: 1991: MCNG 25423 (14-14); UF 85213
(2-2).
My leus sp.
Upper Orinoco: Atabapo River drainage: 1989: LN 89-162 (2-2).
Mvlossoma duriventrus.
Llanos: Apure River drainage: 1981: MCNG 2091 (1-1). 1984: MCNG 17154
(1-1).
Piaractus brachypomus
Upper Orinoco: Sipapo River drainage: 1989: LN 89-63 (1-1).

APPENDIX B
STATISTICAL ANALYSES
Analysis of Covariance (ANCOVA)
Following are the results of ANCOVA comparing intestine length and standard
length of different combinations of piranha species. Analysis carried out using Type III
sum of squares of SuperANOVA computer program on a Macintosh SE/30 computer.
Data were not transformed.
Table B-l. ANCOVA of standard length (SL), with intestine length (EL) as dependent
variable, comparing three piranha species from upper Orinoco: Serrasalmus manueli (n =
60), S. rhombeus (n = 70), and S. cf. eigenmanni (n = 32).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
2
6863.142
3431.571
1.570
0.2112
SL
1
887772.922
887772.922
406.273
0.0001
Species x SL
2
63119.741
31559.870
14.443
0.0001*
Residual
156
340885.717
2185.165
^Conclude that slopes of regression lines are different.
191

192
Table B-2. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and 5. rhombeus (n =
70).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
574.649
574.649
0.288
0.5924
SL
1
1923573.822
1923573.822
964.479
0.0001
Species x SL
1
6466.875
6466.875
3.242
0.0741*
Residual
126
251296.649
1994.418
^Conclude that slopes of regression lines are not different at 0.05 level of significance,
therefore eliminate interaction effect (see Table B-3) to see if y-intercept is the same..
Table B-3. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and S. rhombeus (n =
70) eliminating interactive effect (i.e., adjusting for differences in SL).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
68775.973
68775.973
33.886*
0.0001*
SL
1
1922891.270
1922891.270
947.408
0.0001
Residual
127
257763.523
2029.634
* Adjusting for differences in SL, reject null hypothesis and conclude that y-intercepts are
different, therefore the IL of the two species differ significantly (F = 33.89, P = 0.0001).

193
Table B-4. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and 5. cf. eigenmanni
(n = 32).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
6822.825
6822.825
3.024
0.0856
SL
1
547308.446
547308.446
242.538
0.0001
Species x SL
1
48373.729
48373.729
21.437*
0.0001*
Residual
88
198579.446
2256.585
^Conclude that slopes of regression lines are different, and that the IL/SL ratio of S. cf.
eigenmanni is significantly greater.(F = 21.44, P = 0.0001).
Table B-5. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus rhombeus (n = 70) and S. cf. eigenmanni
(n = 32).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
4463.807
4463.807
1.886
0.1727
SL
1
506164.993
506164.993
213.908
0.0001
Species x SL
1
61742.334
61742.334
26.093*
0.0001*
Residual
98
231895.339
2366.279
^Conclude that slopes of regression lines are different, and that the IL/SL ratio of S. cf.
eigenmanni is significantly greater.(F = 26.09, P = 0.0001).

194
Table B-6. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and low Llanos 5.
manueli (n = 20).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
1
1857.851
1857.851
0.815
0.3696
SL
1
1147080.511
1147080.511
503.084
0.0001
Species x SL
1
1527.190
1527.190
0.670
0.4157*
Residual
76
173287.427
2280.098
^Conclude that slopes of regression lines are not different at 0.05 level of significance,
therefore eliminate interaction effect (see Table B-6) to see if y-intercept is the same..
Table B-7. ANCOVA of standard length (SL) with intestine length (IL) as dependent
variable comparing Upper Orinoco Serrasalmus manueli (n = 60) and low Llanos S.
manueli (n = 20) while eliminating interactive effect (i.e., adjusting for differences in
SL).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Population
1
336.248
336.248
0.148*
0.7014*
SL
1
1481368.833
1481368.833
652.493
0.0001
Residual
127
174814.617
2270.320
* Adjusting for differences in SL, reject null hypothesis and conclude that y-intercepts are
different, therefore the IL of the two species differ significantly (F = 33.89, P = 0.0001).

195
Mann-Whitnev U Test
Following are the results of one-tailed Mann-Whitney U tests comparing the degree
of herbivory of piranha populations from the low Llanos to those from the upper Orinoco.
Comparisons are made using results of percent adjusted volume (%Va), percent dominance
(%D), and percent frequency of occurrence (%0), based on specimens > 80 mm SL
(combining information on the two largest size classes for each species, 80-159 mm SL
and > 160 mm SL). Specimens with empty stomachs were not figured into the
calculations. Number of specimens by species is given in Table 6-9.
Table B-8. Percent adjusted volume (%Va) of plant material in piranhas (> 80 mm SL) as
associated with the low Llanos and upper Orinoco.
Low Llanos
Upper Orinoco
Taxon
%Va
%Va
Pristobrycon sp.
-
100.0
Pristobrycon striolatus
41.0
73.0
Pygocentrus caribe
6.7
11.0
Pygopristis denticulatus
50.0
100.0
Serrasalmus altuvei
0
0
S. cf. eigenmanni
25.0
70.0
S. manueli
0
26.0
S. rhombeus
11.9
2.0
S. elongatus
3.6
-
S. irritans
5.0
-
S. medinai
2.9
-

196
Table B-9. Percent dominance (%D) of plant material in piranhas (> 80 mm SL) as
associated with the low Llanos and upper Orinoco.
Low Llanos
Upper Orinoco
Taxon
%D
%D
Pristobrycon sp.
-
100.0
Pristobrycon striolatus
50.0
80.0
Pygocentrus caribe
11.2
33.3
Pygopristis denticulatus
66.7
100.0
Serrasalmus altuvei
0
0
S. cf. eigenmanni
33.3
68.2
S. manueli
0
27.0
S. rhombeus
12.5
1.7
S. elongatus
4.0
-
S. irritans
8.6
-
S. medinai
6.0
-

197
Table B-10. Percent frequency of occurrence (%0) of plant material in piranhas (> 80
mm SL) as associated with the low Llanos and upper Orinoco.
Low Llanos
Upper Orinoco
Taxon
%0
%0
Pristobrycon sp.
-
100.0
Pristobrycon striolatus
80.0
100.0
Pygocentnis caribe
34.1
50.0
Pygopristis denticulatus
66.7
100.0
Serrasalmus altuvei
28.6
22.2
S. cf. eigenmanni
66.7
81.8
S. manueli
8.3
43.2
S. rhombeus
25.0
15.5
S. elongatus
32.0
-
S. irritaos
18.6
-
S. medinai
26.0
-
Table B-l 1. One-tailed Mann-Whitney U test results testing the prediction that forest
populations fed more on plant material than their savanna counterparts. Ni = number of
species from upper Orinoco: N2 = number of species from low Llanos.
Diet Measure
Ni
n2
u
Mean
SD*
z value*
P
%Va
8
10
23
40
11.22556
- 1.514402
0.0655
%D
8
10
22.5
40
11.21973
- 1.559752
0.0594
%0
8
10
23
40
11.21556
- 1.514402
0.0655
^Corrected for ties

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Haven, 187 pp.

BIOGRAPHICAL SKETCH
Leo G. Nico was bom on December 25, 1954, to Frank and Teresa Nico in East
St Louis, Illinois. He grew up in a small Illinois town where he developed an early
interest in biology and natural history. One year after graduating from high school, he
entered Southern Illinois University at Edwardsville (SIUE), majoring in biology. He was
awarded a Bachelor of Arts degree with honors in 1979. Forsaking plans to enter the
Peace Corps, he became a graduate student at SIUE to work under Dr. Jamie E.
Thomerson on the ecology and natural history of South American annual fishes. Field
work for his master's degree was done in the Orinoco River basin of Venezuela during the
rainy season of 1980. Concurrent with his graduate studies, he did a study of the breeding
birds of the lower Kaskaskia River, under a contract with the Illinois Department of
Conservation. He also held a temporary position with the U.S. Army Corps of Engineers
as a fishery biologist in their Environmental Analysis Section. After receiving his M.Sc.
degree in 1982, he worked one more year for the Federal government, still harboring plans
to work in the tropics as a Peace Corps volunteer. But, once again, his plans were
curtailed upon receiving an invitation from Professor Donald Taphom to help him in a
study of the fishes of the Apure River basin in Venezuela. As a result, he spent from
November 1983 to July 1985 in Venezuela.
In 1985, he moved to Gainesville after being accepted into the Ph.D. program in the
Department of Zoology at the University of Florida. As part of his graduate studies, he did
additional field work in South America, spending two months in Brazil in 1986, and
approximately two years of field work in Venezuela from 1988 tol991.
209

I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
j.
Horst
Professor of Zoology
O. Schwassmann, Chair
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Carter R. Gilbert, C
Professor of Zoolo
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Martha L. Crump
Professor of Zoology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Frank G. Nordlie
Professor of Zoology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
N C-. >
Nigel J. H. 'mith
Professor of Geography
This dissertation was submitted to the Graduate Faculty of the Department of
Zoology in the College of Liberal Arts and Sciences and to the Graduate School and was
accepted as partial fulfillment of the requirements for the degree of Doctor of Philosophy.
December, 1991
Dean, Graduate School
V-\



6
areas of tropical South America (Terborgh 1983, Goulding et al. 1988, Janson and
Emmons 1990), or information gleaned from botanical exploration of the upper Orinoco
(B. Stergios, personal communication), suggest that such habitats make a wide variety and
abundance of fruits and seeds available to fishes during most of the year (Goulding 1980,
Goulding et al. 1988). Even though species diversity is often high in the upper Orinoco,
our collections made with a variety of fishing gear indicate that fish biomass in tropical
forest regions is generally lower than in the low Llanos.
If present ecological conditions are important, environment should strongly
influence both species composition and trophic ecology of piranha assemblages in
particular regions. Accordingly, comparisons of piranhas from the more heavily forested
upper Orinoco basin with those from the open savannas or low Llanos were made to
address the following questions: (1) Do the same species of piranhas occur in both
savanna and forested regions? (2) Do diets differ, and, if so, are fish from populations in
forested habitats significantly more herbivorous than their savanna counterparts? (3) Do
ontogenetic shifts in diet occur and, if so, how do they compare among species and do they
correlate with regional environments? (4) Because gut length is often an indicator of
natural diet in vertebrates (i.e., longer in herbivores), is intestinal length of piranhas and
other serrasalmine fishes correlated with diet? (5) What are the nutritional benefits
associated with different diets or food preferences (e.g., scale- or fin-eating versus flesh
eating)? (6) How do diets of piranhas compare with other serrasalmine species? (7) What
is the relationship between piranha ecology and serrasalmine phylogeny?
The comparative approach is useful in helping us understand aspects of the
evolution and adaptations of closely related species (Clutton-Brock and Harvey 1984,
Huey and Bennett 1986). Recent comparative studies in tropical vertebrate ecology have
focused on birds (Schluter 1988), mammals (Terborgh 1983), and reptiles and amphibians
(Duellman 1990). An objective in many comparative studies is discovery of evolutionary
trends in morphological and behavioral adaptations to different environments, thereby


173
identify a prey species based only on fin fragments or scales found during examination of
stomach contents. However, my observations of feeding by captive fishes indicate that fin-
eating and scale-eating serrasalmine fishes are capable of successfully attacking individuals
of many fish species. Fin-eating piranhas use several basic tactics to approach prey fish,
for instance ambushing, stalking, and active chase. Although particular species appear to
be better suited morphologically for employing one tactic over another (e.g., the stream
lined S. elongatus for active pursuit; narrow deep-bodied species such as S. altuvei for
stalking) (Nico and Taphom 1988, Sazima and Machado 1990), my observations indicate
that the particular tactic used by individuals of a given species can vary widely and seems to
depend on several factors, for example, the amount and type of cover, the density and type
of prey fish, and water clarity. In nature, juvenile Serrasalmns irritans-use aggressive
mimicry to approach other fish (Nico and Taphom 1986, 1988). However, in large
outdoor tanks I have seen individuals use both ambush and pursuit. In the first case, an
individual hides among rocks and ambushes passing fish; in other instances they leave their
hideaway and actively pursue fish in open water over distances of more than a meter. I
have kept a young wild-caught Pygopristis denticulatus for nearly a year in a large
aquarium; it slowly stalks novel prey fish, but it will immediately chase small fish that are
not novel. Based on the size of fins in their stomachs, small juveniles in nature attack fish
that are about their own size; however, large fin-eating piranhas will prey on the fins of fish
much larger than themselves, for example the pimelodid catfishes Brachyplatystoma and
Phractocephalus.
In the Orinoco and elsewhere, studies are needed to determine to what extent
herbivorous fishes specialize on particular seeds or leaves. The method of diet analysis
used here, scoring plant foods as masticated seeds versus other plant material, gives low
diet width values for herbivorous fishes that may be misleading. Goulding (1980, 1983)
and Goulding et al. (1988) reported that herbivorous fishes in the Amazon River basin
exploit a wide range of plant species, but they seem to prefer fruits and seeds of a few


145
O)
c
0)
-D
CC
~o
c
ce
-i '
en
O)
c
a>
0)
c
c
ce
(D
3-
1 -
0
Pst
'Mys
Seg
PsP0
My O
Mys o
Mag Md H
Mya
O O
Pst Pyp
Smss
SrO
Smd _
SaC
a Pn
Sir Sr
o.Jkk "
' Pn
Sel
Ocm
Osm
'Cm
1 Pyp
Standard length >80 mm
o Upper Orinoco
B Llanos
r i i i i 1 i i 1 i i 1 i
0 10 20 30 40 50 60 70 80
% Volume plant material in diet
90 100
Fig. 6-10. Scatter diagram showing relationship between mean intestine length/standard
length (not adjusted for SL) and percent volume of plant material in diet for
selected serrasalmine fish (>80 mm SL). Piranha species: Pyp = Pygopristis
denticulatus', Sa = Serrasalmus altuvei; Seg = S. cf. dgenmannv, Sel = S.
elongatus; Sir = S. irritans: Sm S. manueli; Smd = S. medinai; Sr = S.
rhombeus', others: Cm Catoprion ment-, Mag = Metynnis argenteiis\
Mya = Myleus asterias-, Mys = M. schomburgki; Myt = M. torquatus; and
Md = Mylossoma duriventris.


206
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1253.


42
drainages. Work in any one drainage was usually limited to one part of the year, either
during the high or low water period.
Lowland habitats sampled in the upper Orinoco were channel borders and beaches
of rivers, streams, side channels, old meanders and other back waters, including isolated
floodplain lakes, as well as inundated forest. Elevations ranged from 90 to about 240 m
above sea level. Collection sites and sampling dates were as follows: (1) Guayapo and
Sipapo rivers, from 12 May to 7 June, 1989; (2) lower Ventuari River, including its
tributaries the Yureba, Parti, Asisa, Guapuch ( = Picure), Marueta rivers and the caos
Cucuritl, Moriche and Tabi-Tabi, from 17 September to 16 October, 1989; (3) Atabapo
River, including its tributaries the Atacavi and Temi rivers and the caos Patacame,
Cuchakn, Bocachico, and Chimita, from 23 October to 17 November, 1989; (4) Ocamo,
Putaco, Padamo, and Matacuni rivers, and the caos Jayuwapuei, Jenita, Maveti, and
Yaraca-bawei, including the upper Orinoco River main channel above its confluence with
the Ventuari, from 16 January to 16 February, 1990; and (5) Mavaca River, its tributary
Cao Mavaquita ( = Cao Hauyapiwei), and the upper Orinoco main channel, from 18
January to 20 February, 1991. A total of 200 fish collections representing 180 individual
sites was made in this region, resulting in over 18,000 specimens, of which 500 were
serrasalmine fishes.
Evaluation of Habitats
A variety of habitat parameters was recorded whenever possible for most collection
sites. Qualitative and quantitative estimates were as follows: (1) season (wet, dry, or
transitional); (2) water type (clear, black, white, or combination); (3) water level (isolated
pools, continuous in bank, bank full, or flood condition); (4) watershed topography (level,
moderately rolling, rolling, mountains); (5) stream gradient (flat, slight, moderate, or >30
degrees); (6) land use (natural, cattle, agricultural, or developed); (7) major terrestrial


30
The flat lowlands or peneplains of southern Venezuela are dominated by wet
tropical forests (Figs. 2-2 and 2-4). The altitude of these lowland regions in the upper
Orinoco range from 100 to 500 m, with most less than 200 m (Huber and Wurdack 1984).
Similar to the situation described for Amazonian lowlands (Prance 1979, Kubitski 1989),
many lowland forests in the upper Orinoco are inundated by the annual high water, with
some sites being permanently waterlogged. Aerial photos of the lowlands reveal a history
of streams meandering across their adjacent floodplains. Large and small streams, cutoffs,
and oxbows abound in many of the drainages (e.g., Mavaca River) and, similar to the low
Llanos, interconnections with adjacent drainages within the upper Orinoco are common
during high water. However, aquatic vegetation in the region is much more sparse and
localized in comparison to the low Llanos. Although a few backwaters are choked with
submergent and emergent vegetation, most floodplain lakes in the upper Orinoco have few
or no aquatic plants. The reasons for such scarcity are likely related to high shade,
unconsolidated bottoms, and few available nutrients in the water or substrate. In flowing
waters there are often small bands of flooded grasses along bank edges of inner bends.
The fish fauna of the upper Orinoco is the least known in all of Venezuela, largely because
of the inaccessibility of the region. With very few roads, modes of transportation within
the area are limited almost exclusively to small and medium-sized boats and small planes.
Savannas and Forests during the Quaternary
Both tropical forest and tropical non-forest vegetation originated in the Cretaceous
and Tertiary, about 100 million years ago, periods when world climates were apparently
rather stable and tropical conditions much more widespread (Whitmore and Prance 1987).
However, during the last two million years there have been periodic and dramatic
fluctuations in the distribution of savannas versus forest environments in northern South


153
Wuycheck 1971, Davis and Warren 1971, Bell 1990). The lipid and energy content of
insects is much higher than that of other animal food items eaten by piranhas.
Microcrustaceans, similar to insects, also yield over 20 kJ/g of dry matter (Cummins and
Wuycheck 1971).
The small juveniles (usually <40 mm SL) of several piranhas were found to feed on
aquatic insects, mostly ephemeropterans and chironomid larvae. Pygocentrus caribe,
which feeds heavily on aquatic insects and some fish flesh when young, has a faster
growth rate than other piranhas, such as Serrasalmns irritans, which feed heavily on fins as
juveniles (Nico, unpublished data).
Plant Matter
There are, to my knowledge, no data available on the chemical composition of the
seeds, fruits, and leaves eaten by serrasalmine fishes. As a rule, plant matter tends to be
high in carbohydrates whereas animal matter is high in proteins. Nevertheless, nutrient and
energy content varies considerably among different plant species and different plant parts.
Plants typically accumulate nutrients and energy reserves in seeds and fruits. Seeds are
particularly rich in lipids in the form of oils. My study suggests that piranhas prefer seeds
and hard fruits over other plant parts (e.g., fleshy fruit, leaves, flowers). Goulding et al.
(1988) felt that herbivorous fishes prefer fruits and seeds to leaves because leaves are less
nutritious and frequently contain toxic compounds.
Okeyo (1989) compiled information on the composition of foods found in
alimentary tracts of a wide range of herbivorous fishes showing that aquatic plants vary
greatly in terms of ash, protein, lipid, carbohydrate, and energy content. Previous studies
investigating nutrient quality of plant matter as it relates to animal diets in the neotropics
have focused primarily on mammals and birds. Snow (1981) presented food values of
fruits from 20 tropical and subtropical plant species, reporting protein, fat, and


175
Ecomorpholoeical Correlates
Ecomorphology examines correlations between organism morphology and selective
demands of its external environment Keast and Webb (1966) were among the first to look
closely at possible relationships between fish trophic morphology and fish diets.
Piranhas have interspecific variation in body height, body width, shape of snout
and maximum size; general body shape also changes dramatically during growth in several
species, for example in Serrasalmus rhombeus as described and figured by Gry (1972).
Nico and Taphom (1988) thought that piranhas with sharp snouts (Serrasalmus irritaos and
S. elongatus) were more adapted for nipping fins or taking scales but found that even a few
species with somewhat blunt snouts (S. medinai and Pristobrycon strioiatus) fed heavily on
fins. Sazima and Machado (1990) also suggested that particular piranha body
morphologies were associated with particular predatory tactics: the low profile and
powerful tail of Pygocentrus nattered for giving short chase, and the high fins and narrow
body (in addition to a greenish body color) of the fin-eating S. marginatus for hiding in
vegetation while stalking its prey.
Particular types of morphology or behavior can preadapt animals to their current
ecological niches. For example, Futuyma (1986:424) described how a New Zealand
parrot, the kea (Nestor notabilis), uses its beak to rip through the skin of sheep and feed on
the fat beneath. The beak is similar to that of normal seed- and fruit-eating parrots, but its
form presumably preadapted the kea to invade the sheep-eating niche. Piranhas have a
single row of sharp, somewhat triangular teeth in both jaws used for rapid puncture and
shearing. Dental morphologies exhibit only slight variation among species, and are
sufficiently unspecialized that individuals are able to exploit a broad range of food. As
such, the unique dentition and strong jaw musculature of piranhas preadapts them for
feeding on hard seeds and fruits. This statement presumes, possibly incorrectly, that
camivory is the "primitive" ecological character state within piranhas.


Table 5-6. Food items of Serrasalmus elongatus from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence (nonempty stomachs); %D = percent dominance; and %Va = percent adjusted volume. N = 42.
Size class (mm, SL)
Number examined
Number empty
Food items
II (20-39)
3
0
%Q %D %Va
Ill (40-79)
13
0
%0 %D %Va
IV (80-159)
21
1
%0 %D %Va
V(>160)
5
0
%0 %D %Va
Plant material
-
-
23.1
-
-
30.0
5.0
4.5
40.0
-
-
Decapoda
-
-
-
-
-
5.0
5.0
2.3
-
-
-
Other invertebrates
33.3
-
-
-
-
15.0
5.0
4.5
-
-
-
Small whole fish
-
-
-
-
-
10.0
10.0
9.1
20.0
-
-
Fish flesh
-
-
15.4
12.5
15.6
35.0
30.0
40.9
80.0
40.0
25.0
Fish fins
100.0
100.0 100.0
76.9
50.0
57.8
.40.0
20.0
18.2
40.0
20.0
37.5
Fish scales
-
-
84.6
37.5
26.6
50.0
20.0
18.2
80.0
40.0
37.5
Other
-
-
-
-
-
5.0
5.0
2.3
-
-
-
OO
Os


205
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usually predictable according to species. For the most part, occasional bits of plant material
in the stomachs of typically carnivorous species were considered the result of accidental
ingestion when these fish were attacking prey fish. However, underwater observations in
the Pantanal of Brazil reported by Sazima and Machado (1990) suggested that primarily
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leaves of aquatic plants while scanning for aquatic insects and small crustaceans.
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conditions is presented in Figure 8-1. This model shows trends and not absolute values.
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carnivorous and herbivorous piranhas to be most different when conditions provide for a
roughly equal amount of plant (i.e., mainly seeds) and animal food (i.e., mainly fish), or
when neither type of food is in limited supply. The vertical broken line of Figure 8-1
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likely to be associated either with temporal changes, such as from highwater to lowwater
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community at Cocha Cashu Biological Station, Manu National Park, Peru. Pages
314-338 in A. H. Gentry, editor. Four neotropical forests. Yale University Press,
New Haven, Conneticutt.
Jgu, M., E. L. M. Leao, and G. M. dos Santos. 1991. Serrasalmus compressus. une
espece nouvelle du Rio Madeira, Amazonie (Pisces: Serrasalmidae). Icthyological
Explorations of Freshwaters 2(2):97-108.
Jgu, M., and G. M. dos Santos. 1987. Sur la prsence de Serrasalmus altuvei Ramirez,
1965 (Pisces, Serrasalmidae) dans le bas Rio Negro (Amazonas, Brsil). Cybium
11:47-54.
Jgu, M.. and G. M. dos Santos. 1988. Le genre Serrasalmus (Pisces, Serrasalmidae)
dans le bas Tocantins (Brsil, Par), avec la description d'une espece nouvelle, S.
geryi, du bassin Araguaia-Tocantins. Rev. Hydrobiol. Trop. 21(3):239-274.
Junk, W. 1977. Tecnologa do pescado: composi£ao qumica do pescado. Relatrio
Anual do ENPA. Instituto Nacional de Pesquisas da Amazonia, Manaus.


37
line were ail occasionally effective in capturing species considered uncommon in a
particular drainage or region.
To reduce the risk of missing uncommon or rare species in upper Orinoco
drainages, where most sampling was limited to relatively short periods, I supplemented my
own samples with collections of others. In the field, I recorded the catch of hired
fishermen and Indians, including the daily hook-and-line collections of camp workers.
Field Site Locations and Sampling Periods
Nine drainages of the Orinoco River basin in Venezuela were sampled during the
present study, three in the low Llanos and six in the upper Orinoco (Fig. 3-1).
Low Llanos or Savanna Sites
Three major drainages were studied in the low Llanos of Apure State: the Apure,
Cinaruco, and Capanaparo rivers (Fig. 3-2). Principal habitats sampled were rivers,
streams, natural and artificial lagoons and pools, and flooded savanna. The Apure drainage
was the only site where long-term research on piranhas was carried out.
Apure Drainage. Almost all fieldwork was done in the Cao Caicara watershed of
the Apure drainage in and around the Femando Corrales research station and ranch of the
Universidad de Los Llanos (UNELLEZ) (0725'50"N, 693530"W). This area is
bordered by Cao Caicara, its tributary Cao Maporal, and a smaller stream, Cao
Guaritico. I made periodic samples in the Cao Caicara study area during December 1983;
January, March, May, July, September, and November 1984; and March, April, and May
1985; these were followed by samples taken during August 1988, March, April, and
December 1989, and January, March, and May 1990. I also examined material taken


CHAPTER 4
COMPOSITION OF PIRANHA ASSEMBLAGES
In this chapter I compare the species composition of piranha assemblages from the
low Llanos to those from the upper Orinoco. I also examine and compare species
composition and richness among the nine drainages sampled, and present possible habitat
correlates. Little has been published on the distribution of Orinoco River fishes, with the
upper Orinoco being that part of the basin least explored ichthyologically. Because
sampling effort was not equal among all the drainages, I supplemented my data with
information from museum collections and published records. Although additional
collecting will likely add a few species to faunal lists for several of the drainages, the data
presented represent a first attempt at understanding piranha distribution patterns and habitat
preferences.
Figure 4-1 is a schematic representation showing the relative distances among
drainages in relation to their confluence with the main channel of the Orinoco River.
Table 4-1 is based on my samples supplemented by museum material, and shows the
species composition by region and drainage. A total of eleven piranha species were taken
from the two regions studied. Since 1979, ten species have been collected from the low
Llanos of Apure State, whereas my 1989-1991 samples indicate that at least eight species
occur in the upper Orinoco of the Amazon Territory of Venezuela. Seven species were
widely distributed and inhabited both regions. The Coefficient of Biogeographic
Resemblance (CBR) value comparing piranha species composition between the low Llanos
and the upper Orinoco was 0.78.
Piranha assemblages in five of the six upper Orinoco drainages were numerically
dominated by either S. rhombeus or S. manueli, or both. The exception was the Mavaca
57


49
Analysis of Diets
In order to analyze diets and document ontogenetic shifts in feeding, sampled fishes
were divided into five size classes: Group I) 10-19 mm SL small juveniles; Group II) 20-'
39 mm SL; Group IQ) 40-79 mm SL; Group IV) 80-159 mm SL; and Group V) >160 mm
SL. Several species were not represented by all size classes.
During the study, more than 2,000 serrasalmine fishes were captured; total number
of specimens examined for stomach contents was 1,538 from the low Llanos and 393 from
the upper Orinoco. Standard length (SL) of each specimen was measured to the nearest
mm. Although a few of the largest fish were dissected and examined in the field, most
specimens were preserved after capture and dissected later in the laboratory to determine
stomach contents. I examined stomach contents and recorded frequency of occurrence
(O), number (N), and dominance by bulk (D) for each food item. I also recorded volume
(V) of food items found in stomachs of fishes taken in the field after 1986. Small food
organisms were counted using a Ward counting wheel under 25X magnification. Volume
was determined by water displacement using appropriately-sized graduated cylinders.
Volumes of smaller items were calculated by measuring dimensions with Vernier calipers
or by examination under a dissecting microscope and comparison with known volumes.
An estimate of relative stomach fullness was made using scores ranging from 0 (empty) to
3 (if full, or almost full) (Thomerson and Wooldridge 1970, Nico and Taphom 1988).
For specimens collected in the Apure River drainage before 1986,1 estimated
volume using a point system, referred to as adjusted volume (Va), and derived from D and
stomach fullness (Nico and Taphom 1988). That is, only the dominant food categories of
a given stomach were included and each was assigned the fullness points (1-3) for that
stomach. If two food items in a single stomach were of about equal volume, each received
half the fullness value. Thus, %Va = total fullness points for each food category as a
percentage of all fullness points, and can be shown as:


Pc
Pst
Sel


190
Mvleus schomburgkii
Llanos: Capanaparo River drainage: 1989: MCNG 20067 (2-2); MCNG 20086
(3-3). Cinaruco River drainage: 1989: MCNG 20173 (1-1). Riecito River drainage:
1982: MCNG 6209 (2-2).
Upper Orinoco: Orinoco main stem: 1991: MCNG 25399 (1-1). Ventuari River
drainage: 1989: MCNG 22885 (2-2). Atabapo River drainage: LN 89-162 (2-2). Ocamo
River drainage: 1990: MCNG 22407 (1-1); Mavaca River drainage: MCNG 25401 (1-1)
Casiquiare: 1985: MCNG 12354 (1-1).
My lens torquatus
Upper Orinoco: Orinoco main stem: 1991: MCNG 25398 (2-2); LN 91-3 (4-4).
Ocamo River drainage: 1990: MCNG 23378 (1-1). Ventuari River drainage: 1989:
MCNG 22884 (4-3). Mavaca River drainage: 1991: MCNG 25423 (14-14); UF 85213
(2-2).
My leus sp.
Upper Orinoco: Atabapo River drainage: 1989: LN 89-162 (2-2).
Mvlossoma duriventrus.
Llanos: Apure River drainage: 1981: MCNG 2091 (1-1). 1984: MCNG 17154
(1-1).
Piaractus brachypomus
Upper Orinoco: Sipapo River drainage: 1989: LN 89-63 (1-1).


94
6n
5-
S2 4-
*'
TD
CO
CD
0)
Q 2-
1 -

20-39 mm
fl
40-79 mm

80-159 mm

>160 mm
i! /
fSf /
i /
m/
Ms
ms
l
P. caribe S. rtiombeus S. elongatus S. irritans S. medin S. altuvei P. striolalus C. ment
Species
Fig. 5-4. Diet breadths estimated for eight piranha species, by size class, from the Cao
Caicara area of the low Llanos, Apure River drainage, Orinoco River basin,
Venezuela. Diet breadth calculated using formula of Levins (1968). Most
species not represented in all size classes. Size ranges are standard length.


40
between 1979 and 1984, which included monthly samples of a one-year biomass study of
the area in 1982-1983 (see Taphom and Lilyestrom 1984). A total of about two hundred
fish collections were made in the Apure River drainage in caos Caicara and Maporal and
their adjacent floodplains from 1979 to 1990.
Cinaruco and Capanaparo drainages. I examined collections made by others from
the lower Cinaruco and Capanaparo rivers and their floodplains. Most sites sampled were
within 50 km of the north-to-south road joining San Femando de Apure with Puerto Paez,
a route roughly following 6730' W longitude. Samples were taken in January 1982,
December 1986, January 1987, and March and April 1989. The 1989 collections were the
result of a fish inventory of the two drainages made by D. C. Taphom and A. Barbarino
using seines, cast nets, and hook and line. Overall, sites collected were the main channels
and near-shore areas of the two rivers, as well as Laguna Larga of the Cinaruco River, and
Cao La Pica and Laguna Brava of the Capanaparo drainage.
Upper Orinoco or Forest Sites
Six major drainages in the upper Orinoco, Amazon Territory of Venezuela, were
sampled for analysis of piranha populations from forested regions (Fig. 3-3). These
included the Sipapo, Atabapo, Ventuari, Matacuni, Ocamo, and Mavaca drainages, as well
as the main channel of the Orinoco River. I collected fishes and evaluated habitats during
five expeditions, between early 1989 and 1991, as part of a resource inventory of southern
Venezuela in association with the mineral consortium CVG-TECMIN (Corporacin
Venezolana Guyana Tcnica Minera). Data on serrasalmine fishes from the region are
based on intensive sampling of many sites over relatively short periods of time. Each
expedition lasted between 25 and 40 field days and covered a different drainage or set of


195
Mann-Whitnev U Test
Following are the results of one-tailed Mann-Whitney U tests comparing the degree
of herbivory of piranha populations from the low Llanos to those from the upper Orinoco.
Comparisons are made using results of percent adjusted volume (%Va), percent dominance
(%D), and percent frequency of occurrence (%0), based on specimens > 80 mm SL
(combining information on the two largest size classes for each species, 80-159 mm SL
and > 160 mm SL). Specimens with empty stomachs were not figured into the
calculations. Number of specimens by species is given in Table 6-9.
Table B-8. Percent adjusted volume (%Va) of plant material in piranhas (> 80 mm SL) as
associated with the low Llanos and upper Orinoco.
Low Llanos
Upper Orinoco
Taxon
%Va
%Va
Pristobrycon sp.
-
100.0
Pristobrycon striolatus
41.0
73.0
Pygocentrus caribe
6.7
11.0
Pygopristis denticulatus
50.0
100.0
Serrasalmus altuvei
0
0
S. cf. eigenmanni
25.0
70.0
S. manueli
0
26.0
S. rhombeus
11.9
2.0
S. elongatus
3.6
-
S. irritans
5.0
-
S. medinai
2.9
-


197
Table B-10. Percent frequency of occurrence (%0) of plant material in piranhas (> 80
mm SL) as associated with the low Llanos and upper Orinoco.
Low Llanos
Upper Orinoco
Taxon
%0
%0
Pristobrycon sp.
-
100.0
Pristobrycon striolatus
80.0
100.0
Pygocentnis caribe
34.1
50.0
Pygopristis denticulatus
66.7
100.0
Serrasalmus altuvei
28.6
22.2
S. cf. eigenmanni
66.7
81.8
S. manueli
8.3
43.2
S. rhombeus
25.0
15.5
S. elongatus
32.0
-
S. irritaos
18.6
-
S. medinai
26.0
-
Table B-l 1. One-tailed Mann-Whitney U test results testing the prediction that forest
populations fed more on plant material than their savanna counterparts. Ni = number of
species from upper Orinoco: N2 = number of species from low Llanos.
Diet Measure
Ni
n2
u
Mean
SD*
z value*
P
%Va
8
10
23
40
11.22556
- 1.514402
0.0655
%D
8
10
22.5
40
11.21973
- 1.559752
0.0594
%0
8
10
23
40
11.21556
- 1.514402
0.0655
^Corrected for ties


52
overlap values (Greene and Jaksic 1983), bias increases as the number of resource
categories used increases or is large (Ricklefs and Lau 1980, Smith and Zaret 1982, Krebs
1989). Overlap and breadth indices also give somewhat different results depending on the
methods used to tabulate dietary components, for example, percentages based on total food
volume, weight, frequency of occurrence, or food item number (Wallace 1981). An
additional problem implicit in all overlap and breadth measurements is that the investigator
may recognize resource categories that animals do not For instance, Goulding et al.
(1988:52) suggested that .Amazonian frugivorous fishes "select their preferred fruits and
seeds at what taxonomically are referred to as genera" rather than at the species level.
Conversely, organisms may distinguish resources lumped together by human observers
(Ludwig and Reynolds 1988, Krebs 1989). Finally, most overlap and width indices are
based on the relative use of different resources, without accounting for their relative
availabilities. However, resource availability is difficult to assess and therefore rarely
measured. Those indices that do incorporate some estimate of food availability into their
equations are generally less simple to interpret and more variable between sites (Schluter
1988). Abrams (1980) and Wallace (1981) recommended the Schoener Index as the best
of the measures of niche overlap when available resources to the organism have not been
quantified. Krebs (1989:304-306), referencing Wolda (1981), regarded this measure as
one of the better quantitative similarity coefficients available, showing that it is relatively
little affected by sample size and number of species (i.e., resources states).
Because percentage of occurrence and percentage of total number of food items tend
to over-emphasize the importance of small food items, I used proportions based on total
food volume for calculating diet widths and overlaps. Using food volume introduces the
possible bias that a large prey item in a single large piranha might overshadow all other
items when pooling stomach contents data. However, this problem is overcome to a large
extent by dividing fish into different size classes and treating each size class as a separate
"trophic unit" (sensu Stoner and Livingston 1984).


APPENDIX B
STATISTICAL ANALYSES
Analysis of Covariance (ANCOVA)
Following are the results of ANCOVA comparing intestine length and standard
length of different combinations of piranha species. Analysis carried out using Type III
sum of squares of SuperANOVA computer program on a Macintosh SE/30 computer.
Data were not transformed.
Table B-l. ANCOVA of standard length (SL), with intestine length (EL) as dependent
variable, comparing three piranha species from upper Orinoco: Serrasalmus manueli (n =
60), S. rhombeus (n = 70), and S. cf. eigenmanni (n = 32).
Source
df
Sum of
squares
Mean
squares
F-value
P-Value
Species
2
6863.142
3431.571
1.570
0.2112
SL
1
887772.922
887772.922
406.273
0.0001
Species x SL
2
63119.741
31559.870
14.443
0.0001*
Residual
156
340885.717
2185.165
^Conclude that slopes of regression lines are different.
191


TROPHIC ECOLOGY OF PIRANHAS (CHARACIDAE: S ERRAS ALMINAE)
FROM SAVANNA AND FOREST REGIONS
IN THE ORINOCO RIVER BASIN OF VENEZUELA
By
LEO G. NICO
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA


132
in captivity (Pygopristis denticulatus, another herbivorous piranha, is extremely rare in the
Apure River drainage and has not been taken in Cao Caicara).
Fin eating was also common among juveniles in the Llanos. In the Cao Caicara
area, the young of at least five of the seven piranha species present (i.e, Serrasalmus
rhombeus, S. elongatiis, S. irritans, S. medinai, and Pristobrycon striolatus) fed heavily
on fins. The smallest juveniles (10-19 mm SL) examined from the two regions are
compared in Figure 6-3. Small juvenile Pygocentrus caribe from the low Llanos fed on
small aquatic insects and microcrustaceans in roughly equal amounts (Fig. 6-3).
The Cinaruco and Capanaparo River Drainages
Long-term research in the Cao Caicara area suggested that savanna populations of
piranhas do not depend on plant material. However, my later study of fishes from savanna
areas where gallery forests are more extensive suggest that differences in trophic patterns
between the upper Orinoco and low Llanos are not always distinct. Although uncommon,
three of the four seed-eating piranhas found in the upper Orinoco (i.e., Pristobrycon
striolatus and Pygopristis denticulatus, Serrasalmus cf. eigenmanni) also occur in the
Cinaruco or Capanaparo river drainages of the low Llanos. Based on a limited number of
specimens taken during the dry season, stomach content analysis indicated adult piranhas
of the herbivorous species feed on plant material when available in savanna situations
(Fig.6-7). A description of their diets follows.
Pristobrycon striolatus was collected in both the Cinaruco and Capanaparo rivers.
Two juveniles (42 and 44 mm SL) contained mostly fish fins (80% of total volume); other
items included some plant material (leaf fragment and small stem) and a few scales. Larger
P. striolatus from these two rivers were seed predators (%0-%D-%V): Group IV (n = 8, 1
empty) masticated seeds (85.7-57.1-64.8), other invertebrates (28.6-0-2.0), fish fins
(28.6-0-5.4), fish scales (57.1-42.6-21.0), other (14.3-0-6.8).


106
manueli (>160 mm SL) preyed heavily on fishes, but plant material was occasionally taken
in mass, with plant matter occurring in 12 of 42 Group V stomachs and accounting for
25% of total food volume. Five of six adult S. manueli (>160 mm SL), caught with hook.
and line in the Sipapo River during high water, contained large amounts of masticated
seeds, primarily endocarp, and the sixth was packed with small flowers of a Lecythidaceae,
possibly Gustavia sp. Seven specimens from other forest sites had fed on leaf fragments
and pieces of fruit (exocarp and mesocarp); some of the fruit was identified as the palm
Bactris gasipaes (Palmae). Prey fishes and other items identified from stomachs are given
in Table 6-1. IL/SL ranged from 0.7 for a 52-mm SL juvenile, to 2.2 for a 250-mm SL
adult.
In addition to the 78 large specimens, I examined five small Serrasalmus (<40 mm
SL) that I tentatively identified as juveniles of S. manueli. These small fish, together with
young of Pristobrycon striolatus, were taken from a clump of macrophytes near the banks
of the lower Yureba River, a blackwater tributary of the Ventuari. All five fish had a
prominent black spot on the dorsal fin and well-developed ectopterygoid teeth. The
stomach of a single individual less than 20 mm SL (Group I) contained aquatic insects
(Fig. 6-3), while those of four Group II individuals were packed with fins of other small
fishes (Fig. 6-3, Table 6-3). IL/SL of these small juveniles was less than 1.0.
Serrasalmus cf. eigenmanni Norman 1928
Serrasalmus cf. eigenmanni was the third most common piranha in samples from
the upper Orinoco. It was the most abundant piranha taken in the Mavaca River drainage,
was relatively common in the Ocamo and Matacuni drainages, and a single individual was
taken from the Paru River of the lower Ventuari. All of the above are basically whitewater
rivers. Serrasalmus cf. eigenmanni (Fig. 6-1) is a medium-sized piranha, the largest
specimens collected being two gravid females of 180 mm SL. It has a somewhat blunt
snout, and in terms of body shape, most resembles S. medinai, a species found in the


BIOGRAPHICAL SKETCH
Leo G. Nico was bom on December 25, 1954, to Frank and Teresa Nico in East
St Louis, Illinois. He grew up in a small Illinois town where he developed an early
interest in biology and natural history. One year after graduating from high school, he
entered Southern Illinois University at Edwardsville (SIUE), majoring in biology. He was
awarded a Bachelor of Arts degree with honors in 1979. Forsaking plans to enter the
Peace Corps, he became a graduate student at SIUE to work under Dr. Jamie E.
Thomerson on the ecology and natural history of South American annual fishes. Field
work for his master's degree was done in the Orinoco River basin of Venezuela during the
rainy season of 1980. Concurrent with his graduate studies, he did a study of the breeding
birds of the lower Kaskaskia River, under a contract with the Illinois Department of
Conservation. He also held a temporary position with the U.S. Army Corps of Engineers
as a fishery biologist in their Environmental Analysis Section. After receiving his M.Sc.
degree in 1982, he worked one more year for the Federal government, still harboring plans
to work in the tropics as a Peace Corps volunteer. But, once again, his plans were
curtailed upon receiving an invitation from Professor Donald Taphom to help him in a
study of the fishes of the Apure River basin in Venezuela. As a result, he spent from
November 1983 to July 1985 in Venezuela.
In 1985, he moved to Gainesville after being accepted into the Ph.D. program in the
Department of Zoology at the University of Florida. As part of his graduate studies, he did
additional field work in South America, spending two months in Brazil in 1986, and
approximately two years of field work in Venezuela from 1988 tol991.
209


Piscivores O M S3
Fin eaters (jv) D Hi Hi Hi
Fin eaters (ad) CD O CD S3
Scale eaters ES Bl CU
Herbivores M M M'm Hi S3
Long Intestine £ # # # O O
Piaractus Mylossoma Myleus Metynnis Catoprion Pygopristls Pygocentrus Prlstobrycon Serrasatmus


160
Serrasalmus altuvei has been found recently in the Rio Negro of the Amazon basin where,
as in the Orinoco, it is also considered quite rare (Jgu and Santos 1987, Jgu et al. 1991).
Explanations for the noted natural rarity of these species may be found, perhaps, in their
having more specific habitat requirements (see Gilbert 1980). Some of the more
uncommon species of piranhas seem to have somewhat specialized diets as adults, and a
narrow food preference might account for their low numbers. For example, adult S.
altuvei are basically fin eaters, and some of the other rare piranha species are mainly
herbivorous. (See later discussion of dietary specialization).
Species closely related to piranhas (e.g., Colossoma, Piaractus, Mylossoma) are
known to make long seasonal migrations of many hundreds of kilometers for purposes of
tracking food resources or for reproduction (Lowe-McConnell 1964, Goulding 1980). In
contrast, migratory movements by piranhas seem limited to lateral movements across the
floodplain and to short seasonal journeys between more permanent waters (large streams
and lagoons) and their floodplains. Field researchers have yet to observe piranhas
spawning in the wild or even identify precisely where eggs are deposited (but see Lowe-
McConnell 1964). In all likelihood, spawning sites are located in aquatic vegetation. My
unpublished data on the reproductive condition of adults and monthly differences in body
size indicate that spawning takes place mainly during the early part of the rainy season.
Small juvenile piranhas are always found in flooded vegetation and it has been shown that
they use macrophytes for both shelter from predators and as a foraging area (Menezes et al.
1981, Sazima and Zamprogno 1985, Nico and Taphom 1988, Nico 1990, this study). The
upper Orinoco has few habitats with large areas of aquatic macrophytes and this scarcity
may limit piranha numbers in that region.
In addition to regional differences, differences in species composition and
abundance among habitats within regions also seem to be associated, at least in part, with
differences in types and availability of food resources. Perhaps the clearest example is that
from the Llanos. Earlier work in the Cao Caicara area suggests that all Orinoco savanna


Fig. 8-2. Diets and intestine length mapped onto the proposed phylogeny of Machado-Allison (1985) for genera of the subfamily
Serrasalminae. The four piranha genera are highlighted. Orinoco taxa not examined during this study are not included
in tree. Jv = juvenile trait; ad = adult trait


176
Other morphological features related to feeding, for instance intestine length, show
much more variation among the different piranha species. Previous investigators have
noted that carnivorous fish (like many terrestrial vertebrates) have relatively shorter
intestines than herbivorous fish (see Ribble and Smith 1983), suggesting a correlation
between length of the gastrointestinal tract and the feeding ecology of a species (but see
Smith 1989). A longer intestinal tract provides a greater surface area for digestion and
absorption of difficult to digest plant material. Several researchers have even reported large
intraspecific differences in intestine length among fishes. For example, Odum (1970)
compared two populations of mullet (Mugil cephaliis) and reported that the gastrointestinal
tract was nearly twice as long in those fish living in a marsh habitat and feeding on hard-to-
digest items such as plant detritus and blue-green algae when compared to mullet inhabiting
an area where the predominant food consisted of benthic and epiphytic diatoms, a food
more easily digested. Luengo (1965) noted the relationship between the carnivorous diet of
Pygocentrus caribe (identified as Serrasalmus nattereri) and its relatively short intestine.
My study showed that intestinal length in Orinoco piranhas varies interspecifically
and is closely correlated with diet. Dental morphology, on the other hand, is a relatively
conservative character within the four piranha genera, although relative jaw width and
degree of musculature vary. This contrasts with the situation present in other serrasalmine
fishes, which exhibit a much more diverse dental morphology, indicating a more labile
evolutionary past (Lundberg et al. 1986). The adults of most non-piranha serrasalmines
are herbivorous (e.g., Mylens, Mylossoma, and Metynnis) and have relatively long
intestines. Catoprion ment is an exception because it eats scales and has a short intestine.
In addition, studies with other vertebrates indicate that features other than length (e.g.,
cellular anatomy or biochemical composition) also determine function of the digestive tract,
and these characters may also show inter- and intraspecific differences (e.g., Karasov and
Diamond 1988). However, I found no evidence to suggest that the intestine length of
individual fish changes in response to shifts in diet.


I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
j.
Horst
Professor of Zoology
O. Schwassmann, Chair
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Carter R. Gilbert, C
Professor of Zoolo
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Martha L. Crump
Professor of Zoology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Frank G. Nordlie
Professor of Zoology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
N C-. >
Nigel J. H. 'mith
Professor of Geography
This dissertation was submitted to the Graduate Faculty of the Department of
Zoology in the College of Liberal Arts and Sciences and to the Graduate School and was
accepted as partial fulfillment of the requirements for the degree of Doctor of Philosophy.
December, 1991
Dean, Graduate School
V-\


164
found that Orinoco piranhas, particularly in low Llanos where there is greater fish biomass,
frequently attack small fish.
As a group, piscivorous piranhas are often the predominant predators in lowland
habitats throughout the Orinoco River basin. Even in the upper Orinoco, I found that
carnivorous species (i.e., S. rhombeus and 5. manueli) outnumber individuals of the more
herbivorous species in most areas. The best information on numbers and biomass of
Orinoco piranhas comes from two studies in the Llanos. Based on rotenone sampling in a
savanna lagoon during the dry season, Mago-Leccia (1970) reported that piranhas (mostly
Pygocentrus caribe) accounted for 14 % of the total number of individuals and 26% of the
total fish biomass. In their study of flooded savannas in the Cao Caicara area, Taphom
and Lilyestrom (1984) found that the biomass of P. caribe was greater than any other fish
predator in both dry season and wet season samples. Their rotenone sampling of a dry
season pool showed that piranhas made up 14% of total fish biomass.
2) Fin Eaters. Stomach content analysis, supplemented by my observations on
feeding behavior of wild-caught juveniles, showed that most piranha species pass through
a growth stage, between 20 and 80 mm SL, when fin-eating is common or the predominant
mode of feeding. Fin-eating seems to be common in young of three of the four piranha
genera (all except juvenile Pygocentrus), and includes juveniles of both herbivorous and
carnivorous species from the Llanos and the upper Orinoco. At least two wide-ranging
species, Serrasalmus altuvei and S. elongatus, feed heavily on fins as adults (Roberts
1970, Goulding 1980, Nico and Taphom 1988, this study). Even though fins apparently
do not provide the nutritional benefits of fish flesh (see Chapter 7), many species may eat
fins because fins are an abundant and rapidly renewable resource (Northcote et al. 1987,
Nico and Taphom 1988). In cropping fins instead of eating the whole animal, piranhas
resemble herbivores that condnually exploit their food resource without eliminating it.
Reproduction of piranhas is closely correlated with the reproductive cycle of most other
fishes, thus there is an abundance of small prey available to young fin-eating piranhas.


45
(1) Serrasalmus altuvei Ramrez 1965: Serrasalmus altuvei in Nico and Taphom
(1988); color illustrations in Nico and Taphom (1986:33), photos reproduced in Schulte
(1988:119).
(2) Serrasalmus cf. eigenmanni Norman 1928: Serrasalmus cf eigenmanni may
involve a species complex (W. Fink, personal communication): however, I distinguished
only one species in my samples. This species, to my knowledge, has not been previously
referenced in publications on Venezuelan piranhas. The piranha Serrasalmus nalseni
described and figured by Fernndez-Ypez (1969) is a possible synonym, but I have not
seen the type series. All previous references to Serrasalmus eigenmanni from the Orinoco
probably refer to other species (see Serrasalmus irritans below).
(3) Serrasalmus elongatus Kner 1860: Serrasalmus cf. elongalus in Taphom and
Lilyestrom (1984), Nico and Taphom (1988); color illustrations in Nico and Taphom
(1986), photos reproduced in Schulte (1988:1, 119); photos as S. pingke in Romn
(1983:56).
(4) Serrasalmus irritans Peters 1877: 5. eigenmanni in Taphom and Lilyestrom
(1983); S. irritans in Nico and Taphom (1988) and Winemiller (1989a, 1989b); color
illustrations as Serrasalmus eigenmanni in Nico and Taphorn (1986:31, 33), same photos
reproduced in Schulte (1988:120), photos as S. eigenmanni in Romn (1983:57).
(5) Serrasalmus manueli Fernndez-Ypez and Ramrez 1967: This species has
rarely been referenced in the literature since its original description. I am unaware of
misidentifications. There is no published information on its biology or natural history.
(6) Serrasalmus medinai Ramirez 1965: Serrasalmus caribe in Nico and Taphom
(1988); incorrectly spelled as S. medini in Winemiiler (1989a, 1989b); color illustrations as
Pristobrycon sp. in Nico and Taphom (1986:31, 33, 41), photos reproduced as
Serrasalmus (.Pristobrycon) sp. in Schulte (1988:119), and as Serrasalmus (Pristobrycon)
"iridescent (incorrect locality given) in Schulte (1988:128); photos as S. rhombeus in
Romn (1983:31,60).


8
Eigenmann (1915), Eigenmann and Allen (1942), and Myers (1972) have reviewed
many of the earlier stories about piranhas. Although published anecdotal information
brought notoriety to this group of South American fishes, early accounts did not
significantly contribute to our knowledge of piranha biology and natural history, and many
stories simply aided to perpetuate myths about piranha ferocity.
There have been a moderate number of studies that have addressed the natural diets
of piranhas (Table 1-1). Most of these have focused on only one or a few of the most
common and widespread species, from a single locality or region. The diets of several of
the more uncommon species have never been described. Most studies of piranha diets have
been of fishes inhabiting artificially altered environments. Because a few of the more
common piranha species seem to flourish in man-made lakes, several studies focused on
populations inhabiting reservoirs or impoundments. Work on piranhas has also been done
in watersheds modified to some extent by cattle ranching, agriculture, and by construction
of roadways. Few investigations have been carried out in pristine habitats.
Several of the earliest efforts to characterize piranha diets were carried out in the
Jaguaribe River basin, a coastal drainage located in northeastern Brazil. The first was that
of Menezes and Menezes (1946). Along with information on several other species, they
presented a simple listing of food items, primarily fish remains and insects, found in the
stomachs of 138 specimens of a single piranha species taken in 1944 from the Lima
Campos Reservoir in Cear State. First identified by Menezes and Menezes as Serrasalmo
immaculatus, Braga (1954) later indicated the species was Serrasalmus rhombeus. Braga
also studied Lima Campos piranhas. He recorded the frequency of occurrence and volume
of stomach contents of a large sample of S. rhombeus (n = 2,222; 100-290 mm total
length) during a 12-month study, 1952-1953 (Braga 1954). Of the 1,713 individuals
containing food, predominant food items were freshwater shrimp (Palaemonidae) and fish,
65 and 28 percent of the total food volume, respectively. Braga later published results
from other studies on piranhas in a single volume (Braga 1975), providing diet information


136
Table 6-9. Incidence of herbivory in piranhas (> 80 mm SL) as associated with the low
Llanos and upper Orinoco.
Taxon
Low Llanos
Upper Orinoco
# With
# Without
# With
# Without
Pristobrycon sp.
5
0
Pristobrycon striolatus
8
2
5
0
s
II
O
4^
Pygocentrus caribe
88
170
4
4
f (X2 = 0.31)
Pygopristis denticulatus
4
2
1
0
t (P = 0.71)
Serrasalmus alluvei
2
5
2
7
t (P = 0.61)
S. cf. eigenmanni
2
1
36
8
t (X2 = 0)
S. manueli
2
22
16
21
** (X2 = 6.93)
S. rhombeus
4
12
9
49
f (X2 = 0.26)
S. elongatus
8
17
S. irritans
13
57
S. medinai
13
37
All Serrasalmus
44
151
63
85
** (X2 = 14.77)
All piranhas
144
325
78
89
** (X2 = 13.18)
* P < 0.05, ** P < 0.01, t not significant
Note: Analysis was limited to individuals > 80 mm SL; each specimen containing food
in its stomach was considered a sample point and scored as to whether or not it contained
any plant matter. To test that upper Orinoco populations were more herbivorous than their
counterparts from the low Llanos, a 2 x 2 contingency table X2 test (one tailed, X2 value
given) was used where appropriate; if N < 40 then a Fisher exact probability test (one
tailed, P value given) was applied.


5
The aim of this study is to increase our knowledge of the ecology and natural
history of piranhas and a few of their close relatives. I have attempted to document and
explain similarities and differences in trophic ecology within and among closely related
species by comparing populations from two floristically distinct regions of the Orinoco
River Basin of Venezuela: (1) the upper Orinoco, an area dominated by dense forests, and
(2) the low Llanos of Apure State, a region characterized by immense open savannas.
Piranhas are widely distributed geographically and very abundant in many lowland
tropical habitats, but we know relatively little about their ecology, behavior, and natural
history. Goulding (1980) found many fishes in the Amazonian forest ecosystems,
including several piranhas, to be herbivorous or omnivorous and to depend heavily on
flooded forests for food resources. Influenced by Goulding's findings.' Donald Taphom
and I began, in late 1983, to study the trophic ecology and natural history of piranhas and
other fishes in savanna ecosystems of the Venezuelan Llanos (Nico and Taphom 1988,
Nico 1990). Although my initial research on piranhas focu.-ed on savanna regions in the
Orinoco Basin, I also made visits to southern Venezuela and the Rio Casiquiare in 1985,
and to Marajo Island in the lower Amazon of Brazil in 1986. Subsequently, between May
1988 and March 1991,1 participated in five expeditions to the upper Orinoco basin and its
forests to broaden my investigation of the feeding ecology of Orinoco piranhas as related to
their habitat
Waters of the low Llanos are typically high in fish and invertebrate biomass, and
many sites support large numbers of carnivores (Mago-Leccia 1970, Taphom and
Lilyestrom 1984, Machado-Allison 1987, Saunders and Lewis 1988, Rodriguez and Lewis
1990). However, large woody plants are uncommon, and in conjunction with water stress
caused by the yearly dry periods, production of seeds and fruits is highly seasonal
(Sarmiento 1984). As a result, availability of plant materials, especially fruits and large
seeds, as food for savanna fishes is low, markedly seasonal, and very localized (personal
observations). On the other hand, the few phenologieal studies of wet forests in lowland


12
on S. nattereri from three other reservoirs of the Jaguaribe basin. In that work, Braga
concluded that piranhas were carnivorous, preferring to feed on other fishes, although they
also prey on other vertebrates (i.e., birds and amphibians), some invertebrates, and only
occasionally on plant material, such as seeds, parts of leaves, and algae.
Bonetto et al. (1967) reported on the feeding habits of two piranhas, Serrasalmus
spilopleura (n = 104) and S. nattereri (n = 21), taken from the middle Paran River and its
floodplain in Argentina. Both species fed predominantly on fish, but prey were not
identified to lower taxa. Stomachs of many of the individuals examined contained small
amounts of plant material, for example, roots and leaves of the aquatic plant Salvinia sp.
and roots of Eichhornia sp. (water hyacinth); however, these items were thought to have
been taken accidentally during capture of their principle prey.
Lowe-McConnell (1964) studied the ecology of fishes in the Rupununi savanna of
the Essequibo River basin, British Guiana (present day Guyana). Although not focusing
on fish diets, she briefly mentioned that the stomachs of fishes trapped in drying pools,
including the piranhas Serrasalmus nattereri, S. rhombeus, and Pygopristis denticulatus,
contained only mud and bottom debris; however, these same fishes had large amounts of
body fat. From her work in the Essequibo River drainage, Lowe-McConnell concluded
that the dry season was a period when fishes exhibited reduced feeding and high diet
overlap.
Roberts (1970) was the first to report on the more unusual feeding practices of
piranhas when he found large amounts of fins and some scales in the stomachs of seven
Serrasalmus elongatus from several sites in the Amazon River basin. He also discussed
scale-eating by the serrasalmine Catoprion ment. Saul (1975) collected two piranha
species during his study of habitat and food preferences of fishes at a site along the
Aguarico River, a tributary of the Napo River in the western Amazon Basin, Ecuador. He
found the stomachs of Serrasalmus nattereri (n = 6) to contain fish remains and insects;


Intestine length (mm) Intestine length (mm)
147


31
America that are associated with climatic oscillations (Prance 1982, Whitmore and Prance
1987). Although lowland regions remained essentially tropical, during major glaciations
the equatorial lowland regions experienced dryer and hotter climates (but see Colinvaux
1976). As a result, savanna and open-land environments expanded, whereas humid forests
contracted. During these dry periods, forests were often reduced to combinations of
variably-sized isolated refuges and fingers of gallery forests along major rivers. Indeed,
new data on Pleistocene mammals indicate that savanna habitat may have expanded to such
an extent as to form a continuous band connecting the Orinoco Llanos with the pampas of
Argentina by way of the western Amazon basin (Raney 1991). The last major glacial event
causing a cold, dry Pleistocene climatic phase occurred 13,000-18,000 years ago.
Much controversy exists about the extent and precise location of forests during the
Pleistocene dry periods. Haffer (1987:12) presented a map outlining possible distribution
of both relatively humid areas and tropical forests, forest "refugia, surviving in northern
South America during that period of savanna expansion. His map delineates three major
regions of humid forests in the Orinoco basin: several sections in the Andes; a block near
the southern tip of Venezuela; and a long broad belt (100-200 km wide) south of the main
stem Orinoco, extending from near the mouth of the Meta River eastward through the
Guianas.
In contrast to glacial periods, interglacial or pluvial periods were wetter and
relatively cooler, contributing to the expansion of humid forests and contraction of
savannas. Isolated savannas currently found in the upper Orinoco are thought to be
savanna refugia that survived the cooler and wetter phases. The present climatic condition
is wet and warm (i.e., as opposed to dry and hot), and humid forests are at or near their
maximum extent, whereas the extent of natural savannas and dry forests is restricted
(Whitmore and Prance 1987:63).


165
Various tactics for successfully nipping fins from other fish have been described including
aggressive mimicry (Nico and Taphom 1986, 1988, Sazima and Machado 1990). Where
piranhas are abundant, many fishes have missing or damaged fins (Northcotte et al. 1987,
Nico and Taphom 1988) making the physical condition of fishes a useful indicator of
piranha density.
Defense by prey fish against fin-eating piranhas is an interesting topic and probably
includes both morphological and behavioral adaptations. The fins of several South
American fishes are nearly transparent in water, for instance those of the anostomid
Abramites hypselonotus Although there is no experimental evidence, the near
transparency of their fins probably provide them protection from predation by fin eaters.
Winemiller (1990) presented evidence that the caudal eyespot of the cichlid Astrononis
ocellatus acts as a deterrent against fin predation. However, behavioral adaptations against
fin-eating piranhas do not require a long history of coevolution. For example, I sometimes
give live bluegill (Lepomis macrochirus) and other native North American fish to young
aquarium-kept piranhas. In a large aquarium, small fast-sw imming fishes are able to avoid
predation; however, most bluegill are rapidly attacked and soon killed. Nevertheless, I
have observed that a few individuals survive weeks in a large tank with a single piranha.
Because fin-eating piranhas normally attack from behind and toward the rear of their prey,
these longer-surviving bluegill apparently learn to protect themselves by facing the piranha
and backing into dense vegetation or crevices. Thus they prevent attacks from the rear as
well as possible crippling injury to their caudal fin.
3) Scale Eaters. Scale-eating, or lepidophagy, is known for several unrelated South
American freshwater fishes (Roberts 1970, Sazima 1977, 1983, Sazima and Machado
1982, Goulding et al. 1988). The possible nutritional benefits of scales have already been
briefly discussed in Chapter 7, and like fins, scales can be thought of as a renewable
resource. Many of the serrasalmine species in both the Llanos and the upper Orinoco take
scales in small quantities, but the non-piranha Catoprion ment is the only species in which


53
In my analysis of diets, the similarity or resemblance matrix generated from the
Schoener Index was used as a basis to cluster species using the unweighted pair-group
method using mathematical averages, or UPGMA. I used 2x2 contingency table X2 tests
(one-tailed) and Mann-Whitney U-tests to test the prediction that forest populations fed
more on plant material than their savanna counterparts.
Nutrient Content Analysis of Food Items
In order to compare nutrient values, analyses were carried out to determine ash,
crude protein, total fat, carbohydrate, and energy contents of different food items. Three
types of food items were examined: small whole fish, fish fins, and fish scales. I also
searched the literature for information on the nutrient value of other types of general food
items, for example insects and various types of plant material. Prey fishes used for
analysis were taken from the Apure River drainage, Venezuela, using cast nets and seines
during the dry season in December 1989 and March 1990. Tissues from members of two
unrelated families of fishes were tested: (1) Curimatidae, represented by Curimatella
immaculata, Cyphocharax spilurus, and Steindachnerina argntea; and (2) Cichlidae,
Aequidens pulcher and Cichlasoma orinocense. These species are common in the Orinoco
River basin and are frequently preyed upon by juvenile and adult piranhas.
In total, 135 small cichlids (SL range 39-77 mm) and 96 curimatids (SL range 45-
78 mm) were used for nutrient content determinations. Fish were placed on ice
immediately after capture, transponed to the laboratory at the Universidad de Los Llanos
Occidentales (UNELLEZ) in Guanare, Venezuela, and refrigerated until analysis was
conducted. Body scales were removed from partially frozen specimens with a small fish
scaler, and no attempt was made to clean off the bodys outer mucous layer. Only caudal
and dorsal fins were used for fin samples; these were removed by clipping with scissors
above the fin base to avoid scales. Two or three entire cichlid and curimatid specimens


78
Pvgocentms caribe (Valenciennes 1849)
Pygocentrus caribe was the most abundant piranha in the Cao Caicara area,
occurring in both flooded savanna and flowing waters. This blunt-headed, heavy-bodied
species (Fig. 5-2) reaches approximately 300 mm SL. Stomach contents of 516 P. caribe
in the four larger size classes are given in Table 5-1 and Figure 5-3. Unlike most other
piranha species, fish fins and scales were of minor importance in stomachs of juveniles.
Group II fish fed most heavily on aquatic insects, followed by microcrustaceans, but for
Group in fish flesh was the most important food item, followed by plant material
(primarily vascular plant debris) and aquatic insects. Larger P. caribe of groups IV and V
took mostly fish flesh and whole small fish.
Thirty-two species of prey fishes (mostly characins) were identified from stomachs
of Groups IV and V P. caribe (Table 5-2). There were also several instances of
cannibalism by adults on small juveniles. In addition to fish, larger juveniles and adults
sometimes ate other vertebrates, perhaps as carrion. Different stomachs contained a chunk
of flesh from a small caiman (Caiman crocodilus), skin of a lizard (probably Ameiva), and
a small adult leptodactylid frog. Three individuals taken together had stomachs full of
feathers, flesh, and bone fragments of a white-faced whistling duck (Dendrocygm
viduata). Mammals were not found in P. caribe from the study area, but I have found flesh
and fur of small rodents in specimens from nearby localities.
Serrasalmus irritara Peters 1877
Serrasalmus irritans was very common, usually second only to P. caribe in
numbers of individuals at most sampling sites. My sample consisted of 271 specimens
(Table 5-3 and Fig. 5-3). It has a moderately pointed snout (Fig. 5-2) and is seldom
longer than 160 mm SL. My study shows that juvenile S. irritans (Groups II and III)
specialized on fins of other fishes. Stomachs of the young of this piranha were typically
packed exclusively with fins, mostly from fish smaller or similar in size to the predator.


Table 5-3. Food items of Serrasalmus irritans from the Apure River drainage (Cao Caicara area) by size class. %0 =
percent frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 271.
Size class (mm, SL)
Number examined
Number empty
Food items
%o
II (20-39)
29
1
%D
%Va
%o
III (40-79)
162
7
%D %Va
IV (80-159)
80
10
%0 %D %Va
Plant material
10.7
3.6
1.4
1.9
-
-
18.6
8.3
5.0
Decapoda
-
-
-
0.6
0.6
0.3
1.4
-
-
Aquatic insects
-
-
-
3.2
-
-
1.4
-
-
Other invertebrates
-
-
-
0.6
-
-
1.4
1.4
0.4
Small whole fish
-
-
-
3.2
3.1
4.0
18.6
13.9
18.8
Fish flesh
-
-
-
21.9
17.5
21.0
28.6
25.0
37.1
Fish fins
92.9
92.6
97.3
81.9
73.8
72.3
37.1
22.2
21.3
Fish scales
10.7
-
-
23.2
3.1
1.3
37.1
23.6
14.2
Other
3.6
3.6
1.4
3.9
1.9
1.2
8.6
5.6
3.3
oo


Apure State and the lowland forests of the upper Orinoco undergo extensive flooding
during the wetter part of the year by a combination of rising river water and local rains.


128
O 25 50 75 100
i \ 1 i
SR 40-79
PC 80-159
SM 80-159
SM £160
PC 2160
SR 80-159
SM 40-79
SR 2160 -
SEG 40-79*
SM 20-39
SA 80-159 -
SA2160
PST 20-39 -
SEG 80-159*
PST 80-159
SEG 2160
PST 2160
PSP2160
PYP2160
MYT2160
MYS2160 -
MYA 80-159
MYA2160 -
MYS 80-159_
MYT 80-159*1
CM 80-159 J
SM 10-19 -
PYP 20-39
PST 20-39
PYP 10-19.
General
Piscivores
Fin Eaters
Seed
Predators
Leaf
Eaters
Scale
Eaters
Insect ivores
0 25 50 75 100
Percent diet similarity


Fig. 5-2. General body form and major fin markings of seven piranha species (55-70 mm
SL) and Catoprion ment (Cm) from Cao Caicara study area, Apure Drainage,
in the low Llanos of Venezuela: Pc = Pygocentrus caribe; Pst = Pristobrycon
striolatus, Smd = Serrasalmus medinar, Sr = Serrasalmus rhombeus,
Sa Serrasalmus altuvei, Sir = Serrasalmus irritaos, and Sel = Serrasalmus
elongatus.


199
Braga, R. A. 1975. Ecologia e etologia de piranhas no Nordeste do Brasil (Pisces -
Serrasalmus Lacpde, 1803). Banco do Nordeste do Brasil, Fortaleza, Ceara,
268 pp.
Brooks, D. R. and D. A. McLennan. 1991. Phylogeny, ecology, and behavior.
University of Chicago Press, Chicago, 434 pp.
Burr, B. M., and L. M. Page. 1986. Zoogeography of fishes of the lower Ohioupper
Mississippi Basin. Pages 287-327 in C. H. Hocutt and E. O. Wiley, editors.
Zoogeography of North American freshwater fishes. John Wiley and Sons,
Chemoff, B., A. Machado-Allison, and W. G. Saul. 1991. Morphology, variation and
biogeography of Leporinus brunneus (Pisces: Characiformes: Anostomidae).
Ichthyological Exploration of Freshwaters 1(4): 295-306.
Clutton-Brock, T. H. and P. H. Harvey. 1984. Comparative approaches to investigating
adaptation. Pages 7-29 in J. R. Krebs and N. B. Kavies, editors. Behavioral
ecology: an evolutionary approach. Blackwell Scientific Publications, Oxford.
Colinvaux, P. 1987. Amazon diversity in light of the paleoecological record. Quaatemary
Science Reviews 6:93-114.
Comisin para el Desarrollo del sur de Venezuela (CODESUR). 1979. Atlas de la regin
sur de Venezuela. Ministerio del Ambiente y de los Recursos Naturales Renovables
(MARNR), Caracas, Venezuela, 67 pp.
Cole, M. M. 1986. The savannas: biogeography and geobotany. Academic Press, New
York, 438 pp.
Cummins, K. W and J. C. Wuycheck. 1971. Caloric equivalents for investigations in
ecological energetics. Mitt. Intemat. Verein. Limnol. 18:1-158.
Davis, G. E., and C. E. Warren. 1971. Estimation of food consumption rates. Pages
227-248 in W. E. Ricker, editor. Methods for assessment of fish production in
fresh waters. Blackwell Scientific Publications, Oxford.
Distribuidora Escolar (DISCOLAR). 1983. Discolar atlas de Venezuela. Discolar,
Virginia Gardens, Florida, 320 pp.
Duellman, W. E. 1990. Herpetofaunas in neotropical rainforests: comparative
composition, history', and resource use. Pages 455-505 in G. H. Gentry, editor.
Four neotropical rainforests. Yale University Press, New Haven, Conneticut.
Eigenmann, C. H. 1915. The Serrasalminae and Mylinae. Annals of the Carnigie
Museum 9(3-4):226-272.
Eigenmann, C. H., and W. R. Allen. 1942. Fishes of western South America.
University of Kentucky Press, Lexington,. 494 pp.
Felley, J. D. 1984. Multivariate identification of morphological-environmental
relationships within the Cyprinidae (Pisces). Copeia 1984(2):442-455.
Fernndez-Ypez, A. 1969. Contribucin al conocimiento de los serrasalmidos. Evencias
(Maracay), Number 23, 6 pp. including 2 figures. Mimeograph.


S.L. (mm)
20-39
40-79
80-159
^ 160
SERRASALMUS SERRASALMUS SERRASALMUS SERRASALMUS PYGOCENTRUS PRISTOBRYCON PRISTOBRYCON PYGOPRISTIS
RHOMBEUS MANUELI cf. EIGENMANNI ALTUVEI
CARIBE STRIOLATUS
SP.
n=2 (1.47) n=18(1.83)
n=52 (2.99) n=42(1.99)
BMasticated Seeds
Other Plant Material
Microcrustaceans
Decapoda
n=7 (2.10)
n=8 (1.82) n=1 (1.11)
n=5 (1.08)
DENTICULATUS
n=1 (1.07)
o
K>


56
procedure for identifying feeding patterns in assemblages of fishes (Stoner and
Livingston 1984, Henderson and Walker 1986) and other vertebrates (Jaksic and Medel
1990). The method has also been used extensively to describe fish distribution patterns
(Hocutt and Wiley 1986). Basically, the UPGMA clustering technique generates a
hierarchical tree, or dendrogram, grouping together those samples or objects that are most
similar. UPGMA is widely applied because it can be used with a variety of resemblance
coefficients and also because it forms clusters in a more conservative manner than many
other clustering methods (Gauch 1982:199, Romesburg 1984, James and McCulloch
1990:147). As a measure of secondary validity, an additional clustering technique,
complete linkage (farthest neighbor), was used to assess whether resulting clusters were
more-or-less real rather than mathematical artifacts (Gauch 1982, Romesburg 1984).


Table 5-1. Food items of Pygocentrus caribe from the Apure River drainage (Cao Caicara area) by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 516.
Size class (mm, SL)
Number examined
Number empty
Food items
II (20-39)
110
l
%0 %D %Va
III (40-79)
84
5
%0 %D %Va
IV (80-159)
176
18
%0 %D %Va
V(>160)
146
46
%0 %D %Va
Plant material
17.4
1.8
1.1
43.0
25.3
23.5
29.7
8.7
5.4
41.0
15.0
8.8
Decapoda
-
-
-
10.1
7.2
7.4
3.8
1.2
1.2
9.0
4.7
3.0
Microcrustaceans
78.0
23.7
21.4
19.0
3.6
2.6
-
-
-
-
-
-
Aquatic insects
80.0
55.3
60.7
32.9
14.5
14.7
0.6
-
-
11.0
4.7
3.0
Other invertebrates
36.7
14.0
12.3
30.4
10.8
12.4
5.1
1.2
0.6
21.0
4.7
2.0
Small whole fish
0.9
0.9
1.1
2.5
1.2
1.8
29.1
22.0
24.1
51.0
41.1
51.0
Fish flesh
0.9
0.9
1.1
29.1
19.3
25.3
. 81.6
59.0
63.7
38.0
17.8
20.5
Fish fins
-
-
-
36.7
8.4
4.1
12.0
0.6
0.3
7.0
2.8
1.8
Fish scales
-
-
-
17.7
2.4
1.8
12.0
4.6
2.8
12.0
3.7
2.0
Other
3.7
3.5
2.4
10.1
7.2
6.5
5.1
2.9
1.9
9.0
5.6
7.8
MD


135
I examined the stomach contents of 11 P. denticulatus (19-195 mm SL) taken from
the Capanaparo River drainage during low water (Fig. 6-7). Two small juveniles (19 and
28 mm SL) contained mostly microcrustaceans (ostracods, cladocerans, and copepods);
other food items included aquatic insect fragments (e.g., odonata nymph) and a few
diatoms. Masticated seeds were found in the stomachs of five of the eight specimens
greater than 40 mm SL; food items were as follows (%0-%D-%V): Group HI (n = 3) -
masticated seeds (100.0-66.7-95.0), and fish scales (66.7-33.3-5.0); Group IV (n=3)-
masticated seeds (66.7-66.7-55.0), aquatic insects (adult coleptera) (66.7-33.3-27.5),
fish flesh (33.3-0-17.2), and fish scales (33.3-0-0.3); Group V (n = 3) masticated seeds
(33.3-0-22.7), plant material (woody fiber and twigs) (66.7-33.3-22.7), aquatic insects
(adult coleptera) (66.7-0-6.8), fish scales (66.7-33.3-36.4), and other (soil) (33.3-33.3-
11.4).
Serrasalmus cf. eigenmanni occurs in the Cinaruco River of the Llanos. It appears
to be scarce, however, and I only examined three specimens (155-198 mm SL) (Fig. 6-7).
Two stomachs contained small amounts of leaf fragments. Other items included a few
large fish scales and some fish flesh.
Spatial Variation: Herbivorv versus Carnivory
Based on floristic differences between the two regions, I predicted that populations
in the upper Orinoco would be more herbivorous than their savanna counterparts. Table 6-
9 compares the incidence of herbivory among all piranhas (specimens >80 mm SL) from
the upper Orinoco to those from the low Llanos. With the exception of Serrasalmus
manueli, the proportion of piranhas containing plant matter was not significantly different
between the two regions. However, comparisons combining all species, and combining all
members of the genus Serrasalmus were significant in chi-square tests (Table 6-.9).


99


S.L. (mm)
40-79
80-159
>160
PYGOPRISTIS SERRASALMUS
DENTICULATUS cf. EIGENMANNI
PRISTOBRYCON
STRIOLATUS
n = 2
m
Masticated Seeds
Fish Flesh
i
:
Other Plant Material
Fish Fins
7 7
N N S
/ s
\ \ \
/ / !
Aquatic Insects
n
Fish Scales
1
Other Invertebrates
i
Other


54
were used for tests as small whole fish. All subsequent nutrient analyses were carried out
at UNELLEZ under the direction of the biochemist Dr. Margioly de Morales. Samples
were oven-dried to constant weight at 60 C to prevent lipids in the body tissues from
volatilizing. After drying, samples were ground in a Willey mill and stored in desiccators.
Unless otherwise stated, methods of analysis used follow AOAC (1980) guidelines.
Results are expressed as percentages of dry weight, rather than as percentages of ash-free
dry weight (i.e., on organic matter basis), for ease of comparison to previously published
data. All measurements were duplicated; the differences between replicate subsamples of a
particular food item were generally less than 1%. Ash contents were determined by
combustion of samples of dried body tissue at 550 C for 3 hours (Pierce et al. 1980).
Total fat content was determined by extracting lipids for four hours with diethyl ether.
Crude protein was determined by the Kjeldahl method for nitrogen, where crude protein is
total nitrogen concentration multiplied by 6.25. Carbohydrates were determined as the sum
of crude fiber and nitrogen-free extract; total carbohydrates are the sum of both values.
Energy content was measured using a Parr bomb calorimeter and expressed as kJ per g;
this can be converted to kilocalories per g by dividing by 4.184.
Intestine Length
Length of the intestinal tract (IL) was determined by removing the entire
gastrointestinal tract, placing the extended intestine (without stretching) on a flat surface,
and measuring the distance from the pylorus to the anus (Ribble and Smith 1983). Fecal
material was left in the intestine during measurement Relative intestine length for each fish
was calculated by dividing IL by standard length (SL). An analysis of covariance
(ANCOVA) was carried out in order to compare the regression lines of IL versus SL
among species. A Spearman rank correlation test was used to test for an association
between relative intestine length and the percent volume of plant material among the


58
Fig. 4-1. Schematic representation showing relative distances among the nine sampled
drainages and their approximate location along Orinoco River main channel.
Arrow indicates division between upper and lower Orinoco.


113
Table 6-5. Food items of Serrasalmus altuvei from drainages of the upper Orinoco River
basin, by size class. %0 = percent frequency of occurrence; %D percent dominance;
and %V = percent volume. N = 9.
Size class (mm, SL)
Number examined
Number empty
Food items
%0
IV (80-159)
7
1
%D
%V
%0
V(>160)
2
1
%D
%v
Plant material
-
-
-
100.0
-
12.5
Aquatic insets
33.3
-
2.5
-
-
-
Other invertebrates
16.7
-
0.2
-
-
-
Fish flesh
50.0
33.3
7.0
-
-
-
Fish fins
66.7
50.0
63.1
100.0
100.0
75.0
Fish scales
66.7
16.7
27.0
100.0
-
12.5
Other
16.7
_
0.2
-
-
-


page
Ia¡2k
5-8 Food items of Pristobrycon striolatus from the Apure River drainage (Cao
Caicara area) by size class 89
5-9 Food items of Catoprion ment from the Apure River drainage (Cao
Caicara area) by size class 90
5-10 Food items of small juvenile piranhas (Size Class I, 10-19 mm SL),
tentatively identified as Pygocentrus caribe, from the Apure River drainage
(Cao Caicara area) 92
5-11 Matrix of diet overlaps among different size classes of piranhas from Apure
River drainage, low Llanos 95
6-1 List of taxa identified from the stomach contents of the three most common
piranha species from upper Orinoco River drainages, Venezuela 103
6-2 Food items of Serrasalmus rhombeus from the upper Orinoco River basin
by size class 104
6-3 Food items of Serrasalmus manueli from the upper Orinoco River basin by
size class 107
6-4 Food items of Serrasalmus cf. eigenmanni from the upper Orinoco River
basin by size class Ill
6-5 Food items of Serrasalmus altuvei from the upper Orinoco River basin by
size class 113
6-6 Food items of Pristobrycon striolatus from the upper Orinoco River basin
by size class 115
6-7 Food items of Pygopristis denticulatus from the upper Orinoco River basin
by size class 118
6-8 Matrix of diet overlaps among different size classes of serrasalmine fishes
from upper Orinoco River drainages 124
6-9 Incidence of herbivory in piranhas (> 80 mm SL) as associated with the low
Llanos and upper Orinoco 136
6-10 One-tailed Mann-Whitney U-test results testing the prediction that piranha
species (> 80 mm SL) from upper Orinoco River drainages fed more on
plant material than those from the low Llanos 140
7-1 Estimates of the lipid, protein, ash, carbohydrate, and caloric contents of
fins, scales, and whole fish for two taxa of typical prey fish 149
8-1 Orinoco River basin piranhas categorized by adult diet 158
viii


196
Table B-9. Percent dominance (%D) of plant material in piranhas (> 80 mm SL) as
associated with the low Llanos and upper Orinoco.
Low Llanos
Upper Orinoco
Taxon
%D
%D
Pristobrycon sp.
-
100.0
Pristobrycon striolatus
50.0
80.0
Pygocentrus caribe
11.2
33.3
Pygopristis denticulatus
66.7
100.0
Serrasalmus altuvei
0
0
S. cf. eigenmanni
33.3
68.2
S. manueli
0
27.0
S. rhombeus
12.5
1.7
S. elongatus
4.0
-
S. irritans
8.6
-
S. medinai
6.0
-


46
Table 3-1. List of abbreviations used in figures and tables for piranhas and other
serrasalmine fishes.
Piranhas:
Other Serrasalmine Fishes:
Pc
Pygocentrus caribe
Cm
Catoprion ment
Psp
Pristobrycon sp.
Mag
Metynnis argenteus
Pst
Pristobrycon striolatus
Mya
Myleus asterias
Pyp
Pygopristis denticulatus
Mys
Myleus schomburgkii
Sa
Serrasalmus altuvei
Myt
Myleus torquatus
Seg
Serrasalmus cf. eigenmanni
Md
Mylossoma duriventris
Sel
Serrasalmus elongatus
Sir
Serrasalmus irritans
Sm
Serrasalmus manueli
Smd
Serrasalmus medinai
Sr
Serrasalmus rhombeus


Table 4-1. Occurrence of piranha species in samples from nine drainages in the Orinoco River basin, Venezuela. C = common in fish
samples, P = present but uncommon in samples. Data based on my samples and MCNG material unless otherwise indicated.
River Drainages
Low LLanos
Upper Orinoco
Species
Apure
Capanaparo
Cinaruco Sipapo
Atabapo
Ventuari Matacuni
Ocamo
Mavaca
Totals
Serrasalmus medinai
C
1
Serrasalmus irritans
C
P
2
Serrasalmus elongatus
P
P
P
3
Pygocentrus caribe
C
P
P
P
4
Pygopristis denticulatus
P
P
P
P
P
P
6
Serrasalmus manueli
P
C P
C
C
5
Pristobrycon sp.
P
1
Serrasalmus rhombeus
P
C
C
C C
C
P
7
Pristobrycon striolatus
P
P
P
Pa
P
P
P
7
Serrasalmus altuvei
P
P
P
P
4
Serrasalmus cf.
eigenmanni
P
P P
P
C
5
Total number of species
8
7
6 1
4
6 3
5
5
a = Single specimen from Atabapo River drainage was recorded by Machado-Allison et al. (1989).
VO


207
Smith, L. S. 1989. Digestive functions in teleost fishes. Pages 331-421 in J. E. Halver,
editor. Fish nutrition. Academic Press, San Diego, California.
Smith, N. J. H. 1981. Man, fishes, and the Amazon. Columbia University Press, New
York, 180 pp.
Snow, D. W. 1981. Tropical frugivorous birds and their food plants: a world survey.
Biotropica 13:1-14.
Steyermark, J. A. 1982. Relationships of some Venezuelan forest refuges with lowland
tropical floras. Pages 182-220 in G. T. Prance, editor. Biological diversification in
the tropics. Columbia University Press, New York.
Stoner, A. W., and R. J. Livingston. 1984. Ontogenetic patterns in diet and feeding
morphology in sympatric sparid fishes from seagrass meadows. Copeia
1984( 1): 174-187.
Taphom, D. C. 1990. The Characiform fishes of the Apure River drainage, Venezuela.
Ph.D. dissertation, University of Florida. 892 pp.
Taphom, D. C., and C. G. Lilyestrom. 1984. Los peces del Mdulo Femando Corrales:
resultados del proyecto de investigacin del CONOCIT, PIMA-18. Revista
UNELLEZ de Ciencia y Tecnologa No. 2, pp. 55-85.
Terborgh, J. 1983. Five New World primates: a study in comparative ecology.
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Thomerson, J. E., and D. P. Wooldridge. 1970. Food habits of allopatric and syntopic
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Van Oosten, J. 1957. The skin and scales. Pages 207-224 in M. E. Brown, editors. The
physiology of fishes, Academic Press, New York.
Vieira, I., and J. Gry. 1979. Crescimento diferencial e nutrigao em Catoprion ment
(Characoidei): peixe lepidfago da Amazonia. Acta Amaznica 9(1):143-146.
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London.]
Wallace, R. K., Jr. 1981. An assessment of diet-overlap indices. Transactions of the
American Fisheries Society 110(l):72-76.
Walter, H. 1973. Vegetation of the earth in relation to climate and the eco-physiological
conditions. Springer-Verlag, New York, 237 pp.
Walter, H., E. Hamickell, and D. Mueller-Dombois. 1975. Climate-diagram maps of the
individual continents and the ecological climatic regions of the earth: supplement to
the vegetation monographs. Springer-Verlag, Berlin, 36 pp.
Wessler, E., and I. Werner. 1957. On the chemical composition of some mucous
substances of fish. Acta Chem. Scand. 2:1240-1247.


110
Llanos. Individuals of all sizes are silver-colored and have numerous irregularly-shaped
dark spots, with the number and shape of the spots being quite variable. Adults have a
rather faint black humeral spot The base of the caudal fin is black, which in older fish
covers nearly the entire tail except for a terminal hyaline band. Parts of the cheek and
breast, as well as the pectoral and anal fins, are reddish orange. Although Serrasalmus cf
eigerunanni may involve a species complex (W. Fink, personal communication), I
distinguished only one species in my samples.
The diet of this species has not been reported previously. All larger 5. cf.
eigenmanni were primarily seed predators (Fig. 6-2 and Table 6-4). Masticated seeds,
mostly endocarp, were found in 35 of 46 Group IV and V specimens and accounted for
75% of total food volume. The only other plant materials found were fragments of mature
flowers in two stomachs. Unfortunately none of the seeds or flowers could be identified.
Although its natural diet consisted primarily of seeds, as in other piranhas, adult 5. cf.
eigenmanni readily take hooks baited with fish flesh. The stomachs of two young juveniles
(48 and 76 mm SL) examined were packed exclusively with fins of other small fishes.
IL/SL ratio (n = 32) ranged from 0.9 for a 48-mm SL juvenile, to 3.4 for a 129-mm SL
adult.
Serrasalmus altuvei Ramirez 1965
Serrasalmus altuvei was uncommon in samples from the upper Orinoco. It is a
medium-sized piranha, with a slender pointed snout and a deep body that is more laterally
compressed than that of most other piranhas (Fig. 6-1). The body is silvery, and the sides
are covered with black spots that are vertically elongated in most juveniles and some adults.
Large juveniles and adults have a dark humeral spot and a black terminal band on the caudal
fin. Live S. altuvei from the Mavaca River were found to have a partly red iris, which was
less intense than that of 5. rhombeus. I collected 12 fish (119-169 mm SL), from the
Mavaca, Ocamo and Matacuni rivers, and examined the stomach contents of 9 specimens


62
Table 4-2. Distance between drainages and Coefficient of Biogeographic Resemblance
(in parenthesis) among nine sampled drainages in the Orinoco River basin. Distances
measured in kilometers between drainage mouths by way of Orinoco River main channel.
CBR values range from 0 (no species in common) to 1 (complete similarity in species
composition)
River Drainages
Low Llanos
Upper Orinoco
Apu
Cap
Cin
Sip
Ata
Ven
Mat
Oca
Mav
Drainage area
(km2 x 103)
167
35
25
13
9.4
40.5
10.1
9.8
5.3
Number of
piranha species
8
7
6
1
4
6
3
5
5
Apure
110
(0.80)
160
(0.57)
400
(0)
530
(0.33)
610
(0.57)
945
(0.36)
965
(0.62)
1000
(0.62)
Capanaparo
50
(0.77)
290
(0.25)
420
(0.55)
500
(0.77)
835
(0.20)
855
(0.50)
890
(0.50)
Cinaruco
240
(0.29)
370
(0.60)
450
(0.83)
785
(0.44)
805
(0.55)
840
(0.73)
Sipapo
130
(0.40)
210
(0.29)
545
(0)
565
(0)
600
(0)
Atabapo
80
(0.60)
415
(0)
435
(0.22)
470
(0.44)
Ventuari
335
(0.44)
355
(0.73)
590
(0.73)
Matacuni
20
(0.75)
55
(0.75)
Ocamo
35
(0.80)
Mavaca


14
be analyzed. In the published proceedings of a symposium Leao et al. (1989) reported on
the morphology, reproduction, and diet of Serrasalmus altuvei from the Rio Negro.
Sazima and his colleagues have explored the behavior of piranhas and related
species, particularly in reference to fin and scale-eating, through laboratory work with
captive fishes and underwater observations of free-living fishes in the Pantanal region,
western Brazil (Sazima 1983, 1986, 1988; Sazima and Zamprogno 1985, Sazima and
Pombal 1988, Sazima and Machado 1990). Sazima and Guimares (1987) recognized
Pygocentrus nattereri and Serrasalmus spilopleura as scavengers, feeding on dead and
sometimes decaying fishes, birds, and mammals. They suggested that deaths of humans
attributed to piranhas might often be the result of scavenging on victims already dead from
drowning or other causes. Sazima and Machado (1990) presented data from their
underwater observations on the behavior of three species, S. marginatus, S. spilopleura,
and P. nattereri, with emphasis on their predatory tactics, feeding behavior, and social
interactions while foraging.
Ferreira (1984b) studied the food and feeding habits of the principal fish species
inhabiting the Curu-Una River Reservoir, in the Amazon Basin near Santarm, Brazil.
Ferreira found that the diet of Serrasalmus rhombeus, taken from five localities in the
reservoir, showed slight differences among stations, feeding mainly on fish at four sites,
and on aquatic insects (i.e., ephemeroptera) at a fifth locality. In total, 250 specimens
were examined (ranging from 50 to 320 mm SL) of which 196 piranhas contained food.
Northcote et al. (1986, 1987) reported fin feeding by Serrasalmus spilopleura from
the Americana Reservoir, an impoundment on the Atibaia River in southeastern Brazil.
Analysis of prey fishes with damaged fins showed that S. spilopleura usually nip the lower
lobe of fins, indicating that attacks are made from below and behind prey fishes. They also
suggested that 5. splilopleura was the main, if not the only, fin-feeder in the reservoir fish
community. Mota et al. (1982) studied the seasonal variation in the intensity of feeding, as
measured by stomach fullness, of 5. spilopleura from the Bariri Reservoir in Sao Paulo


21
community of La Esmeralda, nearly 1,800 km by river from the sea, is only 135 m above
sea level, an average drop of less than 1 m for every 10 km of river.
In summary, large rivers of lowland forests that feed the upper Orinoco from the
south include the Mavaca and Atabapo rivers. Big-river tributaries originating in the
Guyana Shield and feeding into the upper Orinoco include the Ocamo, Padamo,
Cunucunuma, Ventuari, and Sipapo; those flowing into the lower Orinoco include the
Caura and Caroni rivers. Large tributaries of the Orinoco that originate on or near the
Andean slopes are the Inirida, Guaviare, Vichada, Tomo, Meta, Cinaruco, Capanaparo,
Arauca, and Apure rivers. About 31 percent of the upper Orinoco volume is continually
diverted into the Amazon basin by way of the Brazo Casiquiare, a natural canal
(CODESUR 1979).
In addition to a diverse flora and topography, the Orinoco River basin is a mosaic
of water types. Alfred Russel Wallace ([1853] 1972) was one of the first to mention the
striking differences in water colors among the various South American waters using the
terms whitewater, blackwater, and Clearwater rivers. In a later and more detailed analysis,
Sioli (1975, 1984) summarized differences among these three water types based on
differences in water color, amount of suspended matter, and chemical properties.
Whitewater streams are turbid because of inorganic sediments, of milk-coffee color (cafe
con leche), relatively rich in nutrients, and of near neutral pH. Blackwater streams are
transparent but reddish brown, the color of tea due to humic acids (the color appears black
where water runs deep), very poor in nutrients and very acidic. Clearwater streams are
also transparent, often greenish in color, typically poor in nutrients, and have a pH that can
range from slightly acidic to slightly alkaline.
In the Orinoco River basin, whitewater and blackwater habitats predominate. Clear
waters are more typical of small caos and the upland reaches of certain rivers. However,
the classification of rivers by water color is not always easy to apply and thus the
usefulness Sioli's classification scheme is somewhat limited. Many, rivers are a mixture of


151
made it difficult to determine if such behavior is widespread. Scales eaten were all large,
thereby eliminating the possibility of intraspecific aggression since all Myleus species have
fairly small scales.
Scale-eating fishes probably have less difficulty in digesting scales than other fish
parts, for instance bone. Because I rarely found whole scales in the posterior parts of the
their intestine, it suggests that ingested scales are broken down into their component parts
in the foregut. Although scales are a common food item, there have been no published
reports on the nutrient value of scales of South American freshwater fishes. My results
from analysis of scales from cichlid and curimatid fishes generally agree with previous
findings (Table 7-1, Fig. 7-1). Whitfield and Blaber (1978) reported that scales from the
mugilid Mugil cephalus, a wide-ranging species of both marine and fresh waters, had a
caloric value of 8.5 kj/g. Scales that have been studied were found to contain 40-85%
protein (van Oosten 1957). The mucus that coats fish scales is rich in proteins (Wessler
and Wemer 1957) and lipids (Lewis 1970). In salmon, the protein content of the mucus is
62% of the dry weight (Harris and Hunt 1973). The mineral proportion, calcium
phosphate, of a teleost scale ranges from 16% to 59%, depending on species (Whitear
1986). Sazima (1983) thought that scale eaters must augment their diet with other kinds of
food. Goulding et al. (1988) found that 100 of 250 fish species from the Rio Negro fed on
scales, usually in small quantities, and they argued that occasional scale eating may act to
supplement diets for those fishes inhabiting rivers that are poor in calcium and
phosphorous (e.g., blackwater habitats).
Fins
Fin eating is common among piranhas and several other South American fishes.
Most fishes taken in the low Llanos are missing pieces of their caudal or dorsal fins during
both high and low water periods. On the other hand, my observations seem to indicate that
the incidence of fin eating is much less in the upper Orinoco (L. Nico, unpublished data).


48
commonly used measures for comparing species presence-absence data (Krebs 1989), and
is calculated as:
CBR = 2C/ (Ni + N2),
where C is the number of species common to two areas, N i is the number of species in the
first area, and N2 is the number of species in the second area. The resulting values range
from 0, if there are no species in common, to 1, if both areas share the same number and
kinds of species. This measure is simple, is not affected by relative numbers of
individuals, and thus is best used when there are no reliable quantitative data on abundance
of species (Magurran 1988, Krebs 1989). Binary similarity measures are not totally
independent of sample size (Wolda 1981, Krebs 1989). However, comparisons when
maximum number of possible species is low give results less affected by sample size
differences than those dealing with many species (see Krebs 1989). CBR is very similar to
the Jaccard Coefficient (Boesch 1977, Romesburg 1984, Duellman 1990); it doubly
weights shared positive attributes (i.e., joint presences), and is preferred over the Jaccard
Coefficient if the entities vary widely in their number of positive attributes (Boesch
1977:22).
To make presence-absence data more reliable, I supplemented my data with
information from collections deposited at MCNG and UF. I also reviewed the literature for
records of species occurrence. A Spearman rank correlation test was used to test for an
association between species composition and drainage area size, and between faunal
similarities and distances among drainages. The similarity or resemblance matrix generated
from the CBR equation was used as a basis for clustering drainages, employing the
unweighted pair-group method using mathematical averages, or UPGMA.


CHAPTER 5
TROPHIC ECOLOGY OF SAVANNA PIRANHAS: THE APURE DRAINAGE
This chapter focuses on the diets of piranhas from the area around the Femando
Corrales ranch and research station of the University of the Western Llanos (UNELLEZ),
located in the Cao Caicara region, Apure River drainage, in the low Llanos (Fig. 5-1). I
give this drainage separate treatment because it is the only site where long-term sampling
(1979-1990) has been carried out (Taphom and Lilyestrom 1984, Nico and Taphom 1984,
1985, 1988, Nico 1990, Taphorn 1990). The existing data base on piranhas from the
Cao Caicara region is the most complete of any single locality or drainage in the Orinoco
basin. The seven species examined were Pygocentrus caribe, Serrasalmus altuvei, S.
medinai, S. elongatus, S. irritaos, S. rhombeus, and Pristobrycon striolatus (Fig. 5-2). I
also report on the diet of the serrasalmine Catoprion ment, a close relative of the piranhas.
Study Area
The study area is located in the low Llanos of Apure State (0725'50"N,
693530"W) about 80 km W of the town of Mantecal (Fig. 5-1). Several permanent
streams border the 12,600-ha ranch, caos Caicara, Maporal, and Guaritico. These low-
gradient streams have mostly silty bottoms, and are bordered by narrow gallery forests.
The ranch is maintained primarily for grazing of cattle and encompasses open flat savanna
with a very gradual sloping terrain west to east. Most of the savanna floodplain of the
ranch is surrounded by a 2.5 m high earthen dike constructed to control flooding during the
rainy season and hold water during the drier part of the year. During the rains most of the
71


Table 5-11. Matrix of diet overlaps among different size classes of piranhas from Cao Caicara area, Apure River drainage, low Llanos.
Overlap index is that of Schoener (1970); SL = Standard Length; JV = small juveniles; see Table 3-1 for species abbreviations.
Species and
Size Range
(mm SL)
PC
2039
PC
4079
PC
80159
PC
£160
SR
2039
SR
4079
SR
80159
SR
£160
SEL
2039
SEL
4079
SEL
80159
SEL
£160
SIR
2039
SIR
4079
SIR
80159
SMD
2039
SMD
40-79
SMD
80159
PST
2039
PST
4079
PST
80159
CM
2039
CM
4079
CM
80159
SA
4079
SA
80159
JV
1019
PC 20-39
100
35.2
5.75
10.7
43.6
2.1
11.2
4.5
0
1.05
10.05
1.05
2.4
3.3
6
14.25
4.85
3.3
14.35
0
13.3
2.5
3.25
1.05
1.05
1
62.9
PC 40-79
100
38.25
49.2
21.35
16.2
54.8
33.4
4.05
21.45
46.55
30.85
6.8
29.6
41.6
26.65
27.25
38.8
27.35
4.05
45
5.3
22.95
25.25
5.85
31.1
22.25
PC 80-159
100
56.05
0.3
20.25
24.45
47.35
0.3
18.7
61.3
28.1
3.05
28.05
66.25
11.9
25.3
68.95
10.3
0.3
28.1
5.55
16
8.2
24.4
53.05
2.5
PC £160
100
4.85
21
30.8
67
1.85
19.45
44.55
24.35
4.6
29.1
51.8
17.75
27.45
43.9
14.85
1.85
25.5
5.6
19.15
10.85
70.55
24.3
7.75
SR 20-39
100
56.45
45.45
31.55
56.5
56.5
18.2
37.5
56.45
56.45
21.25
66.2
56.5
20.15
69.8
56.5
0
0
0.8
0
0
31.25
43.5
SR 40-79
100
54
48.7
79.95
69.25
38.25
48.95
79.9
86.1
41.3
83.85
83.85
40.2
85.25
79.95
8.5
2.9
11.15
2.85
58.55
42.7
0
SR 80-159
100
39.2
0
15.55
54.45
24.95
46.8
63.6
60.2
18.75
19.55
62.1
19.05
0
42.8
2.1
23.55
27.25
18.15
45.4
2.25
SR £160
100
31.55
47.15
50.65
52.65
32.9
57.7
64.4
41.25
50.35
54.9
41.55
31.55
21
0
8.25
0
68.45
52.3
2.7
SEL 20-39
100
57.8
18.2
37.5
97.25
72.25
21.25
77.4
68.4
20.1
<-7
100
0
0
0.8
0
50
31.3
0
SEL 40-79
100
52
79.7
57.75
74.65
51.05
64.3
79.8
48.05
{ 8
57.8
15.55
26.65
29.9
26.6
50
65.65
0
SEL 80-159
100
64.8
20.95
20.95
85.75
30.2
49.7
85.75
28.2
18.2
47.65
21.75
31
22.7
27.3
77.25
4.6
SEL £160
100
37.45
59.75
60.45
44
59.5
57.45
47.5
37.5
24.95
37.5
40.8
37.5
37.5
75.05
0
SIR 20-39
100
73.4
24
80.15
70.55
21.5
76.65
97.25
0
1.4
2.15
1.35
49.95
31.2
1.4
SIR 40-79
100
48.7
79.95
88.75
46.7
82.27
72.3
21.2
1.3
8.55
1.25
53.95
53.5
1.15
SIR 80-159
100
34.15
50.05
86.1
31.25
21.3
37.4
16.7
27.45
19.15
40.05
72.5
3.05
SMD 20-39
100
77.3
29.55
92.9
77.4
6.45
2.15
6.5
3.2
50
37.75
12.4
SMD 40-79
100
50.15
78.4
68.4
17.15
10.45
16.9
9.6
54
53.25
1.6
SMD 80-159
100
30.15
20.1
45.8
14.5
23.55
15.25
33.85
80.4
0.05
PST 20-39
100
76.7
9.95
0
3.3
0
50
41.25
13.3
PST 40-79
100
0
0
0.8
0
50
31.3
0
PST 80-159
100
1.4
2.45
0
0
42.8
2.25
CM 20-39
100
77.75
73.55
0
18.8
1.4
CM 40-79
100
87.5
5.8
22.05
0
CM 80159
100
0
18.75
0
SA 4079
100
31.25
0
SA 80-159 100 0


92
Table 5-10. Food items of small juvenile piranhas (Size Class 1,10-19 mm SL),
tentatively identified as Pygocentrus cabe, from the Apure River drainage (Cao
Caicara area). %0=percent frequency of occurrence (nonempty stomachs); N = mean
number per nonempty gut; %D = percent dominance; and %Va = percent adjusted
volume.
Number examined
Number empty
Food items
%0
N
114
3
%D
%Va
Plant material
5.4
nda
-
-
Microcrustaceans
91.0
27.5
54.8
58.1
Aquatic insects
73.0
3.4
37.9
36.9
Other invertebrates
12.6
0.2
4.0
2.3
Other
7.2
nda
3.2
2.7
a Not determined/not applicable


137
Many piranhas feed on small amounts of plant material, therefore using frequency
of occurrence as a measure of herbivory tends to over-emphasize the importance of small
plant items that in reality may not contribute much to the overall diet To overcome this
possible bias. Figure 6-8 summarizes the diet data in terms of the degree of herbivory using
three different diet measures including percent adjusted volume (%Va), percent dominance
(%D), and percent frequency of occurrence (%0) (for explanation of determination see
Chapter 3). Based on the data given in Figure 6-8, one-tailed Mann-Whitney U-tests were
used to determine whether forest piranhas (> 80 mm SL), as a group, were more
herbivorous than their savanna counterparts (Table 6-10). In each case (i.e., using %Va,
%D, and %0) the resulting probability (P) values fell between 0.07 and 0.05. As
previously mentioned, seven of the eleven piranha species were found in both the Llanos
and the upper Orinoco. In five of these seven wide-ranging piranha species, plant material
(in terms of %Va, %D, and %0) was greater in upper Orinoco populations than those from
the Llanos (Fig. 6-8). Four species (including three herbivorous species) showed fairly
substantial differences between regions. Serrasalmus rhonibeiis was the only species in
which samples from forest populations contained less plant food than those from savanna
sites.
Although primarily a carnivore, Serrasalmus manueli was one of the few Orinoco
species that was relatively common in both the low Llanos (i.e., Capanaparo River
drainage) and the upper Orinoco (e.g., Sipapo and Atabapo rivers) and also fed to some
extent on seeds. Figure 6-9 summarizes and compares diets of S. manueli Llanos
populations with samples from the upper Orinoco. Considering only individuals > 80 mm
SL having food in their stomachs, two of 24 S. manueli examined from the Llanos
contained plant material whereas 16 of 37 individuals taken in the upper Orinoco contained
seeds or other plant remains. The two Llanos S. manueli containing plant material in their
stomach were larger than 160 mm SL.


Table 5-9. Food items of Catopon ment from the Apure River drainage (Cao Caicara area) by size class. %0 = percent
frequency of occurrence; %D = percent dominance; and %Va = percent adjusted volume. N = 104.
Size class (mm, SL)
II (20-39)
III (40-79)
IV (80-159)
Number examined
51
50
3
Number empty
0
0
0
Food items
%o
%D
%va
%o
%D
%Va
%0
%D
%Va
Plant material
25.0
2.0
2.1
50.0
19.0
16/1
33.3
33.3
28.6
Microcrustaceans
2.0
-
-
-
-
-
-
-
-
Aquatic insects
2.0
-
-
-
-
-
-
-
-
Other invertebrates
3.9
2.0
1.4
-
-
-
-
-
-
Small whole fish
-
-
-
4.0
3.4
5.0
-
-
-
Fish flesh
-
-
-
2.0
1.7
2.5
-
-
-
Fish fins
-
-
-
2.0
1.7
0.8
-
-
-
Fish scales
100.0
96.1
96/4
100.0
74.1
75.6
100.0
66.7
71.4


Fig. 6-4. Diets by size class (>80 mm SL) of four serrasalmine species from the upper Orinoco River basin:
Catoprion ment, Myleus asterias, M. schomburgkii, and M. torquatus. Size of segments represents
percentage of volume of each prey type; n = number of stomachs examined; numbers in parentheses
represent diet breadth using formula of Levins (1968).


208
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Richards, editors. Biology of the integument 2: vertebrates. Springer-Verlag,
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Whitfield, A. K., and S. J. M. Blaber. 1978. Scale-eating habits of the marine teleost
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Whitmore, T. C. and G. T. Prance (editors). 1987. Biogeoraphy and Quaternary history
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Wiens, J. A., J. F. Addicott, T. J. Case and J. Diamond. 1986. Overview: the importance
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Winemiller, K. O. 1989a. Ontogenetic diet shifts and resource partitioning among
piscivorous fishes in the Venezuelan Llanos. Environmental Biology of Fishes
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Wolda, H. 1981. Similarity indices, sample size and diversity. Oecologia 50:296-302.
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Haven, 187 pp.


36
effectively pull the seine forward, a seine was set stationary, and one or more "kickers"
drove fishes from the vegetation into the net.
Nylon bag seines (6x2 m with 2x2 m bag, 6.4 mm mesh) or large beach seines
(10x2 m, 6.4 mm mesh) were used in more open shallow water habitats. These nets
sampled for a broad range of fish sizes, but because few areas had clean substrates, large
seines were usually limited to open beaches along rivers or streams, and lagoons, where
there was little submerged debris.
Nylon and monofilament gill nets with float lines were used to sample selectively
for medium and large-sized fishes, including adult and subadult piranhas. Gill net sizes
were 20x2 m (20 cm stretch mesh), 10x5 m (5 cm mesh), 50x2 m (with two 25-m long
panels of 5 and 7 cm mesh, respectively), and 100x2 m (6 cm mesh). For taking piranhas,
gill nets were set in areas with little or no current, used in conjunction with seines, and in
deeper water (>1.5 m) where use of seines was impractical. Set gill nets were monitored
and all fish removed every 0.5 to 6 hours, depending on time of day and local fish
abundance. Because piranhas can damage gill nets, nets set in areas with high piranha
densities were checked more frequently.
All piranha species occurring in the Orinoco River basin take baited hooks (personal
observation). Hook-and-line fishing was done mostly with natural bait, using hand lines
and occasionally rod and reel. Different sizes and types of commercial hooks were used to
sample for fishes of different sizes. Type of bait employed was noted so as to not be
mistakenly recorded later as part of their natural diet. In general, sampling by hook and
line yielded the same piranha species, and proportions of individuals, as those caught by
gill net.
Overall, piranha species that were common in any one area were taken by two or
more types of sampling gear. No one capture technique seemed to be selective for a
particular piranha species, or group of species. Seines, gill nets, cast nets, and hook and


Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
TROPHIC ECOLOGY OF PIRANHAS (CHARACIDAE: SERRASALMINAE)
FROM SAVANNA AND FOREST REGIONS
IN THE ORINOCO RIVER BASIN OF VENEZUELA
by
Leo G. Nico
December, 1991
Chairman: Dr. Horst O. Schwassmann
Major Department: Zoology
This study emphasizes interspecific and intraspecific comparisons of the trophic
ecology of piranhas (Characidae: Serrasalminae) from two vegetatively distinct regions in
the Orinoco River basin of Venezuela: (1) the upper Orinoco in the Federal Amazon
Territory, an area dominated by dense tropical forests, and (2) the low Llanos of Apure
State, a region characterized by immense open savannas. Eleven piranha species were
taken from the two regions studied. Since 1979, ten species have been collected from the
low Llanos of Apure State, whereas my 1989-1991 samples indicate that at least eight
species occur in the upper Orinoco. Seven species were widely distributed and inhabited
both regions. The high similarity in species composition between the two regions suggests
that there are really no distinct savanna versus forest piranha assemblages.
All piranhas exhibit changes in diet with age. The smallest juveniles, < 20 mm
standard length (SL), prey mainly on microcrustaceans and small aquatic insects. Older
juveniles of most species, between 20 and 80 mm SL, commonly eat fins. Fin eating by
xii


CHAPTER 3
METHODS
Field Sampling
In the field I tried to collect as many individuals, sizes, and species of serrasalmine
fishes as possible from each region and drainage, but I did not attempt to measure fish
biomass. Sampling of fishes was done in all major habitats using appropriate combinations
of collecting gear and fishing tactics so as to obtain the most information in a short period
of time. Although piranhas were taken in greatest numbers during the day, especially near
twilight, night collections were also made in the two major regions studied. For sampling
piranhas, I depended mainly on various combinations of seines, gill nets, cast nets, and
hook and line. Harpoons, spear gun, minnow traps, trotlines, and commercial
(5% rotenone) and natural (barbasco) fish toxicants were used only rarely; these capture
methods contributed little to the total sample of serrasalmine fishes taken. In the field, most
fishes collected were preserved immediately in 10-20% formalin; in the laboratory,
preserved specimens (those less than about 200 mm SL) were transfered to 70% ethanol or
35% isopropanol. A few young piranhas were kept alive and maintained in aquaria.
Each type of sampling gear targeted a certain size range of fishes. For collecting
young piranhas and other small fishes, I used small nylon seines (6x2 and 5x2 m, 6.4 mm
mesh), nylon and monofilament cast nets ranging from 1.8 to 3 m diameter (2 to 2.5 cm
mesh), and hand nets (3 mm mesh); these were normally limited to use in shallow areas
(<1.5 m deep). Small seines and hand nets were the most effective equipment for sampling
in areas with dense aquatic vegetation. In instances where vegetation made it difficult to
35


13
those of S. marginatus (n = 4) held fish and fish remains. Both species were found
primarily in floodplain lakes or side channels, as opposed to the main river.
The relationship between piranha feeding patterns and environment had not been
investigated in any detail, however, until Goulding (1980) studied the diets of medium and
large-sized adult fishes, including seven piranha species, from in and around the Machado
River, a Clearwater tributary of the turbid-water Madeira River in Amazonia Brazil, a region
of seasonally inundated forests. He found that large Serrasalmus rhombeus (n = 254), the
most common piranha taken, were primarily piscivores that often bit chunks of flesh out of
large fish. Of added interest, fruits and seeds made up an estimated 10 percent of the total
volume of food eaten by S. rhombeus. Adult S. elongatus (n = 85) collected by Goulding
were similar to the juveniles examined by Roberts in that they had fed heavily on fins and
scales. Goulding reported that five of the seven species fed heavily on seeds, which they
masticated before swallowing. These five piranhas, which were relatively uncommon in
samples, included Serrasalmus serrulatus (n = 36), Serrasalmus cf. striolatus (n 9), and
three unidentified Serrasalmus species (n = 5?). Goulding concluded that Amazonian
fishes had evolved a close interrelationship with lowland forests, and that many fishes
depended on flooded forests for food in the form of fruit, seeds, and other allochthonous
materials. In addition to being seed predators, Goulding (1983) later indicated that
piranhas sometimes took seeds whole, and suggested that these fish also acted in dispersal
of seeds.
After Goulding completed his work in the Madeira River basin, he was joined by
Carvalho and Ferreira (Goulding et al. 1988) in a study on the natural history of
Amazonian fishes in habitats associated with the main channel of the lower Rio Negro. Of
approximately 450 species taken in the Rio Negro, six were piranhas. They did not
discuss piranha diets in much detail, but reported that fin and scale eating by adult piranhas
seemed to be common. Their collections of juvenile piranhas from the Rio Negro are yet to


158
Table 8-1. Orinoco River basin piranhas categorized by adult diet (L = Llanos; U = upper
Orinoco).
Largely Carnivorous
Largely Herbivorous
Pygocentrus caribe (L, U)
Serrasaimus altuvei (L, U)
Serrasalmus elongatus (L)
Serrasaimus ini tans (L)
Serrasalmus manueli (L, U)
Serrasaimus medinai (L)
Serrasalmus rhombeus (L, U)
Pygopristis denticulatus (L, U)
Serrasalmus cf. eigenmanni (L, U)
Pristobrycon striolatus (L, U)
Pristobrycon sp. (U)


S.L. (mm)
PYGOCENTRUS SERRASALMUS
CARIBE RHOMBEUS
SERRASALMUS SERRASALMUS
ELONGATUS IRRITANS
SERRASALMUS SERRASALMUS PRISTOBRYCON
MEDINAI ALTUVEI STRIOLATUS
CATOPR ION
MENTO
20-39
40-79
80-159
>160
n=84 (5.92) n=15(1.52)
n=29 (1.06)
n=80 (4.13) n=53 (3.27)
Plant material
Decapoda
n=12 (1.62) n=i 08)
n=162 (1.76) n=58 (2.02) n=3 (2.00) n=1 (1.00) n=50(1.66)
n=146 (3.13) n=10 (3.42) n=5(2.91)
\ \
/ .
\ \
Microcrustacea
Aquatic Insects
n=3 (1.69)
-4


172
conditions, especially in forested habitats. Perhaps the best examples of carnivorous
piranhas adjusting its diet to local conditions are individuals of Serrasalmus manueli that
had fed on seeds and fruits in the flooded forests of the Sipapo River.
Generalist versus Specialist
In his analysis of avian diets, Sherry (1990) discussed the subject of specialist
versus generalist from both ecological (i.e., tactical) and evolutionary (i.e., strategic) points
of view, also taking into account other closely related dichotomies (e.g., stereotypy vs.
plasticity, monophagy vs. polyphagy, specialized vs. opportunistic). Ln a study of insects,
Fox and Morrow (1981) found that many herbivorous species have generalized diets over
their entire geographical ranges but that they may function as specialists with restricted diets
in specific areas.
Diet breadth, as estimated by Levins' index (see Chapter 3), measures the diversity
and evenness of resource use. Thus, diet breadth is actually a quantitative attempt to
measure the degree of dietary specialization (i.e., the resulting value being lower for a
dietary specialist and higher for a dietary generalist). Unlike many dominant predators
found in freshwater communities, piranhas are little limited by gape size (i.e., not gape-
limited predators sensu Zaret 1980) because they use their teeth to cut out bite-size pieces
even from fairly large food items. Nevertheless, because larger piranhas are able to attack
or ingest a wider range of food sizes than smaller conspecifics, it would be expected that
diet breadth would increase with increasing fish size.
Although I found that diet breadth among piranhas usually changed with age, there
was no consistent pattern among species. The lowest diet breadth measured during my
study were for species and size classes considered to be scale eaters and fin eaters, fairly
specialized types of feeding behaviors. Nevertheless, species or size classes that specialize
on the fins or scales of other fishes can choose to attack many different fish species and
select from a wide range of prey fish sizes. In most instances, it was not possible to


16
catches, suggest an early morning peak of activity in Pygocentrus nattereri, Serrasalmus
elongatus, and S. rhombeus, and a late afternoon peak for the latter two species. Nico
(1990) found that young Pygocentrus notatus ( = P. caribe) had a peak feeding activity in
the morning, whereas adults seemed to be more active near dusk.
Intestine length of a few piranha species has been measured by Braga (1954),
Luengo (1965), Bonetto et al. (1967), and Jgu and dos Santos (1988). Braga reported
that the digestive tract of Serrasalmus rhombeus averaged 1.4 times the standard length.
Luengo (1965), relating intestine length to natural diet, reported that the highly carnivorous
Serrasalmus nattereri ( = Pygocentrus caribe) taken in the Venezuelan Llanos had a short
intestine compared with that of Prochilodus reticulatus (= Prochilodus mariael), a
prochilodid fish that feeds primarily on organic mud and detritus. Martinez (1976:67)
studied the anatomy of what was identified as Serrasalmus nattereri ( = Pygocentrus caribe)
and reported 10 to 12 intestinal caeca originating near and slightly past the pylorus. In a
taxonomic treatment, Jgu and dos Santos (1988) provided information on intestine length
and number of pyloric caeca for several piranha species from the Rio Tocantins of Brazil,
but they did not suggest dietary correlations.
Organization of Dissertation
The content and sequence of the chapters reflect the major components of my study.
Chapter 2 provides an overview of the Orinoco River basin and describes the environment
of the two study regions. Chapter 3 identifies the study sites and details field and
laboratory methods used. Chapter 4 compares the species composition of piranha
assemblages between the two regions and among the different drainages. Chapter 5
presents results from long-term studies on the trophic ecology and natural history of
savanna populations of piranhas from a site in the Apure River drainage. Chapter 6
focuses on the trophic ecology of populations of serrasalmine fishes from six drainages in


189
Other Serrasalmine Fishes
Catoprion ment
Llanos: UNELLEZ module.-1979: MCNG 9422 (2-2). 1980: MCNG 4428 (1-
1); MCNG 5897 (10-10); UF 37061 (1-0). 1981: MCNG 1986 (1-1); MCNG 2055 (5-5);
MCNG 2179 (1-1); MCNG 4866 (1-1). 1984: MCNG 10708 (31-31). 1985: MCNG
11385 (78-5). Cao Maporal.-1980: MCNG 6070 (6-6); MCNG 9111 (8-8). 1981:
MCNG 5765 (5-5); MCNG 7655 (6-6); MCNG 9179 (1-1); MCNG 9358 (1-1); MCNG
10219(1-1); UF 77720 (1-0). 1982: MCNG 7046 (3-3). 1983: MCNG 10071 (13-13).
1984: MCNG 11374 (2-2); MCNG 11375 (1-1). 1989: MCNG 23388 (1-1)
Upper Orinoco: Ocamo River drainage: 1990: MCNG 23415 (2-2). Mavaca River
drainage: 1991: MCNG 25403 (1-1); MCNG 25404 (1-1); MCNG 25362 (1-1); MCNG
25353 (1 1); UF 85217 (1-1).
Metvnnis spp.
Llanos: Apure River drainage: 1984: LN 84-7 (1-1). 1985: MCNG 11508 (17-
3). 1989: MCNG 23174 (6-1); MCNG 23145 (3-1); MCNG 23178 (1-1); MCNG 23161
(1-1).
Upper Orinco: Mavaca River drainage: 1991: MCNG 25333 (1-1); MCNG 25360
(1-1); MCNG 25411 (2-2); MCNG 25363 (1-1); LN 91-19 (2-1); LN 91-45 (1-1).
Mylens asterias
Upper Orinoco: Mavaca River drainage: 1991: UF 85212 (2-0); MCNG 25334
(11-2). Matacuni River drainage: 1990: MCNG 23381 (1-1); MCNG 23379 (1-1);
Ocamo River drainage: 1990: MCNG 23380 (8-8); MCNG 22288 (5-4); MCNG 22412
(4-3); MCNG 22413 (1-1); MCNG 22408 (2-2); MCNG 23416 (16-14).