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Foraging and reproductive ecology in a community of bats in Panama

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Foraging and reproductive ecology in a community of bats in Panama
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Bonaccorso, Frank J
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English
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vi, 122 leaves : ill., map ; 28 cm.

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Subjects / Keywords:
Animal feeding behavior ( jstor )
Bats ( jstor )
Canopy ( jstor )
Female animals ( jstor )
Food ( jstor )
Forests ( jstor )
Fruits ( jstor )
Insects ( jstor )
Rainy seasons ( jstor )
Species ( jstor )
Bats -- Panama -- Canal Zone ( lcsh )
Bats -- Feeding and feeds ( lcsh )
Bats -- Reproduction ( lcsh )
Dissertations, Academic -- Zoology -- UF
Zoology thesis Ph. D
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bibliography ( marcgt )
theses ( marcgt )
non-fiction ( marcgt )

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Thesis:
Thesis--University of Florida.
Bibliography:
Includes bibliographical references (leaves 115-119).
Additional Physical Form:
Also available online.
General Note:
"This study was submitted as partial fulfillment of the Ph.D. degree...".
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Frank Joseph Bonaccorso.

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University of Florida
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FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUI1rY
OF BATS IN PANAMA







By



FRANK JOSEPH BONACCORSO














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










UNIVERSITY OF FLORIDA 1975

























This work is dedicated to Clark Sanford, Julie Wiatt, and Bill

Biven, my field assistants, who endured a year of damp weather, irritating insects, bat bites, tough pork chops, and numerous other tropical hardships, yet shared the enumerable joys we encountered. We learned much together of tropical forests and ourselves arid are better people

for it.















ACKNOWLEDGMENTS

This study was funded by NSF Grant GB-36068 to Dr. J. H. Kaufmann, NIH Biomedical Sciences Grant No. RR7021-07 from the Division of Sponsored Rsearch of the University of Florida to Dr. S. R. Humphrey, and the Environmental Sciences Program of the Smithsonian Tropical Research Institute. The Florida State Museum and Smithsonian Tropical Research Institute provided logistical support.

Dr. B. K. McNab, both in his writings and classroom discussions, induced and encouraged the "germplasm" of interest which launched me into the study of the ecology of tropical bat communities. Drs. S. R. Humphrey, J. H. Kaufmann, E. Leigh, N. Smythe, A, F. Carr, D. H. Hirth, and T. C. Emmel unselfishly took time to provide constructive guidance. Dr, Robin Foster verified my seed identifications and cultured in me a deep appreciation for tropical plant ecology, Clark Sandford, Julie Wiatt, Bill Biven, and Janet Hall faithfully assisted with fieldwork and laboratory preparations under trying conditions. The creative talents of Nancy Halliday and Sylvia Scudder have rendered the illustrations. Finally, I wish to thank the scientists, students, and visitors coinciding with my residence on BCI, as well as the Smithsonian staff, for bringing encouragement, friendship, intellectual atmosphere, and volleyball to an isolate field station and making 1973 the most pleasant and memorable year I have experienced.

iii











TABLE OF CONTENTS

Page

AKNOWLEDGEMENTS ................................................... iii

ABSTRACT .......................................................... v

INTRODUCTION ...................................................... 1

STUDY AREA ........................................................ 3

MATERIALS AND METHODS ............................................. 6

Mathematical Formulae ........................................ 10

PHENOLOGY AND FOOD RESOURCES ...................................... 12

SPECIES DIVERSITY ................................................. 20

RESOURCE PARTITIONING ............................................. 27

Canopy Frugivore Guild ....................................... 31
Groundstory Frugivore Guild .................................. 50
Scavenging Frugivore Guild ................................... 62
Nectar-Pollen-Fruit-insect Omnivor6 Guild .................... 65
Sanguivore Guild ............................................. 70
Gleaning Carnivore Guild ..................................... 73
Slow-Flying Hawking Insectivore Guild ........................ 80

REPRODUCT ION ...................................................... 87

Canopy Frugivore Guild ....................................... 87
Groundstory Frugivore Guild .................................. 94
Scavenging Frugivore Guild .................................... 97
Nectar-Pollen-Fruit-Insect Omnivore Guild .................... 97
Sanguivore Guild ............................................. 97
Gleaning Carnivore Guild..................................... 97
Slow-Flying Hawking Insectivore Guild ........................ 98

CONCLUSIONS ....................................................... 101

Species Diversity And Phenology ............................... 101
Foraging And Reproductive Strategies ......................... 104

LITERATURE CITED ................................................... 115

A PPEND IX ........................................................... 120

BIOGRAPHICAL SKETCH ................................................ 122

iv















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



FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUNITY OF BATS IN PANAMA



By

Frank Joseph Bonaccorso

August, 1975


Chairman: Dr. John H. Kaufmann Major Departmet nt: Zoology

Resource partitioning, reproduction, species diversity, and community structure in a forest community of 35 bat species were studied on Barro Colorado Island, Panama Canal Zone. Sixteen months of fieldwork w ere conducted between July 1971 and August 1974. Over 2,800 bats were captured, banded, and released with data collected on food habits.. activity cycles, habitat selection, reproductive timing, and morphological feeding adaptations for each species. Information on the seasonality and abundance of fruit, flower, and insect resources

used by bats also was collected.

The diversity of tropical lowland bat communities in any one

habitat changes significantly on a seasonal basis. Fluctuating levels of food resources require that many species utilize different habitats and foraging strategies through a year. Competitive interactions, predator avoidance, and climatic fluctuation further influence the

v









foraging strategies of each species, Tropical bat faunas can be broken down into feeding gUilds on the basis of general food habits and method of food procurement. Within the most complex guilds, such as the canopy frugivore guild, food resources are partitioned in time and space and by size and quality, Within the simplest guilds food resources are partitioned primarily by food particle size. The most important mechanism of resource partitioning separating similar species is food particle size. Some species complexes appear to be limited not by absolute amount of food but by the distribution of those resources in a few concentrated patches accessible to only a limited number of individuals at a given time. Reproduction coincides with high levels of available food resources within each feeding guild.


































vi
















INTRODUCTION

Mention of the words "tropical forest" among ecologists typically triggers visions of species rich communities, complex competitive interactions, and relatively stable environmental conditions. Indeed, faunal lists in the tropics are large,and food webs are intricately complex. It is also true that organisms inhabiting tropical latitudes usually are subjected to less extreme environmental fluctuations than are their counterparts in temperate or polar regions. However, it is too infrequently e-mphasized that even species in tropical forests must possess behavioral flexibility to counter and survive climatic and biotic environmental change. There are two major reasons for this general lack of insight. Firstly, few detailed studies of tropical organisms have spanned periods of Lcveral years or even seasons. And secondly, the behavioral responses of tropical species to environmental fluctuations are often quite subtle. Whereas temperate animals commonly exhibit

obviou-s and dramatic reactions to seasonal change such as hibernation or long distance migration, tropical species may only need to switch food types or microhabitats, or briefly halt reproduction. Nevertheless, genetic and behavioral flexibility are requisites for survival for most tropical as well as temperate species.

Tropical bats are particularly worthwhile subjects for studies of diversity, competitive interaction, and response to environmental fluctuation because of their individual abundance and the complex taxonomic






2

and ecological communities they form. About 100 species of bats occur in each of the small countries of Central America (Hall and Kelson, 1959). It is common to find 30 to 50 species in one macrohabitat measuring a few square kilometers in area. For example Barro Colorado Island (15 sq km), Panama, currently supports populations of at least 35 species.

Among tropical bat species, few are known or suspected to reproduce year round or to specialize on constantly abundant food resources. The common vampire bat, Desmodus rotundus, is one notable exception (Wimsatt and Trapido, 1952). Instead, most bats, even in equatorial regions, are seasonally polyestrous or monestrous in reproduction (Baker and Baker, 1936; Mutere, 1970; Fleming, 1973) and make seasonal shifts in food habits (Wilson, 1971b; Fleming et al., 1972; Heithaus et al., 1975).

The objective of this dissertation is to delineate adaptive strategies used by tropical bats that enable them to survive fluctuating environmental conditions and coexist with numerous similar species in complex communities. The field work represented herein documents seasonal changes in diversity, mechanisms of resource partitioning, and reproductive timing through one complete year and portions of two other

years..
















STUDY AREA

The primary research site was on Barro Colorado Island (BCI).

Barro Colorado lies within freshwater Lake Gatun, in the Panama Canal Zone, at 9 0 10 North latitude and 79 0 51'1 West longitude. This field site was selected because it has a rich bat fauna, relatively undisturbed mature moist forest, modern living and laboratory facilities, and reference collections of animals and plants. A secondary site was located on the mainland opposite BCI at the base of Buena Vista Peninsul a.

The climate of this lowland area of Panama is warm and humid with a seven-month wet season and a three-month dry season. Dry season

months, January through March, each receive less than 60 mm of rain. Wet'season months, May through November, typically receive in excess of 250 ,mm of rain. April and December are months of transition between dry and wet seasons and receive amounts of rain that vary considerably from year to year. Thus in years when April and December are very dry, the dry season may last for five months. Average annual rainfall since 1926 has been 2,820 mm (Smythe, 1974). Monthly sums of rainfall for 1973 are shown in Table 1.

During night time sampling of bats, relative humidity under the forest canopy never fell below 80 percent. Measurements were made at

2 m above ground with a sling pyschrometer. Daily temperatures on the forest floor fluctuate from a mean minimum of 22.1 0 C to a mean maximum of 28.0 0 C with no significant seasonal variation (Smythe, 1974).

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Barro Colorado is in the Iropical Moist Forest life zone (Holdridga, 1967). This 15 km2 island is covered with mature forest that is over 60 years in age. The only human disturbance to the vegetation' osults from re-cutting forest trails and maintaining a small laboratory clearing, and an undetermined amount of illegal poaching. Further details on the geology, climate, biology, and history of the island are given by Kaufmann (1962) and Foster (1973).















MATERIALS AND METHODS
2
Seventeen sampling stations were located in an approximately 2 km

central strip of Barro Colorado Island and one station was on Buena Vista Peninsula (Fig. 1). Habitats sampled during the study are classified as mature forest (14 stations on BCI), creeks (3 stations on BCI), and second growth (I station on Buena Vista). The mature forest has a completely closed canopy and is a minimum of 60 years old in all places. Some tracts within the forest have been undisturbed for 400 years (Robin Foster, pers. comm.). The creek stations are lined w;th rich .shrub growth and the creek bed receives direct sunlight. The second growth habitat at Buena Vista is approximately 20 years old and consists of thick shrub growth and scattered small trees that form a discontinuous canopy.

Ex.cept on rare occasions v/hen nets were damaged by tree falls or vandalized by poachers, each sampling station consisted of four or six

6 x 2 m mist nets and one or two Tuttle harp traps (described in Tuttle, 1974) set across permanent trails. Nets were set in pairs at 100 m intervals, with one of each pair at ground level (0 to 3 m) and the other at subcanopy and lower canopy level (3 to 12 m). Early in the study nets were rigged in the canopy as high as 25 m above ground, but use of these nets was soon discontinued because few bats were captured in themwhich seemed to reflect a lack of much flight activity in the canopy levels. Harp traps were usually set at ground level in low, narrow tunnel-like passages created by the vegetation and trails. At a few stations where

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Nets and traps were open from sunset to sunrise 67 times between

11 January and 31 December 197/3. On 28 other nights during that period sampling was conducted for less than a full night. The total sampling during 1973 involved 4,376 net-hours, 1,213 trap-hours, and 2,324 captured bats.

In 1971, 3147 net-hours of sampling during a pilot study yielded 282 bats between 20 June and 18 August. In 1974, 454 net-hours of additional sampling yielded 278 bats between 10 June and 17 July. No harp traps were available during these times for effective sampling of small insectivorous bats.

Because Crespo et a]. (1972) and Morrison (1975) have demonstrated that vampires and fruit bats avoid flying during intense moonlight, whole-night samples were taken only between the last and first quarters of the moon. Only such whole-night samples were used to calculate species diversityand activity cycles were taken during phases of the lunar cycle that do not produce enought light to influence bat flight activity.

Nets and traps were, checked at least twice every hour for the purpose of removing bats. Whenever possible, checks were made more frequently to prevent bats from chewing out of nets. Upon removal from a net or trap each bat was placed in an individual cloth bag. Usually within an hour after capture the bats were banded and released at the sampling, station. The following data were recorded for each individual: species, hour of capture, capture location, sex, age class, reproductive condition of females, food in feces or mouth, weight, and forearm length.







10

Age classes were distinguished as follows. Infants were unable to fly and were encountered only when carried by the mother. Juveniles were able to fly but still had the infant pelage. Subadults had the adult pelage but were smaller in weight than adults and were reproductively immature. Adults possessed both adult pelage and weight.

Pregnancy, lactation, and reproductive inactivity of adult females were determined by palpation. Additionally, females could be distinguished as nulliparous or post-lactating by examining the condition of the teats.

Fecal pellets obtained from individual animals were placed in separate glassine envelopes for laboratory identification of food species. Fruits and pollens in fecal pellets were identified to species by comparing unknowns with seeds, pulp fibers and pollen grains in a reference collection assembled by the author. Pellets were collected from insectivores but remain unidentified because the hard parts of arthropods eaten by bats are masticated into tiny fragments that are difficult to identify. Pollen on the fur was collected by swabbing with a gelatin described by Beattie (1971). The pollen-containing gelatinwas then melted on slides for microscopic identification. Frequently, animals were captured with whole fruits held in the mouth. Additional information on food habits was gathered by placing plastic sheets under two roost trees of Carollia perspecillata to gather discarded fruits and fecal matter.

Mathematical Formulae

(I) Species Diversity, HI pi loge Pi, where pi is the number of the ith species divided by sample size (Shannon and Weaver, 1949).







11

(2) Equitability, E = HI/Hmax, where Hmax is the natural logarithm of the number of observed species (Sheldon, 1969).

(3) Niche breadth, loge B = -2,Pi loge Pi, in which the functions are the same as described in Equation 1. Values approaching zero indicate narrow niche breadths and specialists. Values approaching one indicate wide niche breadths and generalists (Levins, 1968).
2 2
(4) Niche overlap, CX = 2E Xi Yi/E Xi + Yi where Xi is the proportion of the ith food species in the diet of bat species X, and Yi is the proportion of the ith food species in the diet of bat species Y (Morista, 1959). I follow Zaret and Rand (1971) in considering species with overlap values greater than 0.6 to be critically similar in terms of food overlap.
















PHENOLOGY OF FOOD RESOURCES

Most of the bat species on Barro Colorado depend largely on fruit, flowers, or insects as food resources. Only a few species feed on the flesh or blood of vertebrates or non-insect invertebrates, The abundance and diversity of fruits, flowers, and insects in Central America, even in moist and wet forests, strongly fluctuate on a seasonal time scale (Foster, 1973; Smythe, 1974; Frankie et al., 1974).

Pollen and nectar on Barro Colorado are available to bats as reliable food sources only in the dry season, and only four species of flowering plants are known to be used by bats (Table 2). Two common species, Ochroma ]a.opus and Pseudobombax septenatum, flower from mid-December to mid-March. While these two species are in bloom nectar and pollen are very abundant, The other two pollen types used by bats remain unidentified. One of these is known only from February-March sampling and the other from August-September.

Fruits from 45 plant species were found to be eaten by bats on the island (Table 2). Nineteen of these species were trees, 11 were shrubs, four were vines, four were epiphytes, and seven are unknowns, Mature fruits of the species eaten by bats are available all year. There are times, however, when few fruits of only a few species are available. During 1973 a maximum of 19 fruiting species was available from midMarch to mid-April, and a minimum of 6 species was available in NovemberDecember (Table 2). Two of the fruits available in November-December, 12









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Ficus insipida and F. yoponensis, were very scarce, but Spondias radlkoferi and S. mombin were quite abundant.

Most of the plant species producing fruits eaten by bats produce

ripe fruits for periods of only one to four months. Only three species, F. insipida, F. obtusifolia, and F. yoponensis, have ripe fruits available nine or more months per year. Individuals in the populations of these fig species fruit asynchronously once or twice per year. F. insipida and F. y v.ponensis populations show three major fruiting peaks and troughs each year (Morrison, 1975).

The plant genera CeLropia, Spondias, Vismia, and Pier each have two or more bat-dispersed species that set fruit in sequential time periods (Table 2). There are 10 species of pipers on BCI eaten by bats. Though no one of these species is available for more than a few months, two or more species have ripe fruit throughout the year. Heithaus et al. (1975) report that pipers are important bat fruits in Costa Rica and that several species are available in similar sequential series. Snow (1965) reports that 18 species of the bird-dispersed genus Miconia are sequentially available throughout the year in Trinidad.

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in Barro Colorado forest over a three-year period were reported by Smythe (974). Though these samples represent all nocturnal flying insects, not just those eaten by bats, they provide a useful index of the abundance and fluctuation of the potential food resources for insectivorous bats through the year (Fig. 3). The light trap collections show that nocturnal insect biomass in the early wet season is as much as eight times that of the biomass at the end of the wet season and during the dry season (Fig. 2). Large insects (> 5 mm in length) were responsible

































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for this seasonal change in biomass, with Isoptera, Diptera, and Lepidoptera among the orders eaten by bats that have particularly dramatic population increases in the wet season. By contrast, small insects k 5 mm in length) were abundant throughout the year.
















SPECIES DIVERSITY

Considerable variation occurred in the bimonthly measures of species diversity (Table 3). All three diversity indices, H', E, and SN, were at maxima during the dry-to-wet transition sampling period. The three diversity measures then declined in each of the next three bimonthly periods to a minimum in the late-wet season. Whereas 27 bat species were present in the study area in the dry-to-wet transition, only 19 species were sampled in the late-wet season. During this same interval H' dropped from 2.33 to 1.52 and equitability from 0.707 to 0.515. In the wet to dry transition period the diversity values began to increase. Dry season values were very similar to wet-dry transition values,but SN increased from 22 to 25 in this period.

The diversity values were lowest in the mid- and late-wet season

samples because 13 of the species common in the dry season became noticeably rare or absent (indicated by asterisks in Appendix 1) from the study area in one or both bimonthly periods. These include seven insectivorous species (47%g of the total insectivorous species), five frugivorous species (42%), and one nectarivorous species (50%). These species appear to move to other habitats precisely at the time when bat-dispersed fruits and nocturnally flying insects, the two most important food resources for bats in this community, become relatively scarce on the study site (Fig.

2 and Table 2).

Of the seven insectivorous bat species that move out of the

mature forest late in the wet season, six are fol iage gleaners and one 20








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22

is an aerial hawker. The foliage gleaners prey chiefly on large insects such as cicadas, grasshoppers, and roaches (Wilson, 1971b; this study). Smythe (1974) has shown that large nocturnal insects (greater than 5 mm in length) become quite scarce on this same study area beginning in the middle of the wet season, whereas small insects (smaller than 5 mm in length) are relatively constant in abundance through the year. It appears that the foliage-gleaning bats find food resources in tile study area sufficiently depressed in the latter part of the wet season that they move out of the area. On the other hand, small insects remain an abundant food resourceand aerial feeding bats remain in the mature forest of Barro Colorado all year. Peropteryx kappleri, an aerial feeding bat, is an exception as it does move out of forest habitat in the late wet season.

Of the two bat species that are primarily nectarivorous in this

community, Glossophaga soricina switches from pollen and nectar to fruits and insects in the early wet season and then moves out of the area in the middle wet season, not to return until bat flowers appear in the dry season. Phyllostomus discolor stays in the area the entire year, subsisting on fruits and insects during the wet season.

Among the fruit-eating species that seasonally move in and out of the Barro Colorado mature forest is Vampyressa pusiIla, the smallest species of the 13 frugivorous bats on BCI. V. pusilla is a feeding specialist on small fig fruits. This bat left the study area when few individuals of its most important food species, Ficus yoponensis, were producing fruits in July-October and returned in November when mature F. Yponensis fruits were again abundant. While specific reasons why other frugivorous species moved in and out of the study site are unclear,







23

their absence in September-November corresponds with the annual period when few food plants are producing fruit (Table 2).

The abundance of individual bats on the study area, as measured by the number of bats captured per sampling-hour, showed a pattern of seasonal change markedly different from the diversity measures pattern. Bats were captured in greatest numbers relative to sampling effort in the dry--to-wet transition, 0.425 bats/hr, and in the late wet season,

0.423 bats/hr (Table 3). The large numbers of bats captured in the dryto-wet transition sampling reflect large populations. Food resources were abundant then; females of most species were in the latter stages of lactation; and juveniles were entering the flying population and learning to forage. These latter two activities are among the most energetically demanding in mammalian life cycles (MigUela, 1969; Studier et al.,

1973), and the timing of these costly activities seems geared to a period of food abundance.

The late wet season peak in capture rate does not solely reflect large numbers of individuals on the study area. Though a number of species had at this time moved out of the young forest, some of the remaining frugivorous species were recruiting juveniles into the flying population from the second birth pulse of the year. Probably much of the high capture rate is attributable to intense foraging activity necessitated by low food supplies.

The diversity values for insectivorous and frugivorous species,

when computed separately, change similarly through the seasons (Table 4). For both groups, species diversity is high from mid-November through mid-July and low the remainder of the year. Fruit bat diversity rises and falls in time as does the diversity of fruit (see Table 2). However,









24







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insectivore bat diversity sharply rises four months before insect biomass explosively increases (see Fig. 2). The latter anamoly may be due to ineffective harp trap placement and particular under-representation of the abundant species, Pteronotus_ parnelii, during the first months of field work. This would cause the dry season diversity value to be higher than it should be. Most species of fruit bats remain in the BCI mature forest habitat throughout the year. On the other hand, the species number of insect-eating bats in the dry-to-wet transition is nearly double that of the late wet season because of the movement of foliagegleaning species in and out of the forest.

A measure of annual variation is achieved by comparing the diversity of frugivorous species in June, July and August of 1971, 1973, and 1974 (Table 5). In all three years there is a consistent trend toward lower diversity as the wet season progresses. However, the magnitude of the diversity values varies from year to year. This indicates that some annually variable factor or complex of factors, possibly food availability, predation, or reproductive success, influences fruit bat species diversity. Insectivore diversity is not compared because harp traps for effective sampling were available only in 1973.








26






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RESOURCE PARTITIONING

Thirty-five species of bats were found to coexist on Barro Colorado Island in 1973. Thirty-one species were captured in diversity samples and four additional species were seen in flight or at roosts. Noctilio leporinus, N. labialis, and Molossus molossus restricted their flight activities to habitats that were not sampled--the shallow inlets of the lake (Noctilio) and above the forest canopy (Molossus). The fourth species not captured in the diversity samples, Vampyrum spectrum, is a top carnivore and may be represented by very-few. individuals on the island. A pair of V. spectrum was netted by A. L. Gardner and D. E. Wilson on 5 January 1973. I saw a single animal in June 1973 flying at dawn. No other sightings of V. spectrum were reported in 1973.

A first step at understanding how 35 species of bats coexist on

this small island can be made by dividing the fauna into feeding guilds. Feeding guilds will be distinguished on the basis of two parameters-general 'food type and method or place of food procurement. It will be assumed that little or no competition for food resources occurs between members of different feeding guilds, though they may compete for roosting space. The bats on Barro Colorado may be divided into nine feeding guilds, each of which contains one to nine species.

Justification for the placement of species into specific feeding guilds will be provided in succeeding sections. For the moment, the feeding guilds are defined as follows:

(1) "Canopy frugivores" -- forage mostly on fruits that grow in

27







28

the trees of the canopy and subcanopy level of the forest, above 3 m from the ground.

(2) "Groundstory frugivores" -- forage mostly on fruits of shrubby groundstory plants, 0 to 3 m above ground level.

(3) "Scavenging frugivores" -- feed mostly on over-ripe fruit.

(4) ''Nectar-pollen-fruit-insect oinivores" -- forage for pollen and nectar from flowering trees when available in the dry season and then switch to a fruit and insect diet in the wet season.

(5) "Sanguivores' -- feed only on the blood of mammals and birds.

(6) "Gleaning carnivores'' -- forage for small animals (arthropods or vertebrates) that are perching or moving on vegetation or on the ground.

(7) "Slow-flying hawking insectivores'' -- forage for flying insects in small openings beneath or in the forest canopy or over streams.

(8) "Fast-flying hawking insectivores'' -- forage for flying insects above the forest canopy or in very large open spaces.

(9) "Piscivores" -- forage for fish or aquatic invertebrates at or just above the surface of lakes and large streams.

The distribution of mean body weights for each bat species on

Barro Colorado by guild is plotted in Figure 3. Three guilds contain a single species, and I expect that each of these species is sufficiently unique to preclude serious interspecific competition for food. The species within the groundstory frugivore, canopy frugivore, and piscivore guilds increase in body weight with a geometric progression factor of about 1.3 to 1.8 (with one exception in the canopy frugivore guild). We might expect that the species within each of these guilds exploit very similar types of food, captured in very similar manners, and that





























Figure 3. Mean body weights of bat species by feeding guilds. (Dashed lines separate members of different families that belong to the same feeding guilds.) 1. Carollia castanet, 2. C. perspecillall,
3. Vamgyressa pusilla, 4, Thiroderma trinitatum, 5. Artibeus Ehaeotis, 6, Vamgyrops helleri, 7. Chiroderma..Vijjosum, 8. Vamp Wes caraccioloi,
9. Artibeus jamaicensjj, 10. A, lituratus, 11. Centurion yLfj, 12. Glossophaga soricina, 13. Phylloltomus discoloL, 14, Phyl]oderma stenops, 15. Desmodus rotundus, 16. Micronycteris meaplotis, 17. M, brachyotij, 18. Mimon crenulatum, 19. ronycteris hirsute, 20. TrachoRs cirEhosus, 21. Tonatia sylvicola, 22. T. bidens, 23. Phyllostomus hantatu 24, Vampyrum spectrum, 25. Rho2eessa tumida, 26. Myotis nigicans, 27. S19ccopteryx leptura, 28. Centronycteris maximilliani, 29. S2ccqpteryx bilineata 30. Peropteryx kappleri, 31. Pteronotuj sugpurensis, 32. P. Larnellii, 33. Molossus f 34. Noctilio labially, 35. N. leporinus










30

























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31

food resources are partitioned largely by particle size as predicted by the theoretical reasonings of Hutchinson (1959), McNab (1971a and b) and May (1973). These authors postulate that similar species may avoid competition for food by differing in body weights by a factor of at least 1.3 (May, but McNab and Hutchinson used the figure 2.0), each species specializing in food particles proportional to its body weight (and to the linear dimensions of its food handling apparatus, e.g., tooth row length, gape size, tongue length, etc.).

The gleaning carnivore and slow-flying hawking insectivore guilds

each contain some species that are very similar in size to other species of their guilds. We might expect that such species feed on similarsized food particles of very different taxa or of similar taxa from different microhabitats.

The nectar-pollen-fruit-insect omnivore guild contains species very different in size; this may partly result from a recent extirpation of Lonchophylla robusta, a species intermediate in size between Glossophaga soricina and Phyllostomus discolor. The sexual dimorphism in body weights of P. discolor is another complicating factor. Canopy Frugivore Guild

Body size

Eight species, all in the subfamily Stenoderminae of the Phyllostomatidae, constitute the canopy frugivore guild on Barro Colorado. These eight species range from 8.1 to 69.3 g in mean body weight (Table 6). There is a mean increment of 1.44 between the body weights of adjacently sized animals among the seven species designated as fig feeding specialists in Table 6. Artibeus phaeotis, a feeding generalist, and Chiroderma trinitatum are nearly the same in size.







32




Table 6. Weights rn grams of canopy frugivore bats on Barro Colorado.




Sample Sample Wgt / Wgt* Remarks
Species Mean size size Ig sm
(OR) (S.D.) n


V. pusilla 8.1 0.6 22 -- Fig specialist

C. trinitatum 12.3 1.2 7 1.53 very rare fig specialist

A. phaeotis 13.0 1.2 30 -- food generalist

V. helleri 16.2 2.2 8 1.31 very rare fig specialist

C. villosum 22.4 2.1 13 1.38 fig specialist

V. caraccioloi 36.0 2.3 27 1.61 fig specialist

A. jamaicensis 47.2 3.4 30 1.31 fig specialist

A. lituratus 69.3 5.6 30 1.47 fig specialist


mean ratio of weight increment=1.44






weight of larger species divided by weight of smaller species in the pair compared.







33

Food selection

All eight canopy frugivore species feed primarily on fruits of

large canopy and subcanopy trees, in particular figs of the genus Ficus. Over 60% of the annual diet (by frequency of occurrence in fecal matter) of seven of these bat species consists of fig fruits (Table 7); these include C. trinitatum, but not A. phaeotis of the same weight. A. phaeotis depends on figs for 30% of its diet. Five species of Ficus, all of which are green colored at maturity, are eaten and dispersed by these stenodermines on Barro Colorado. Fig species that produce large fruits are preferred by large batsand fig species that produce small fruits are preferred by small bats.

Figs form the bulk of the diet of Artibeus jamaicensis throughout most of the year. However, during the latter part of the wet season and the very beginning of the dry season mature fig fruits are very scarce (Morrison, 1975). At this time A. jamaicensis turns more heavily to other fruits and pollen (Table 8). The relative importance of pollen in the diet of A. jamaicensis is grossly underestimated here because my sampling schedule did not coincide with the two weeks in late December and early January when figs were very scarce and flowers were very abundant. Similar seasonal switches in diet also probably occur for A. lituratus and V. caraccioloi but the data are weak. No conclusions can be made from the scant data on the smaller species of canopy frugivores with respect to seasonal switches in diet.

Unlike the fig specialists, A. phaeotis eats a more even distribution of many types of fruits (Tables 7 and 8) with no one species strongly dominating the diet. Throughout the year figs are a minor component of the diet, while other fruits are very important in certain














34




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35




Table 8. Bi-monthly samples of important food species in the diets
of Artibeus and Vampyrodes. Sampling periods begin at
mid-month.

Food Species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan

Artibeus jamaicensis

Ficus spp. 18 25 25 35 21 17

Cecropia spp. 3 3

Spondias spp. 1 8 6

Quararibea 9

Pollen 1

Total feeding samples* 20 30 32 39 35 37

Artibeus lituratus

Ficus spp. 2 4 .2 1 4

Spondias spp. I I I

Pollen 1

Total feeding samples* 3 4 5 2 7

Artibeus phaeotis

Ficus spp. 2 1 2 1 3

Cecropia spp. 1 5

Spondias spp. 8

Total feeding samples* 5 6 9 1 11

Vampyrodes caraccioloi

Ficus spp. 1 2 4 3 1

Pollen 2

Total feeding samples* 3 3 4 3 2


*Includes genera of lesser importance not shown here.







36

months. Cecropia exim-ia is an important food item from July to September, as is Spondias radlkoferi in November to January.

Feeding niche breadths based on food species by frequency of occurrence in the diet are presented in Table 9. Large niche breadth values represent food generalists and small values food specialists. A. phaeotis stands alone at the generalist extreme of this index. A. jamacensis has an intermediate position between the generalist and the extreme specialists. The remaining six species are bunched as extreme specialists. Hereafter, all members of this guild will be referred to as 'fig specialists" except for the feeding generalist, A.phaeotis.

Niche overlap in food species is compared in Table 10. The highest values of overlap in canopy frugivores occur between species most similar in size (diagonal left edge of Table 10). A. phaeotis overlaps little with all the fig specialists, except for V. helleri, which is similar in size. The high values of overlap between many of the fig specialist species indicate that some mechanism other than selection of food species must be operable to reduce behavioral interference and/or interspecific competition for food in this guild.

Several types of evidence strongly suggest that food is a limiting factor for fruit bats on Barro Colorado, at least during some parts of the year, The biomass of fruit and the number of species of fruiting trees fluctuate quite drastically on a seasonal basis (see Phenology section). During the late wet season fruit availability is low~ and an increased, proportion of captured fruit bats have empty stomachs (83% in Oct-Nov) as compared to times of fruit abundance (71% in Mar-Apr).






37





Table 9. Feeding niche breadths of canopy frugivores.





Bat Species Number of genera of Number of species of Niche Breadth*
known food plants known food plants (loge B)


V. pusilla 2 4 0.94

C. trinitatum 3 4 1.33

A. phaeotis 10 12 2.10

V. helleri 2 3 1.01

C. villosum I 3 1.01

V. caraccioloi 4 5 1.04

A. jamaicensis 9 16 1.61

A. lituratus 5 7 1.33





*Sample sizes for calculating niche breadths are as in Table 7.






38








Table 10. Feeding niche overlaps (CA ) among species of the
canopy frugivore guild

<< I> I>

O-.*

00
rt 0




A. phaeotis .215** .354*and .615** .241** .465** .485** .518**

V. pusilla .968* .452 .796 .679 .272 .152

C. trinitatus .893* .743 .644 .209 .412

V. helleri .798* .886 .852 .452

C. villosum .727* .200 .310

V. caraccioloi .994* .962

A. jamaicensis .983*

A. lituratus






Denotes species most similar in body weight ** Denotes overlap with the feeding generalist







39

Also by the late wet season several species of fruit bats have temporarily moved out of the study areaand the remaining individuals and species spend a greater part of their nightly time budgets in foraging (see Species Diversity section). Even when fruit is very abundant in terms of total biomass, it is concentrated in a limited amount of space, the few trees fruiting at any moment, and may still be a limiting factor for population size.

Vertical stratification

Handley (1967) and Harrison (1962) demonstrated a vertical stratification of flight activity in Neotropical bat species, with most canopy frugivores preferring upper levels of the forest. On Barro Colorado, pusilla, A. phaeotis, C. villosum, V. caraccioli, and A. lituratus were captured with highly significant frequency in the nets and traps set above 3 m (Table 11). V. helleri and C. trinitatum also were captured most frequently in subcanopy-canopy levels, but sample sizes for these species are small, and frequency differences are not statistically significant. A. jamaicensis is the only species of the guild to show a significant preference for activity at the groundstory level, yet 42% of the captures of even this species were in the upper levels of the forest. Though most of its food items grow in the upper levels of the forest, A. jamaicensis may fly close to the ground to avoid predators. On the other hand this behavior may be an artifact of the human management of the forest, with this species opportunistically finding it more efficient to fly along cleared trails than to repeatedly detect and avoid vegetation at higher levels.





40





Table 11. Vertical stratification of canopy frugivore species on
Barro Colorado. Statistical significance indicates preference for one of the two vertical strata.





Bat Species No. of bats captured at No. of bats captured at
ground level, 0 to 3 mm subcanopy levels, 3 to 12 mm



V. pusilla 5 25**

C. trinitatum 2 4

A. phaeotis 36 56*

V. helleri 3 6

C. villosum 4 24**

V. caraccioloi 4 30**

A. jamaicensis 467** 326

A. lituratus 23 66**




Significant by Chi Square Test (P <.05).

** Highly significant by Chi Square Test (P < .01).

Yates Correction for Continuity is used on all tests of samples
with N < 200 (Sokall and Roh Ifl969).






141

Habitat selection

Comparison of netting samples from the young open forest of Buena Vista and the closed canopy forest and creek habitats of Barro Colorado provide a measure of species preferences for three habitats (Fig. 4). As a group the fig specialists are much more common in the closed forest and creeks lined by closed forest than in the shrubby open forest where few mature trees of their preferred food species are found. A. phaeois. and A. jamaicensis are common to very abundant in all three habitats, as would be expected from their more generalized food requirements. None of the extreme fig specialists are common on Buena Vista Peninsula. Fedn behavior

Canopy frugivores usually carry fruits by mouth from fruiting trees to night feeding roosts (Goodwin and Greenhall, 1961; Morrison, 1975). On BCI Morrison found that the night feeding roosts of A. -jamaicensis are frequently several hundred meters away from the fruiting trees where they.are picked. Only when feeding on the large fruits of Dipteryx panamensis did Artibeus feed on fruiting trees. All four most common canopy frugivore species were observed to carry whole or partially eaten fruits in flight. These animals presumably were transporting food items to a night feeding roost for consumption. Whether the less common species in the guild use night feeding roosts is unknown.

The fruits carried in flight by fruit bats vary in weight from less than 1 g to about 20 g. Most bats carry fruits that weigh 20 to 40% of their own body weight. Table 12,lists the range in weights of some fruits eaten by stenodermine bats. There is considerable variation in the weights among and within species for these fruits (even in fruits from the same individual tree).










































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44







Table 12. Wet weights in grams of some fruits eaten by bats on
Barro Colorado Island that were collected beneath
fruiting trees.




Plant Species Fruit Weights
Range Mean S. D. N



Ficus insipida 7.1-11.4 9.1 1.5 10

Ficus obtusifolia 14.2-19.0 17.0 2.5 3

Ficus yoponensis 1.5- 5.6 3.1 1.1 12

Anacardium excelsum 4.2- 6.2 5.1 0.7 7

Calophyllum longifolium 9.3-17.7 14.7 3.3 7

Dipteryx panamensis 18.0-26.3 22.3 3.6 5

Spondias radlkoferi 8.6-13.0 o10.6 1.4 9

Quararibea asterolepis 4.9- 6.3 5.45 0.6 4

Astrocaryum standleyanum 17.0-20.5 18.8 1.8 4

Piper cordulatum 0.5- 2.0 1.2 0.5 15









Food particle size plays an important role in the partitioning of food resources among similar species in many types of animals (e.g. Diamond, 1973; Brown and Lieberman, 1973) and may be particularly important for fruit bats because of the behavior of carrying fruits in flight to feeding roasts. According to the theory of optimal foraging strategy (Schoener, 1969), each bat should attempt to maximize the amount of food it harvests per unit of time and thus select the largest food particles it can efficiently find and handle. The weight that a bat can carry in flight without seriously impeding manuverability probably sets the upper limit on food particle size for these animals.

Figure 5 shows that there is a highly significant correlation (by F distribution, P <.01) of fruit weight with bat weight for fruits carried into nets by the three largest species of bats in the canopy frugivore guild. Most of the points in this figure represent Ficus insipida fruits, the most important food species in the diet of all three bat species. Thus even though these three bats have high overlap in food species (Table 10), they are able to specialize on food particle sizes proportional to their body weights. The smaller canopy frugivore species probably do the same thing, but no data are available.

Each species in the canopy frugivore guild has a distinct cycle of flight activity. The three largest species, V. caraccioloi, A. Jamaicensis, and A. lituratus, each have their greatest peaks in activity at different times of the night (Fig. 6). Since'all three of these species feed largely in the same individual trees in the course of the night, the offsetting cycles of activity probably function to minimize interspecific aggression from crowding at the resource trees, especially when resources are concentrated in a few trees per night. Reduced






























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SglDgdS HDV3 AO IVIOi AO INID 13d







50

crowding at resource trees presumably is of importance in permitting more efficient feeding and in making these bats less obvious to the many kinds of arboreal and aerial predators that eat bats (Humphrey and Bonaccorso, 1975).

A similar pattern of offsetting major activity peaks should be expected in the small canopy frugivores, all of which feed heavily on Ficus yoponensis and F. popenoaei. Figure 7 shows that V. pusilla is most active in the first two hours after sunset, and C. villosum is most active later in the night. Paucity of data prevents comparison of the other small fig specialists.

A. phaeotis, the feeding generalist, has a much more even distribution of activity through the night than any other species (Fig. 7). Many of the fruits eaten by A. phaeotis are not eaten by other stenodermine bats and it need not compromise its activity cycle to avoid crowded resource trees.

Groundstory Frugivore Guild

Body size

Two species in the subfamily Carollinae of the Phyllostomatidae

constitute the groundstory frugivore guild on Barro Colorado. They are Carollia castanea and C. perspicillata. These have mean body weights of 12.4 and 17.9 g, thus differing in body weight by a factor of 1.44 (Table 13).

A few individuals of a third species of the genus Carollia,

C. subrufa, were captured and banded by R. K. LaVal in 1972 on Barro Colorado (pers. comm.). In 1973 and 1974 I recaptured some of LaVal's banded C. perspicillata and C. castanea, but I have not encountered any of the C. subrufa he marked. It is difficult to distinguish























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53








Table 13. Weights of groundstory frugivore bats on Barro Colorado





Bat species Mean Standard Sample Weight of larger species
) deviation size divided by weight of
smaller species in the
pair compared


C. castanea 12.4 1.8 30 -C. perspicillata 17.9 1.8 30 1.44







54

C. perspicillata and C. subrufa by field characters,and it is possible that I lumped a few individuals of C. subrufa with C. perspicillata because I was not aware that C. subrufa was present on BCI. I believe C. subrufa is very rare on Barro Colorado, and lumping a few of them with C. perspicillata would influence the data on this latter species to a very minor extent.

Food selection

C. castanea and C. perspicillata are food generalists in that they eat a fairly even distribution of a large number of kinds of fruits and have large niche breadth values (Tables 14, 15, and 16). Though no one food species dominates their diet in any one season or over a long portion of the year, eleven species of the shrubby plant genus Piper (Piperaceae) constitute the bulk of the diet of C. castanea and nearly one-third of the diet of C. perspicillata. Ten species of pipers were identified in the fecal samples from C. castanea and nine species from C. perspicillata. At least one species of piper is available with mature fruit in every month of the year on Barro Colorado (see Table 2). C. castanea eats pipers all year long, but no pipers were evident in the diet of C. perspicillata from mid-September through mid-November. C. perspicillata appears to feed exclusively on subcanopy and canopy fruits in the late wet season. Particularly important are Solanum hayseii, Quararibea asterolepis and Cecropia exima. Other fruiting trees are important food species along with pipers at other seasons. Though fruiting shrubs dominate the diet of C. castanea, fruiting trees are somewhat more important than shrubs for C. perspicillata.

In addition to the fecal samples from captured animals, food habits data for C. perspicillata were obtained by monitoring droppings below







55



Table 14. Food species in the diet of C. castanea as determined from frequency of occurrence of seeds in fecal samples. Sampling periods begin at mid-month.


Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total


Shrubs

Piper aequale 3 3 3 6 15

P. cordulatum 8 1 9

P. reticulatum 1 3 1 5

P. marginatum 3 1 1 1 6

P. carrilloanum 1 1 2

Piper 109 1 1 2 4

Piper 114 1 1

Piper 120 1 1 2

Piper 122 3 3

Piper 150 2 2

Trees

Carludovica palmata 1 1

Solanum hayseii 2 2

Markea panamensis 9 1 1 11

Vismia 1 2 1 3

Brosimum bernadettae 1 1

Dipteryx panemensis I I

Aechmeia tillandsoides 1 1

Unknown

Unknown 104 1 1

Unknown 123 1 1






56



Table 15. Food species in the diet of C. perspicillata as determined from frequency of occurrence of seeds in fecal samples. Sampling periods begin at mid-month.


Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total


Shrubs

Piper aequale 1 I

P. cordulatum 10 1 II

P. reticulatum 7 7

P. marginatum I1 1 3

Piper l09 4 1 1 6

Piper 114 1 1 2

Piper 116 1 1

Piper 120 2 1 3

Piper 150 2 2

Trees

Carludovica palmata 1 1

Solanum hayseii 1 6 1 1 9

Markea panamensis 1 4 5

Vismia 1 4 5 9

Vismia 2 1 1 2

Cecropia exima 1 1 1 3

Brosimum bernadettae 3 3

Quararibea asterolepis 6 6

Dipteryx panamensis 7 1 8

Cassia undulata 3 3







57

Table 15, continued,



Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total




Unknown 101 1 1

Unknown 103 1 1

Unknown 104 1 1

Unknown 125 4 4

Unknown 127 2 2

Insects 5 1 6









58





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59

two day roosts of this species. Both roosts were in hollow Anacardium excelsum trees. With the exception of A. excelsum all common food items identified from the day roost droppings appeared as important food items in the fecal samples from captured bats during the same bimonthly periods (Table 17).

Why did not A. excelsum ever show up in the fecal material from captured bats? Probably A. excelsum is the only tree species that commonly serves as both a day roost and an important food resource for C. perspicillata. These bats need only fly to the canopy of the roost tree, pick a fruit, and carry it back inside the roost to eat it. The bats would usually digest and excrete the fruit before flying away from the roost to forage for other fruits; thus little chance would exist for this pulp to show up in netted animals. The Carollia colonies in A. excelsum trees consisted only of 6 to 8 bats and each colony probably had access to more A. excelsum fruits when in season than they could eat.

Anacardium excelsum is the only fruit I know to be eaten by bats

on Barro Colorado that is not dispersed. Not only are the fruits carried within the hollow parent tree, but it is the single, large seed and not the fruit' pulp that is eaten. However, a few seeds probably are dispersed when dropped by mistake.

Overlap between the diets of the two Carollia is moderate in terms of food species. A CX value of 0.584 is obtained from lumping the food habits data from fecal samples from the entire year. Food overlap was very high in May-July sampling, CA = 0.798. This latter value, as well as the annual value of overlap, would be considerably smaller if it were possible to correct for Anacardium eaten in roost trees by C. perspicillata. Even though roosts were not monitored, it is unlikely that





60




Table 17. Frequency of occurrence of food species in the diet of C. perspicillata as determined from fruit droppings and seeds below day roosts. Sampling periods begin at mid-month.




Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan*Total



Anacardium excelsum 5 83 39 127

Piper cordulatum 39 35 9 83

P. reticulatum 6 6

Piper 109 6 6

Solanum hayseii 1 1 2

Vismia 1 2 2 4

Quararibea asterolepsis 5 15 20

Cassia undulata 5 1 6

Unknown 155 12 12

Unknown R-l 3 3




* No data.







61

C. castanea eats much of this fruit, as it is larger than all other important fruits in the diet of C. castanea. Habitat selection

Of the three habitats sampled, the Carollinae were most common in the second growth forest and least common in the mature forest, as are their most important food plants. C. castanea accounted for 21.7% of all bats captured in the second growth forest, 2.7% of the bats in the creeks, and 1.4% of the bats in the mature forest (Fig. 6). C. perspicillata constituted 15.8%, 16.0%, and 5.4% of the bat individuals captured in those habitats. Whereas many species of pipers grew abundantly in the sunlight of the open canopy second growth and along the creeks (though less so along creeks), only one species, P. cordulatum, was abundant in the shade of the mature forest. Vertical stratification

C. castanea and C. perspicillata were both captured more frequently at ground level than at upper levels of the forest (C. castanea = 20 ground level, 14 upper levels; C. perspicillata = 50 ground level, 34 upper levels), but the difference was not statistically significant. Both species feed on plants of ground and canopy levels. Known groundstory fruits make up 78.4% of the diet of C. castanea and 38% of the diet of C. perspicillata. During seasons when C. perspicillata is feeding mostly on canopy fruits, it also is captured more frequently in high nets and traps.

Feeding behavior

Carollia castanea and C. perspicillata both have been captured

carrying fruits in the mouth and presumably use night feeding roosts as do canopy frugivores. Some fruits are carried back to the day roost







62

for consumption as already discussed. The use of day roosts as feeding places by C. perspicillata is mainly a phenomenon related to feeding on one fruit, Anacardium excelsum, as is evident from the dominance of this fruit below day roosts and the decrease of dropped fruits and seeds when A. excelsum is not in fruit (Table 18). It is likely that temporary night feeding roosts are used by these bats to avoid making the day roosts conspicuous to predators and to reduce flight distances between foraging forays.

The flight activity of Carollia through the night is presented in

Figure 8. Both species show major peaks of flight activity in the first hour of darkness. This is much earlier than the start of most canopy frugivores' flight activity and is probably due to the groundstory becoming dark about an hour before the canopy level of the forest. Cycles of flight activity in groundstory frugivores are bimodal or trimodal as are those of canopy frugivores. Two or three such bouts of diel feeding activity also have been observed in fruit bats by Brown (1968) and LaVal (1970) and seem characteristic of bats that feed on foodstuffs that are not efficiently assimilated. Scavenging Frugivore Guild

Body size

Centurio senex (Stenoderminae, Phyllostomatidae), the wrinkle-faced bat, is the sole member of the scavenging frugivore guild. A lactating female weighed 22 g and a pregnant female weighed 27 g. No other weights are available from Barro Colorado for this species, nor are there any useful data on vertical stratification or habitat selection.






















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65

Food species selection and feeding behavior

From several morphological features, particularly the small teeth and narrow esophagus, Paradiso (1967) concluded that C. senex probably feeds on a "soft fruit or fluid diet". The small teeth, narrow esophagus, and lack of facial hair (like vultures) on this bat are suggestive of its possibly feeding on over-ripe or decaying fruit. Hence I tentatively designate it a "scavenging frugivore". The amount of rotting fruit on the forest floor is incredibly large on Barro Colorado and potentially could provide an abundant food resource for such a bat. Goodwin and Greenhall (1961) mentioned finding fruit pulp in stomachs of C. senex from Trinidad. Of the individuals that I captured on Barro Colorado one defecated an unidentifiable fruit pulp and the other carried a fresh Spondias radlkoferi fruit in its mouth. At this time it can neither be confirmed nor disproved that Centurio is a scavenging frugivore. Though it is very similar to Chiroderma villosum in body size I haye no doubt that this anatomically unusual bat is ecologically quite different from any other frugivorous species on Barro Colorado with respect to food habits.

Nectar-Pollen-Fruit-Insect Omnivore Guild Body size

The nectar-pollen-fruit-insect omnivore guild (hereafter referred to as the omnivore guild) contains three species, all of the family Phyllostomatidae -- Glossophaga soricina (Glossophaginae), Phyllostomus discolor (Phyllostominae), and Phylloderma stenops (Phyllostominae). The mean body weight for P. discolor on Barro Colorado is 4.36 times larger than that of G. soricina (Table 18), a larger difference than is found between species adjacent in size in any other guild. The large







66

Table 18. Weights in grams of omnivore bats on Barro Colorado.







Bat species Mean Standard Sample Wgt f Wgt *
(x) Deviation size ig sm
(S. D.) (N)



G. soricina 9.8 1.0 9 -P. discolor 42.8 3.9 27 4.36

male P. discolor 44.6 3.6 17

female P. discolor 39.7 2.1 10 -P. stenops 61.0 -- 1 1.42










'Weight of larger species divided by weight of smaller species in the pair compared.







67

gap in body weight between G. soricina and P. discolor exists because of the recent extirpation of a bat species belonging to this guild. As recently as the early 1950's, Lonchophylla robusta (Glossophaginae), was alive on Barro Colorado (Hall and Jackson, 1953). This species eats nectar, pollen, fruit, and insects (Howell and Burch, 1974). L. robusta from Costa Rica weigh about 17 g~and if this species were still present on Barro Colorado the ratios between body weights of the four omnivore guild members would be 1.4, 2.6, 1.4. The large ratio between L. robusta and P. discolor actually would have been somewhat less than 2.6 because of the sexual dimorphism in body weights of P. discolor. The dimorphism in body weights between male and female P. discolor is very slight (Table 18) but significant (P <.05, Student's t-test). Food selection

Nectar and pollen are consumed by guild members almost exclusively in the dry season, as large flowers suitable for bat use are in bloom only then (see Phenology). The few data available suggest that during the wet season fruit and insects become dietary staples (Table 19) That insects were not present in the food samples from G. soricina on Barro Colorado is probably because of poor sample size and the fact that this species moved out of the study area during the wet season. Nothing beyond the observations of Jeanne (1970) of P. stenops eating social wasp larvae and my two observations of. fruit eating is known about the diet of this bat.

Phyllostomus discolor is neither an extreme specialist nor generalist in terms of food species (niche breadth = 1.65). Several types of flowers are visited for pollen and nectar in the dry season. And in addition to insects, several types of fruits are eaten in the w~t season. The







68

Table 19. Seasonal use of pollen and fruit by the omnivore guild on Barro Colorado.




Food species No. of dry season No. of wet season
samples samples


P. discolor, N = 23 Pollen:

Ochroma lagopus 6

Pseudobombax septenatum 6

Unknown 202 Fruit'

Cecropia exima 2

Unknown 124 3

Insects: 3

G. soricina, N = 6

Pollen:

Ochroma lagopus 3

Unknown 201 I

Fruit:

Cecropia exima 1

Piper 109 I

P. stenops, N = 2

Fruit:

Unknown 110

Unknown 151 1







69

available data are too limited to consider niche breadth values for P. stenops and G. soricina, or to calculate niche overlaps between guild members.

Vertical stratification

All of the flowers and fruits eaten by P. discolor and 83% of those eaten by G. soricina in this study area grow in the subcanopy and canopy of the forest. Both species were captured most frequently in the upper levels of the forest, 3 of 4 for Glossophaga and 40 of 54 for Phyllostomus. For P. discolor preference for flying above groundstory shrubs is highly significant (P <.Ol, Chi Square Test). Habitat selection

Phyllostomus discolor was common in the mature forest and second growth but uncommon over creeks. Some of the important tree species producing flowers and fruits eaten by Phyllostomus are common only in second growth (e.g. Ochroma); others are common only in mature forest (e.g. Pseudobombax); and still others are common in both habitats (e.g., Cecropia).

Feeding behavior

During the dry season bats are frequently captured with pollen

heavily dusted over the anterior parts of the body. It is likely that these animals visit a number of flowers in succession, consuming nectar and performing pollination services at each flower, and then later perch to ingest pollen by grooming it from the fur and skin.

None of the bats in this guild were captured carrying fruit in the mouth,and it is not known whether they use night feeding roosts.

Sixty-nine percent of all P. discolor captured in all-night samples were taken within two hours of sunset. Such a strong unimodal pattern







70

of flight activity (Fig. 9) also is reported by LaVal (1970) and suggested by Heithaus et al. (1974) for this species in Costa Rica. My data are insufficient for discussing the flight activity cycle of Glossophaga; however, LaVal (1970) reports a strong peak in activity at dusk and in the first hour of darkness just before the peak in P. discolor activity. Sanguivore Guild

ky size

Of the three extant vampire species, only Desmodus rotundus, the common vampire, occurs on Barro Colorado Island and in the surrounding vicinity. The pre-meal mean body weight of D. rotundus is 33.5 g. Food selection

Wild vampires feed only on the blood of homoiothermic vertebrates (McNab, 1973). While vampire feeding behavior and prey selection is well documented in agricultural areas where domestic livestock are the chief food source (Turner, 1975), nothing is known of the prey species of vampires in remote areas where only wild animals are potential hosts. Vertical, stratification

Where domestic animals are the source of food, vampires fly almost exclusively within 3 m of ground level (Bonaccorso, unpublished data). It is possible that vampires more commonly fly in the canopy level in isolated forests where arboreal species (e.g., monkeys and birds) may be important sources of blood meals for these bats. On Barro Colorado Island two vampires were captured in subcanopy nets and one in a ground net.

Habitat selection

Vampires were clearly more abundant on Buena Vista Peninsula than on Barro Colorado Island. Desmodus was the fourth most abundant species in
























41


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73

the Buena Vista samples (7.9% of the total captures)whereas on Barro Colorado Desmodus was one of the least commonly captured species (0.2% of the total captures, and see Fig. 4). Horses, cattle, pigs, and fowl of the scattered farms in the Buena Vista-Frijoles area provide a dependable and abundant food source that "los vampiros" constantly parasitize (Fulo Sanchez, pers. comm.). Gleaning Carnivore Guild

Bod size

The largest feeding guild within the bat fauna of Barro Colorado,

the gleaning carnivore guild, is formed by nine species of phyllostomine bats. This guild also presents the largest range in body size within any of the BCI feeding guilds (Table 20). Micronycteris megalotis, one of the smallest bats on Barro Colorado, has a mean body weight of 6.3 g., while Vampyrum spectrum, the largest species on the island, weighs about 120 g.

The increment in body weight between successively larger species is more irregular within the gleaning carnivore guild than in any other guild on the island (see Fig. 3). Two species have mean body weights of close 'to 15 g., and three species have mean body weights of 31 to 36 g. On the other hand all three species of the genus Micronycteris differ from the next smaller species by a factor of 1.5. Food species selection

Little precise information can be offered at this time concerning the prey species eaten by members of this guild. Excepting Vampyrum spectrum, guild members feed predominately on insects most of the year. I have a large collection of fecal samples from these species but as yet have found no one able to identify the minutely fragmented insect exoskeletons that constitute these samples.






74)


Table 20. Weights in grams of gleaning carnivore bat species on
Barro Colorado.




Bat species Mean Standard Sample Wgt, / Wgt
() Deviation size Ig sm
(S. D.) (N)



M. megalotis 6.3 0.6 6 -M. brachyotis 9.7 1.1 3 1.53

M. crenulatum 14.7 0.7 Y12 1.52

M. hirsuta 15.2 1.2 7 1.03 1.57

T. cirrhosus 31.0 3.8 13 2.09

T. sylvicola 32.6 3.6 10 1.04

T. bidens 35.6 2.3 7 1.09

P. hastatus 91.2 4.0 7 2.56

V. spectrum 120.0 -- I 1.31






Weight of larger species divided by weight of smaller species in the pair compared.







75

On the basis of characteristics of echolocation, Novick (1971)

hypothesized that large-eared insect- and vertebrate-eating bats, such as are found in the gleaning carnivore guild, are adapted to distinguish and capture prey items resting on foliage. Ross (1967) and Wilson (1971b) have shown in food habit studies that three such large-eared species, Antrozous pallidus, Macrotus waterhousii and Micronycteris hirsuta, do feed primarily on large insects that spend much of their time perching on vegetation or on the ground. Gardner's (1975) review of the scattered information on food habits of the bats in this guild further confirms that food items such as lizards and large insects probably are gleaned from foliage.

Micronycteris. Wilson (1971b) reported that large roaches, Orthoptera, and scarabeid beetles are the most important items in the diet of M. hirsuta on Orchid Island, a small island adjacent to Barro Colorado. During the dry season, fruit became an important component of the diet of this species as indicated by droppings below the study roost. My food samples show that M. megalotis and M. brachyotis also switch in part to fruit diets in the dry season. M. brachyotis also eats nectar and pollen. An individual captured in mid-December was thoroughly dusted with the pollen of a balsa tree (Ochroma lagopus).

Tonatia. A very large male cicada (Fidicina mannifera) weighing 2.5 g was carried into a net in the mouth of a Tonatia bidens in July of 1974. The prothorax of the cicada had been crushed by the bat's teeth and the cicada was dead when removed from the net. Because this event occurred in the mating season of the cicadas, amongst the loud nocturnal chorusing of the males, it posed the question of how Tonatia locates such insect prey. Do bats locate such prey items via echolocation or sounds produced by the insects?








76

Two T. bidens, one male and one female, were released in a large outdoor flight cage, one at a time, on BCI. Both individuals were immediately attracted to the sounds of calling male cicadas that I held by forceps inside the cage. The cicadas were plucked from the forceps by the flying bats and eaten with gusto at a perch. Female cicadas held so that their wings could not move in the forceps were ignored by these bats; however, when the wings were allowed to flap nosily, the bats again were attracted to the cicadas and ate them. During later experiments large nocturnal grasshoppers, katydids, beetles, and moths (species not identified) placed on the ins ide cage screening were "gleaned'' from the screening and eaten by these bats. It is obvious that Tonatia bidens was able to locate cicadas from sounds produced by the cicadas, but whether other large foliage-clinging insects, many of which produce ultrasound, were echolocated or detected from insectproduced sounds remains an interesting question for future research.

Only insect fragments were found in the fecal samples of T. bidens and T. sylvicola from BC!.

Phyllostomus. Insects and fruits were found in the fecal samples of Phyl'ldstomus hastatus. It also has been reported by several authors to eat birds and rodents (Gardner, 1975).

Vampyrum. Vampyrum spectrum, the false vampire bat, is the largest New World bat. It appears to feed primarily on birds and small mammals, though investigators report some fruit and insects in its diet (Gardner, 1975). A hollow tree roost monitored by J. Bradbury (pers. comm.) in Costa Rica had a steady flow of feathers from parrots, trogons, cuckoos, anis, and many other birds appearing at its base. D. J. Howell and I kept a Vampyrum alive in captivity for three weeks on a diet of small bats






77

and birds ranging in size to large doves (Howell and Burch, 1974). When released in a large room with small fruit bats (10-20 g) the false vampire would fly up behind its flying victim and slap it into its jaws with a wingtip. One morning at sunrise on Barro Colorado, a false vampire circled about an Artibeus jamaicensis I was untangling from a net. The Vampyrum was apparently attracted by the alarm calls of the fruit bat and circled for over a minute before leaving.

Mimon. Fecal samples of Mimon crenulatum from BCI appear to contain only insect chitin.

Trachops. Fecal samples of Trachops cirrhosus from BCI appear to contain only insect chitin, but this species is reported to eat lizards such as anoles and geckos that are gleaned from vegetation, as well as some fruit (Gardner 1975; Howell and Burch, 1974). Vertical stratification

Mimon crenulatum and Tonatia sylvicola show a significant preference for flight in the groundstory level of the forestand the small samples for Micronycteris brachyotis and Tonatia bidens are just barely below significance levels for showing a preference for flight activity in the subcanopy-canopy level (Table 21:). Thus the two similarly sized species of Tonatia appear to forage in separate vertical strata.

Should future research increase sample sizes on vertical stratification it would not surprise me if none of the three species of the genus Micronycteris show a strong preference for one particular vertical stratum. All three species are very different in body size and probably specialize on mutually exclusive sizes of prey items.

Though the data are very limited, the two very large species in this guild, Phyllostomus hastatus and Vampyrum spectrum were captured or seen







78







Table 21. Vertical stratification of gleaning carnivore species on Barro Colorado.




Bat species No. of bats captured No. of bats captured
at ground level, at subcanopy levels,
I to 3 mm 3 to 12 mm



M. megalotis 1 3

M. brachyotis 6 12

M. hirsuta 6 3

M. crenulatum 9* I

T. cirrhosus 5 2

T. sylvicola 18** 3

T. bidens 2 8

P. hastatus 0 4

V. spectrum + 0 3




Significant by Chi Square Test (P < .05).

** Highly significant by Chi Square Test (P <.01). + Based on two net captures in Costa Rica and one visual sighting on on Barro Colorado

Yates Correction for Continuity is used on all Chi Square Tests (Sokall
and Rohlf, 1969).






79

flying only in the subcanopy-canopy levels of the forest. The groundstory (0 to 3 m) on Barro Colorado has the most dense foliage cover of any of the vertical strata of the BCI forest (E. Leigh, unpubl. data). P. hastatus and V. spectrum may be too large to maneuver well through the thick groundstory vegetation.

Habitat selection

Several gleaning carnivore species prefer either creek or forest habitats on Barro Colorado to the exclusion or near exclusion of the other habitat. Micronycteris brachyotis and Tonatia sylvicola are both common species in the forest station samples but were totally absent from creek samples (Fig. 6). Trachops cirrhosus represents 4% of all individual bats sampled at creek stations (8th most abundant species in creek samples) but only 0.5% of the individuals sampled at forest stations (17th most abundant species in forest stations). All other species in the guild are approximately equally abundant in creek and forest samples. Comparisons with Buena Vista second growth samples are not made because most species in this guild were under-represented at Buena Vista from lack of harp-trapping.

So far I show that most bat species within a given feeding guild partition food resources on the basis of food particle size. However, some ofthe gleaning carnivores seem to use additional mechanisms to partition food resources between similarly sized species.

The existing data make it appear that a spatial mechanism, specialization in foraging microhabitat, permits Trachops cirrhosus, Tonatia sylvicola, and Tonatia bidens, all similar sized gleaning carnivores, to partition food resources within the same macrohabitat. I suggest that T. cirrhosus specializes on prey items it can glean from low







80

foliage along creeks, that T. sylvicola specializes on prey items it can glean from groundstory foliage in the forest, and that T. bidens specializes on prey items it can glean from trees in the forest and along creeks or from the ground. Future research likely will show that all three species eat invertebrates and vertebrates weighing between 2 and 15 g, including lizards, frogs, and large insects. Feeding behavior

The gleaning carnivores eat rather large prey items relative to their body weight. It probably is common for them to carry prey to a feeding roost or day roost for consumption (Wilson, 1971b; Bradbury, pers. comm.).

Data on activity cycles are too scant for meaningful analysis.

M. brachyotis, M. crenulatum, T. sylvicola, and T. cirrhosus appear to have a major peak of activity in the first two hours after sunset. Slow-flying Hawking Insectivore Guild

Eight species belonging to three families constitute the guild of slow-flying hawking insectivores. Four species belong to the Emballonuridae, two to the Vespertilionidae, and two to the Mormoopidae. An additional species, Thyroptera tricolor of the Thyropteridae, is known in recent years only from a single 1973 sighting on BCI. T. tricolor perhaps should be included in this guild if a population still exists on BCI, but the species is probably near extirpation on the island because of plant succession that has resulted in the disappearance of most large-leafed groundstory plants (e.g. Musa and Callithea) used as roosts (Findley and Wilson, 1974).







81

Body size

Mean body weights of the species in this guild range from 4.2 to 22.6 g (Table 22). Wing morphology and flight behavior (Bonaccorso, unpubl. data) suggest that species within the same family are most similar in foraging behavior. Thus, species are grouped in subguilds by families. The two mormoopids differ in mean body weight by a factor of 1.37, a figure that suggests these two species may divide food resources solely on the basis of particle size. The two vespertilionids, on the other hand, are very similar in body size. Analysis of the relationships among body weights of the four emballonurids is complicated by small sample sizes and sexual dimorphism. The mean body weights of males of the four species differ by a factor of 1.25 to 1.47. Food selection

All species of this guild appear to feed on fairly small flying

insects. Prey items are eaten on the wing rather than carried to feeding roosts. Some emballonurids hover around tree foliage and probably feed to some extent on insects attracted to host trees. One BCI fecal sample from Pteronotus parnellii examined by Terry Erwin contained leg parts of a small beetle of the family Alicuidae. All other samples await analysis.

Vertical stratification

Pteronotus parnellii almost exclusively restricts its flight to

within 3 m of the ground (Table 23). Myotis nigricans and S. bilineata apparently fly with nearly equal frequency in groundstory and subcanopy levels of the forest. Peropteryx kappleri is probably a specialist on insects of the subcanopy, as indicated by the capture of all four BCI individuals in high nets and numerous visual observations made by the author in Belize (unpubl. data).








82


Table 22. Weights in grams of slow-flying hawking insectivore bat species on Barro Colorado.





Bat species Mean Standard Sample Wgt / Wgt*
() deviation size lIg sm
(s. D.) (N)


Emballonuridae

S. leptura ** 4.2 -- 1 -C. maximilliani ** 5.2 -- 2 1.25

S. bilineata males 7.7 0.56 11 1.47

S. bilineata females 8.7 0.7 3 -P. kappleri ** 11.2 -- 2 1.46

Vespertilionidae

R. tumida 4.2 -- 2 -M. nigricans 4.4 0.67 II 1.05

Mormoop i dae

P. suapurensis 16.5 -- 1 -P. parnelli 22.6 1.48 30 1.37




Weight of larger species divided by weight of smaller species in the pair compared.

** Males and females are probably dimorphic in body weight.







83


Table 23. Vertical stratification of slow-flying hawking insectivore species on Barro Colorado


No.of bats captured at No. of bats captured at Bat species ground level, 1 to 3 m subcanopy levels, 3 to 12 m




S. bilineata 7 4

C. maximilliani 2 0

P. kappleri 0 4

R. tumida 1 0

M. nigricans 3 3

P. parnellii 74** 1




** Highly significant by Chi Square Test (P <.01) with Yates.

Correction for Continuity (Sokall and Rohlf, 1969).






84

Habitat selection

P. parnellii is the second most abundant species in the forest station samples but is very rare in the creeks (Fig. 4). The only specimen of P. suapurensis was captured in the forest.

Myotis nigricans was captured only at forest stations, whereas Rhogeesa tumida was captured only at or near creeks. These two similar-sized species may differ in habitat requirements.

Visual observations of Saccopteryx bilineata were possible because

this species is crepuscular. Individuals repeatedly fly in circles around feeding territories in small clearings of the forest (e.g. treefalls) or over creeks (J. Bradbury, pers. comm.). I have frequently watched territory holders chase intruding conspecifics out of their territories emitting high pitched audible sounds as they fly.

Flih behavior

Pteronotus parnellii is one of the most commonly seen species on Barro Colorado, as it flies low along forest trails. Ultrasonic pulses picked up by a bat detector indicate that P. parnellii feeds as it flys back and forth in long loops along the forest trails and groundstory vegetation.

The flight activity of P. parnellii through the course of the night is bimodal with a major peak of activity occurring one to four hours after sunset and a minor peak occurring eight to ten hours after sunset (Fig. 10). Data on activity cycles of other species are limited, but P. parnellii appears to be the only species in the slow-flying hawking guild that has no strong peak of activity the first hour after sunset. Based on netting, visual observations, and ultrasonic detection, the emballonurids are active from an hour before sunset to an hour after sunset and again at a similar period about sunrise.

























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REPRODUCTION

Three patterns of reproduction occur in Neotropical bats: seasonal monestry, seasonal polyestry, and year-round polyestry (Fleming, 1973). Present information indicates that a single young is born per litter except in the genus Rhoeq9ssa in which the usual litter size is two (Humphrey and Bonaccorso, 1975).

Canopy Frugivore Guild

Canopy frugivores are seasonally polyestrous, with one birth peak at the end of the dry-to-wet transition and a second about the middle of the wet season (Figs. 11-13 and Table 25; Wilson, 1975). The first birth peak for all species coincides with the beginning of the first predictably steady rains of the year in late April and May, a time of fruit abundance. Large species such as A. jamaicensis and A. lituratus are pregnant (as detectable by palpation) by the first week of January. Small species like A. phaeotus are not in a similar stage of pregnancy until late January. Lactation then proceeds for one or two months during a period of food abundance. There is a postpartum estrousand females are well advanced in the second pregnancy of the year while lactation is still underway (Fleming, 1971).

The second birth and lactation peaks are less synchronized among species because of differences in gestation and lactation periods; the same is true to a lesser degree within species because of individual variation. For example, the second peak of lactation occurs in JulySeptember for A. jamaicensis and A. phaeotis, but not until September87















































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Full Text
Table 7. Most important food genera and species for bats in the canopy frugivore guild.
Bat Species
Percent of diet from most
important genera of food plant*
Most important species
of plant food*
N
V. pus i 11 a
92% Ficus
F. yoponensis
13
C. trinitatum
60% Ficus
F. popenoaei
5
A. phaeotis
30% Ficus
Spondias radlkoferi
33
V. he 11e ri
67% Ficus
F. inspida
6
C. villosum
100% Ficus
F. popenoaei
6
V. caraccioloi
76% Ficus
F. inspida
17
A. jamaicensis
78% Ficus
F. i ns idida
185
A. 1 ituratus
65% Ficus
F. inspida
20
* By frequency of occurrence


STUDY AREA
The primary research site was on Barro Colorado Island (BCl).
Barro Colorado lies within freshwater Lake Gatun, in the Panama Canal
Zone, at 9 10 North latitude and 79 51' West longitude. This field
site was selected because it has a rich bat fauna, relatively undis
turbed mature moist forest, modern living and laboratory facilities,
and reference collections of animals and plants. A secondary site was
located on the mainland opposite BCl at the base of Buena Vista Penin
sula.
The climate of this lowland area of Panama is warm and humid with
a seven-month wet season and a three-month dry season. Dry season
months, January through March, each receive less than 60 mm of rain.
Wet' season months, May through November, typically receive in excess
of 250 .mm of rain. April and December are months of transition between
dry and wet seasons and receive amounts of rain that vary considerably
from year to year. Thus in years when April and December are very dry,
the dry season may last for five months. Average annual rainfall since
1926 has been 2,820 mm (Smythe, 197^). Monthly sums of rainfall for
1973 are shown in Table 1.
During night time sampling of bats, relative humidity under the
forest canopy never fell below 80 percent. Measurements were made at
2 m above ground with a sling pyschrometer. Daily temperatures on the
forest floor fluctuate from a mean minimum of 22.1 C to a mean maximum
of 28.0 C with no significant seasonal variation (Smythe, 197^).
3


t
77
and birds ranging in size to large doves (Howell and Burch, 1974). When
released in a large room with small fruit bats (10-20 g) the false
vampire would fly up behind its flying victim and slap it into its jaws
with a wingtip. One morning at sunrise on Barro Colorado, a false vam
pire circled about an Artibeus jamaicensis I was untangling from a net.
The Vampyrum was apparently attracted by the alarm calls of the fruit
bat and circled for over a minute before leaving.
Mimon. Fecal samples of Mimon crenulatum from BCI appear to contain
only insect chitin.
Trachops. Fecal samples of Trachops cirrhosus from BCI appear to
contain only insect chitin, but this species is reported to eat lizards
such as anoles and geckos that are gleaned from vegetation, as well as
some fruit (Gardner 1975; Howell and Burch, 1974).
Vert ica1 stratification
Mimon crenulatum and Tonati a sy1vicol a show a significant preference
for flight in the groundstory level of the forest,and the small samples
for Micronycteris brachyotis and Tonati a bidens are just barely below
significance levels for showing a preference for flight activity in the
subcanopy-canopy level (Table 21). Thus the two similarly sized species
of Tonatia appear to forage in separate vertical strata.
Should future research increase sample sizes on vertical stratifi
cation it would not surprise me if none of the three species of the
genus M?cronycters show a strong preference for one particular vertical
stratum. All three species are very different in body size and probably
specialize on mutually exclusive sizes of prey items.
Though the data are very limited, the two very large species in this
gui Id, Phy1lostomus hastatus and Vampyrum spectrum were captured or seen


99
That females have a postpartum estrous is indicated by simultaneous
pregnancy and lactation in March-May and recaptures of marked individ
uals. Females are reproductively inactive from mid-October through
December.
Scaveng ? ng Frugivore Guild
Though only two female Centurio were captured during the study,
one female pregnant in February and another lactating in November indi
cate that the wrinkle-faced bat is probably seasonally polyestrous like
other fruit bats.
Pollen-Nectar-Fruit-insect Omnivore Guild
The only reproductive data available from Barro Colorado are for
Phyllostomus discolor, which appears to follow the pattern of seasonal
polyestry explained for frugivorous guilds (Table 26).
Sanguivore Guild
Though only six adult female vampires were captured during the
study the appearance of pregnant females in June, July, and August and a
lactating female in January suggest that Desmodus rotundus is either
seasonally polyestrous or, as suggested by Wimsatt and Trapido (1952),
polyestrous year round.
G1 eaning Carn1vore Guild
The fragmentary data available for this guild suggest a bimodal
pattern of seasonal polestry for the genera Micronycteris, Trachops, and
Tonatia. The first birth pulse in these genera coincides with the begin
ning of the wet season (Table 26 and Wilson, 1975). A pregnant and lac
tating female Tonatia sylvicola captured in March provides the first
evidence that this species has two litters per year and a postpartum
estrous.


Figure 13.
Reproductive timing
in female Art ibeus phaeotis.
' (
|
: i


for
Figure 9. Frequency of capture through the night as a measure of flight activity
Phy]lostomus discolor.


28
the trees of the canopy and subcanopy level of the forest, above 3 m from
the ground.
(2) !,Groundstory frugivores" -- forage mostly on fruits of shrubby
groundstory plants, 0 to 3 m above ground level.
(3) "Scavenging frugivores" feed mostly on over-ripe fruit.
(4) "Nectar-pol1en-fruit-insect omnivores" forage for pollen and
nectar from flowering trees when available in the dry season and then
switch to a fruit and insect diet in the wet season.
(5) "Sanguivores" -- feed only on the blood of mammals and birds.
(6) "Gleaning carnivores" -- forage for small animals (arthropods
or vertebrates) that are perching or moving on vegetation or on the
ground.
(7) "Slow-flying hawking insectivores" -- forage for flying insects
in small openings beneath or in the forest canopy or over streams.
(8) "Fast-flying hawking insectivores" -- forage for flying insects
above the forest canopy or in very large open spaces.
(9) "Piscivores" -- forage for fish or aquatic invertebrates at or
just above the surface of lakes and large streams.
The distribution of mean body weights for each bat species on
Barro Colorado by guild is plotted in Figure 3- Three guilds contain
a single species, and i expect that each of these species is sufficiently
unique to preclude serious interspecific competition for food. The
species within the groundstory frugivore, canopy frugivore, and piscivore
guilds increase in body weight with a geometric progression factor of
about 1 ..3 to 1.8 (with one exception in the canopy frugivore guild).
We might expect that the species within each of these guilds exploit
very similar types of food, captured in very similar manners, and that


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.
Brian K. McNab
^ Professor of Zoology
Thi5 dissertation was submitted to the Department of Zoology in the
College of Arts and Sciences and to the Graduate Council, and was accepted as
partial fulfillment of the requirements for the degree of Doctor of
Philosopny.
August, 1975
Dean, Graduate School


65
Food spec ies selection and feeding behavior
From several morphological features, particularly the small teeth
and narrow esophagus, Paradiso (1967) concluded that C_. senex probably
feeds on a "soft fruit or fluid diet". The small teeth, narrow esoph
agus, and lack of facial hair (like vultures) on this bat are suggestive
of its possibly feeding on over-ripe or decaying fruit. Hence I tenta
tively designate it a "scavenging frugivore". The amount of rotting
fruit on the forest floor is incredibly large on Barro Colorado and
potentially could provide an abundant food resource for such a bat.
Goodwin and Greenhall (1961) mentioned finding fruit pulp in stomachs
of £. 5enex from Trinidad. Of the individuals that I captured on Barro
Colorado one defecated an unidentifiable fruit pulp and the other carried
a fresh Spondias radlkoferi fruit in its mouth. At this time it can
neither be confirmed nor disproved that Cen tur io is a scavenging frugi
vore. Though it is very similar to Chiroderma villosum in body size
I have no doubt that this anatomically unusual bat is ecologically quite
different from any other frugivorous species on Barro Colorado with
respect to food habits.
Nectar-Pollen-Fruit-Insect Omnivore GuiId
Body size
The nectar-po11en-fruit-insect omnivore guild (hereafter referred
to as the omnivore guild) contains three species, all of the family
Phy1 lostomatidae -- Glossophaga soricina (Glossophaginae), Phy11ostomus
discolor (Phyllostominae), and Phy11oderma stenops (Phyllostominae).
The mean body weight for P_. d i sco lor on Barro Colorado is 4.36 times
larger than that of G_. sor i c i na (Table 1 8) j a larger difference than
is found between species adjacent in size in any other guild. The large


80
foliage along creeks, that T\ sylvicola specializes on prey items it can
glean from groundstory foliage in the forest, and that T_. bi dens special
izes on prey items it can glean from trees in the forest and along creeks
or from the ground. Future research likely will show that all three
species eat invertebrates and vertebrates weighing between 2 and 15 g,
including lizards, frogs, and large insects.
Feeding behavior
The gleaning carnivores eat rather large prey items relative to
their body weight. It probably is common for them to carry prey to a
feeding roost or day roost for consumption (Wilson, 1971b; Bradbury,
pers. comm.).
Data on activity cycles are too scant for meaningful analysis.
M_. brachyoti s, M_. crenu 1 atum, J_. sylvicola, and T. ci rrhosus appear to
have a major peak of activity in the first two hours after sunset.
Slow-flying Hawking Insectivore Guild
Eight species belonging to three families constitute the guild of
slow-flying hawking insectivores. Four species belong to the Embalonu-
ridae, two to the Vesperti 1 ionidae, and two to the Mormoopidae. An
additiona'l species, Thyroptera tricolor of the Thyropteridae, is known
in recent years only from a single 1973 sighting on BCI. T_. tricolor
perhaps should be included in this guild if a population still exists
on BCi, but the species is probably near extirpation on the island be
cause of plant succession that has resulted in the disappearance of
most large-leafed groundstory plants (e.g. Musa and Cal 1ithea) used as
roosts (Findley and Wilson, 197*0*


CONCLUSIONS
Though tropical forests are relatively stable terrestrial environ
ments, nearly all animal species must seasonally alter their foraging
and reproductive behavior in response to fluctuating environments whether
they be food generalists such as coatis (Kaufmann, 1962) and red-winged
blackbirds (Orians, 1973) or food specialists such as three-toed sloths
(Montgomery and Sunquist, 197^), anteaters (Lubin and Montgomery, unpubl.
data) and hummingbirds (Wolf, 1970; Snow and Snow, 1972). Several recent
papers have discussed how Central American bats respond to seasonal
changes by altering foraging and reproductive behavior (Mares and Wilson,
1971; Fleming et a 1., 1972; Heithaus e_t_ aj_.; 1975; Humphrey and
Bonaccorso, 1975). The present study shows that on Barro Colorado Island,
Panama, bat species diversity, as well as foraging and reproductive stra
tegies of individual bat species, all undergo marked seasonal variation
in the moist tropical forest.
Spec ies Diversity and Pheno1ogy
Maximal diversity in the bat community of Barro Colorado occurs from
March through July, the principal growing season. During this time rains
are frequent yet mild and many plants and insects, having passed through
reproductive inactivity in the dry season (except for flowering activity),
undergo rapid growth and reproduction. Deciduous trees flush new leaves
and mature fruits become abundant both in diversity and biomass. Most
of the large orders of insects including Coleptera, Lepidoptera, and
103


33
Food selection
All eight canopy frugivore species feed primarily on fruits of
large canopy and subcanopy trees, in particular figs of the genus Ficus.
Over 60% of the annual diet (by frequency of occurrence in fecal matter)
of seven of these bat species consists of fig fruits (Table 7); these in
clude C_. tr i n i tatum, but not A_. phaeot is of the same weight. A_. phaeot i s
depends on figs for 30% of its diet. Five species of Ficus, all of which
are green colored at maturity, are eaten and dispersed by these steno-
dermines on Barro Colorado. Fig species that produce large fruits are
preferred by large bats, and fig species that produce small fruits are
preferred by Small bats.
Figs form the bulk of the diet of Artibeus jamaicensis throughout
most of the year. However, during the latter part of the wet season
and the very beginning of the dry season mature fig fruits are very
scarce (Morrison, 1975). At this time A_. jama i cens i s turns more heavily
to other fruits and pollen (Table 8). The relative importance of pollen
in the diet of A_. j ama i cens i s is grossly underestimated here because my
sampling schedule did not coincide with the two weeks in late December
and early January when figs were very scarce and flowers were very
abundant. Similar seasonal switches in diet also probably occur for
A_. 1 ? turatus and V_. caraccioloi but the data are weak. No conclusions
can be made from the scant data on the smaller species of canopy frugi-
vores with respect to seasonal switches in diet.
Unlike the fig specialists, A_. phaeotis eats a more even distribu
tion of many types of fruits (Tables 7 and 8) with no one species
strongly dominating the diet. Throughout the year figs are a minor
component of the diet, while other fruits are very important in certain


119
Wilson, D. E. 19/1a. Ecology of Myotis nigricans (Mammalia: Chiroptera)
on Barro Colorado Island, Pamama Canal Zone. J. Zool. Lond., 163:1-13.
, 1971b. Food habits of Micronycteris hirsuta (Chiroptera: Phyllo-
stomatidae). Mamm., 35:107-110.
. 1975- Reproductive strategies, _i_n Biology of the New World
Leaf-Nosed Bats (Baker, R, J. and J. K, Jones, eds.). Texas Tech
Press, Lubbock, (in press).
Wimsatt, W, A, and H, Trapido. 1952, Reproduction and the female
reproductive cycle in the tropical American vampire bat, Desmodus
rotundus murinus. Amer. J, Anat., 91 :415-446,
Wolf, L, L. 1970. The impact of seasonal flowering on the biology of
some tropical hummingbirds. Condor, 72:1-14.
Zaret, T, M, and A, S. Rand, 1971. Competition in tropical stream fishes:
support for the competitive exclusion principle. Ecol., 52:336-342,


foraging strategies of each species. Tropical bat faunas can be
broken down into feeding guilds on the. basis of general food habits
and method of food procurement. Within the most complex guilds, such
as the canopy frugivore guild, food resources are partitioned in time
and space and by size and quality. Within the simplest guilds food
resources are partitioned primarily by food particle size. The most
important mechanism of resource partitioning separating similar species
is food particle size. Some species complexes appear to be limited not by
absolute amount of food but by the distribution of those resources in
a few concentrated patches accessible to only a limited number of
individuals at a given time. Reproduction coincides with high levels
of available food resources within each feeding guild.


Tab 1e 16.
Feeding niche breadths of groundstory frugivores.
Bat species
Number
known
of genera of
food plants
Number of species of
known food plants
% of diet composed
of pipers
Niche breadth
(loge B)
Ca rol 1 i a
castanea
8
18
78 (N
= 60)
2.47
Ca rol 1 i a
perspici1 lata
10
24
27 (N
= 103)
2.63
Based on frequency of occurrence of each species in the diet from samples in Tables 14 and 15


79
I
flying only in the subcanopy-canopy levels of the forest. The ground-
story (0 to 3 m) on Barro Colorado has the most dense foliage cover of
any of the vertical strata of the BCI forest (E. Leigh, unpubl data).
P_. hastatus and V_. spectrum may be too large to maneuver well through
the thick groundstory vegetation.
Habitat selection
Several gleaning carnivore species prefer either creek or forest
habitats on Barro Colorado to the exclusion or near exclusion of the
other habitat. Micronycteris brachyotis and Tonati a sy1vico1 a are both
common species in the forest station samples but were totally absent from
creek samples (Fig. 6). Trachops cirrhosus represents b% of all individ
ual bats sampled at creek stations (8th most abundant species in creek
samples) but only 0.5% of the individuals sampled at forest stations
(17th most abundant species in forest stations). All other species in
the guild are approximately equally abundant in creek and forest samples.
Comparisons with Buena Vista second growth samples are not made because
most species in this guild were under-represented at Buena Vista from lack
of harp-trapping.
So far I show that most bat species within a given feeding guild
partition food resources on the basis of food particle size. However,
some of the gleaning carnivores seem to use additional mechanisms to
partition food resources between similarly sized species.
The existing data make it appear that a spatial mechanism, special
ization in foraging microhabitat, permits Trachops cirrhosus, Tonatia
sylvicola, and Tonatia bidens, all similar sized gleaning carnivores,
to partition food resources within the same macrohabitat. i suggest
that T. cirrhosus specializes on prey items it can glean from low


56
Table 15. Food species in the diet of C_. perspici 1 1 ata as determined from
frequency of occurrence of seeds in fecal samples. Sampling periods begin
at mid-month.
Plant species
Jan-Mar
Ma r-l
May May-Jul
Ju1-Sep
Sep-Nov Nov-Jan Total
Shrubs
Piper aequa1e
1
1
P. cordulatum
10
1
1 1
P. reticulatum
7
7
P. marginatum
1
1
1
3
Piper 109
4
1
1 6
Piper 1 1
1
1
2
Piper 116
1
1
Piper 120
2
1 3
Piper 150
2
2
T rees
Carludovica palmata
1
1
Solanum hayseii
1
6
1
1 9
Markea panamensis
1
k
5
Vismia 1
k
5
9
Vismia 2
i
1
2
Cecropia exima
i
1
1 3
Brosimum bernadettae
3
3
Quararibea asterolepis
6 6
Dipteryx panamensis
7
1
8
Cassia undulata
3
3


40
Table 11. Vertical stratification of canopy frugivore species on
Barro Colorado. Statistical significance indicates pref
erence for one of the two vertical strata.
Bat Species
No. of bats captured at No. of bats captured at
ground level, 0 to 3 mm subcanopy levels, 3 to 12 mm
V. pus ilia
5
25**
C. trinitatum
2
4
A. phaeotis
36
56*
V. hel1eri
3
6
C. vi 1 los urn
4
24**
V. caraccioloi
4
30**
A. jamaicensis
467**
326
A. 1ituratus
23
66**
* Significant by Chi Square Test (P_ <.05).
** Highly significant by Chi Square Test (P < .01).
Yates Correction for Continuity is used on all tests of samples
with N< 200 (Sokall and Rohlf,1969).


76
Two T_. bidens, one male and one female, were released in a large
outdoor flight cage, one at a time, on BCI. Both individuals were
immediately attracted to the sounds of calling male cicadas that I held
by forceps inside the cage. The cicadas were plucked from the forceps
by the flying bats and eaten with gusto at a perch. Female cicadas
held so that their wings could not move in the forceps were ignored by
these bats; however, when the wings were allowed to flap nosily, the
bats again were attracted to the cicadas and ate them. During later
experiments large nocturnal grasshoppers, katydids, beetles, and moths
(species not identified) placed on the inside cage screening were
"gleaned" from the screening and eaten by these bats. It is obvious
that Tonatia bidens was able to locate cicadas from sounds produced by
the cicadas, but whether other large foliage-clinging insects, many of
which produce ultrasound, were echolocated or detected from insect-
produced sounds remains an interesting question for future research.
Only insect fragments were found in the fecal samples of T_. b i dens
and T_. sy 1 vi col a from BCI.
Phy11ostomus. Insects and fruits were found in the fecal samples
of Phyl lo'stomus hastatus. It also has been reported by several authors
to eat birds and rodents (Gardner, 1975).
Vampyrum. Vampyrum spectrum, the false vampire bat, is the largest
New World bat. It appears to feed primarily on birds and small mammals,
though investigators report some fruit and insects in its diet (Gardner,
1975)- A hollow tree roost monitored by J. Bradbury (pers. comm.) in
Costa Rica had a steady flow of feathers from parrots, trogons, cuckoos,
anis, and many other birds appearing at its base. D. J. Howell and I
kept a Vampyrum alive in captivity for three weeks on a diet of small bats


Figure 10. Frequency of capture through the night as a measure of flight activity
for Pteronotus parn!1 ii.


83
Table 23* Vertical stratification of slow-flying hawking insectivore species
on Barro Colorado
Bat species
No.of bats captured at No. of bats captured at
ground level, 1 to 3 ni subcanopy levels, 3 to 12 m
S. b11ineata
7 b
C. maximi11iani
2 0
P. kappleri
0 b
R. tmida
1 0
M. nigricans
3 3
P. parnel 1 i i
7 b** 1
** Highly significant by Chi Square Test (P_<.01) with Yates
Correction for Continuity (Sokall and Rohlf, 1369).


2
and ecological communities they form. About 100 species of bats occur
in each of the small countries of Central America (Hall and Kelson,
1959) it is common to find 30 to 50 species in one macrohabitat measur
ing a few square kilometers in area. For example Barro Colorado Island
(15 sq km), Panama, currently supports populations of at least 35 species.
Among tropical bat species, few are known or suspected to reproduce
year round or to specialize on constantly abundant food resources. The
common vampire bat, Desmodus rotundus, is one notable exception (Wimsatt
and Trapido, ¡952). instead, most bats, even in equatorial regions, are
seasonally polyestrous or monestrous in reproduction (Baker and Baker,
1936; Mutere, 1970; Fleming, 1973) and make seasonal shifts in food
habits (Wilson, 1 971b; Flemi ng e_t_ aj_. 1972; Hei thaus et al ., 1975).
The objective of this dissertation is to delineate adaptive strate
gies used by tropical bats that enable them to survive fluctuating
environmental conditions and coexist with numerous similar species in
complex communities. The field work represented herein documents
seasonal changes in diversity, mechanisms of resource partitioning, and
reproductive timing through one complete year and portions of two other
years..


109
guild contains fewer species than the canopy frugivore guild. In South
America the other genus in the subfamily Carollinae, Rhinophy11a, appears
to fit into the groundstory guild from information in Handley (1967) that
they are captured mostly in ground level nets. Some species of the
stenodermine genus Sturnira may also fit into the groundstory guild.
Far fewer shrub species than tree species produce bat-dispersed
fruits in tropical forests of Central America (12 versus 27 known species
on BCI; and see Heithaus et_ a_K 1975)- Also, shrubs produce a much
smaller range of fruit sizes than do trees. On Barro Colorado shrub
fruits preferred by bats range from about 0.2 to 2.0 g, a tenfold range;
whereas tree fruits preferred by bats range from about 2.0 to 30 g, a
fifteenfold range. Finally most shrub fruits are soft berries or catkins,
but tree fruits additionally may be drupes, monkeypods, and other forms.
Because of the greater variation in kinds, sizes, and shapes of canopy
fruits there are many more ways to specialize on canopy fruits than on
groundstory fruits, hence the larger numbers of species in the canopy
frugivore guild.
The foraging strategy of groundstory frugivores on Barro Co 1 orado.
Groundstory frugivores have small home ranges in comparison to large bats
that specialize on canopy fruits. This probably occurs because shrub food
species are abundant as individual plants and uniform in distribution
compared to tree species. It is probable that a large number of shrubs
must be visited each night by a groundstory frugivore in order for it to
find sufficient food. Each shrub has only a few small mature fruits
available per night (especially true of pipers) and a given shrub may be
stripped of fruits by other bats before an individual visits it or between


Figure 8. Frequency of capture through the night as a measure of flight activity
for two groundstory frugivore species.


Figure 2. Schematic representation of fluctuation in biomass of nocturnal flying
insects through the year (based on samples from three years, after Smythe, 197^).


61
£. castanea eats much of this fruit, as it is larger than all other
important fruits in the diet of C_. castanea.
Habitat select ion
Of the three habitats sampled, the Carollinae were most common in
the second growth forest and least common in the mature forest, as are
their most important food plants. C_. castanea accounted for 21.7% of
all bats captured in the second growth forest, 2.7% of the bats in the
creeks, and 1.4% of the bats in the mature forest (Fig. 6).
£. perspici1 lata constituted 15-8%, 16.0%, and 5.4% of the bat individ
uals captured in those habitats. Whereas many species of pipers grew
abundantly in the sunlight of the open canopy second growth and along
the creeks (though less so along creeks), only one species, P_.
cordu1atum, was abundant in the shade of the mature forest.
Vertical stratification
C_. castanea and C_. perspi ci 11 ata were both captured more frequently
at ground level than at upper levels of the forest (C_. castanea = 20
ground level, 14 upper levels; C_. perspici 1 1 ata = 50 ground level,
34 upper levels), but the difference was not statistically significant.
Both species feed on plants of ground and canopy levels. Known ground-
story fruits make up 78.4% of the diet of C_. castanea and 38% of the
diet of £. perspi ci 1 lata. During seasons when C_. persp ic i 1 1 ata is
feeding mostly on canopy fruits, it also is captured more frequently
in high nets and traps.
Feed ing behavior
Carol 1 ia castanea and C_. perspici 1 lata both have been captured
carrying fruits in the mouth and presumably use night feeding roosts as
do canopy frugivores. Some fruits are carried back to the day roost


11
(2) Equitabi 1 ity, E = H/Hmax, where Hmax is the natural logarithm of
the number of observed species (Sheldon, 1969).
(3) Niche breadth, loge B = ~Zp¡ loge p¡, in which the functions are
the same as described in Equation 1. Values approaching zero indicate
narrow niche breadths and specialists. Values approaching one indicate
wide niche breadths and generalists (Levins, 1968).
a 2 2
(4) Niche overlap, CA= 2£ X¡ Yj/£ X¡ + Y¡ where X¡ is the propor
tion of the ith food species in the diet of bat species X, and Y¡ is the
proportion of the ith food species in the diet of bat species Y (florista,
1959). follow Zaret and Rand (1971) in considering species with over
lap values greater than 0.6 to be critically similar in terms of food
overlap.


5b
_C. perspici 1 lata and C_. subrufa by field cha racters, and it is poss i ble
that I lumped a few individuals of C_. subrufa with £. persp i c i 1 lata
because I was not aware that C_. subrufa was present on BCI. I believe
C_. subrufa is very rare on Barro Colorado, and lumping a few of them
with (^. perspici 1 lata would influence the data on this latter species
to a very minor extent.
Food selection
C. castanea and JC. persp i c i 1 1 ata are food generalists in that they
eat a fairly even distribution of a large number of kinds of fruits and
have large niche breadth values (Tables 14, 15, and 16). Though no one
food species dominates their diet in any one season or over a long
portion of the year, eleven species of the shrubby plant genus Piper
(Piperaceae) constitute the bulk of the diet of C_. castanea and nearly
*
one-third of the diet of C_. persp i c i 1 1 ata. Ten species of pipers were
identified in the fecal samples from C_. castanea and nine species from
C. perspici 11 ata. At least one species of piper is available with
mature fruit in every month of the year on Barro Colorado (see Table 2).
C. castanea eats pipers all year long, but no pipers were evident in the
diet of perspici 11 ata from mid-September through mid-November.
C_. persp i c i 1 1 ata appears to feed exclusively on subcanopy and canopy
fruits in the late wet season. Particularly important are Solanum
hayseii, Quararibea asterolepis and Cecropia exima. Other fruiting
trees are important food species along with pipers at other seasons.
Though fruiting shrubs dominate the diet of _C. castanea, fruiting trees
are somewhat more important than shrubs for C_. perspici i lata.
in addition to the fecal samples from captured animals, food habits
data for C_. persp i c i 1 1 ata were obtained by monitoring droppings below


Figure 5. Linear regression of fruit weight on bat body weight for fruits carried
into nets by _\/. ca race i o 1 o i A. |ama icensis, and /\. 1 i tu ra tus.


TABLE OF CONTENTS
Page
AKNOWLEDGEMENTS iii
ABSTRACT v
INTRODUCTION 1
STUDY AREA 3
MATERIALS AND METHODS 6
Mathematical Formulae 10
PHENOLOGY AND FOOD RESOURCES 12
SPECIES DIVERSITY. . 20
RESOURCE PARTITIONING 27
Canopy Frugivore Guild 31
Groundstory Frugivore Guild 50
Scavenging Frugivore Guild 62
Nectar-Pol 1 en-Fru i t-1 nsect Omnivore Guild 65
Sanguivore Guild 70
Gleaning Carnivore Guild 73
Slow-Flying Hawking Insectivore Guild.... 80
REPRODUCTION 87
Canopy Frugivore Guild 87
Groundstory Frugivore Guild 94
.Scavenging Frugivore Guild 97
Nectar-Pol len-Fru i t~ I nsect Omnivore Guild 97
Sanguivore Guild 97
Gleaning Carnivore Guild..,.. 97
Slow-Flying Hawking Insectivore Guild 98
CONCLUSIONS 101
Species Diversity And Phenology.. v 101
Foraging And Reproductive Strategies 104
LITERATURE CITED 115
APPENDIX 120
BIOGRAPHICAL SKETCH 122


73
the Buena Vista samples (7-9% of the total captures), whereas on Barro
Colorado Desmodus was one of the least commonly captured species (0.2%
of the total captures, and see Fig. 4). Horses, cattle, pigs, and fowl
of the scattered farms in the Buena Vista-Frijoles area provide a
dependable and abundant food source that "los vampiros" constantly para
sitize (Fulo Sanchez, pers. comm.).
Gleaning Camivore Guild
Body size
The largest feeding guild within the bat fauna of Barro Colorado,
the gleaning carnivore guild, is formed by nine species of phyllostomine
bats. This guild also presents the largest range in body size within
any of the BCI feeding guilds (Table 20)* Micronycteris megalotis, one
of the smallest bats on Barro Colorado, has a mean body weight of 6.3 g.,
while Vampyrum spectrum, the largest species on the island, weighs
about 120 g.
The increment in body weight between successively larger species is
more irregular within the gleaning carnivore guild than in any other
guild on the island (see Fig. 3)- Two species have mean body weights
of close 'to 15 g., and three species have mean body weights of 31 to
36 g. On the other hand all three species of the genus Micronycteris
differ from the next smaller species by a factor of 1.5-
Food species selection
Little precise information can be offered at this time concerning
the prey species eaten by members of this guild. Excepting Vampyrum
spectrum, guild members feed predominately on insects most of the year,
i have a large collection of fecal samples from these species but as
yet have found no one able to identify the minutely fragmented insect
exoskeletons that constitute these samples.


30-
fi:l] Nulliparous
_] ?? that have given birth
60-
40-
20-
0 -
few data
N = 40
to
UJ
<
5
UJ
UL.
rj
D
<
u.
o
I
z
UJ
U
c
UJ
Ol.
90 -
Pregnant
80 -
Ej Lactating
| '' Nonreproducing
70 -
60-
50-
40-
30 -
20 -
m
-.I
fe'-i
i; ;i|

O
10-
_ m

^
0-
Scl


J-M M-M
N = 12 42
uaroina perspicif iafa
few data
|-i;f few data
-
M-J
7
S-N
11
few data
CO
CO


16
Ficus inspida and F_. yoponens i s, were very scarce, but Spond ias
radlkoferi and S. mombin were quite abundant.
Most of the plant species producing fruits eaten by bats produce
ripe fruits for periods of only one to four months. Only three species,
F_. i ns i p i da, F. obtus i fol ia and _F. yoponens i s have ripe fruits avail
able nine or more months per year. individuals in the populations of
these fig species fruit asynchronously once or twice per year.
F_. inspida and f_. yoponens i s populations show three major fruiting peaks
and troughs each year (Morrison, 1975)
The plant genera Cecropi a, Spondias, Vismia, and Piper each have
two or more bat-dispersed species that set fruit in sequential time
periods (Table 2). There are 10 species of pipers on BCI eaten by bats.
Though no one of these species is available for more than a few months,
two or more species have ripe fruit throughout the year. Heithaus et ai.
(1375) report that pipers are important bat fruits in Costa Rica and
that several species are available in similar sequential series. Snow
(1965) reports that 18 species of the bird-dispersed genus Mi conia are
sequentially available throughout the year in Trinidad.
The biomass and numbers of nocturnal insects caught in light traps
in Barro Colorado forest over a three-year period were reported by Smythe
(197^). Though these samples represent all nocturnal flying insects,
not just those eaten by bats, they provide a useful index of the abun
dance and fluctuation of the potential food resources for insectivorous
bats through the year (Fig. 3). The light trap collections show that
nocturnal insect biomass in the early wet season is as much as eight
times that of the biomass at the end of the wet season and during the
dry season (Fig. 2). Large insects (> 5 mm in length) were responsible


FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUNITY
OF BATS IN PANAMA
By
FRANK JOSEPH 30NACC0RS0
A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF
THE UNIVERSITY OF FLORIDA IN PARTIAL
FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
1975


100
Mimon crenulatum has a monestrous reproductive cycle (Table 26).
The peak in pregnancies occurs in the dry-to-wet season transition with
lactations peaking in the early wet season. Mimon are reproductively
inactive from September through December.
Slowf ly i ng Hawk? ng I nsect i vore Guild
Female Pteronotus parnellii are monestrous (Fig. 15). Pregnancies
occur from late December through mid-April. Lactation proceeds from
mid-March through late October; however, most young bats are weaned by
mid-July. The percentage of females suckling young in the May-July
sampling indicates that at least 53% of the adult females succeed in
raising young to the latter stages of nursing. This latter figure is in
reality much larger because some females have already weaned young by
the end of this sampling period. Unfortunately juvenile P_. parnel 1 i i
cannot be distinguished from adults on the basis of pelage color as is
possible for many other species.
During the March-May sampling 16% of the captured females were
null¡parous adults,and these were probably all one-year-olds. However,
in the next sampling period 50% of the females captured were nulliparous,
indicating that young of the year were entering the flying population
(top graph in Fig. 15). In the July-September sample, 65% of the females
were nulliparous. The number of nulliparous females then declined to
47% by the next sampling period; associated with the fact that only 16%
of the females were nulliparous in March, this pattern suggests a high
mortality for females in the latter half of their first year. Such a
pattern has been found in temperate Myotis (Humphrey, 1975b).


Arfibeus lifuratus
OD


Table 4.
Seasonal variation in species diversity, species number, and equitability of frugivorous
and insectivorour bat species on Barro Colorado Island. Sampling periods begin at about
the middle of each calendar month and are based on lunar cycles.
Seasons :
Dry
Dry-Wet
T ransition
Early-
Wet
Mid-
Wet
Late-
Wet
Wet-Dry
Transition
Months:
Jan-Ma r
Mar-May
May-Ju1
Jul-Sep
Sep-Nov
Nov-Jan
F rug ? vores
Species Diversity
(h ')
1.717
1.705
1.695
1.330
1 .094
1 .662
Equitabi1ity
(E)
0.650
0.646
0.661
0.577
0.456
0.693
Species Number
(SN)
12
12
12
10
1 1
10
Total Bats Sampled
249
263
21 4
205
261
162
I nse
ctivores
Species Diversity
(H1)
1.909
1 -587
1.526
1 .278
1 .003
1 .698
Equitabi1ity
(E)
0.796
0.618
0.614
0.555
0.482
0.737
Species Number
(N)
12
Is
13
10
8
10
Total Bats Sampled
55
107
76
43
46
22


116
Gardner, A, L. 1975. Feeding habits of New World leaf-nosed bats, _i_n
Biology of the New World Leaf-Nosed Bats (Baker, R. J. and J. K.
Jones, eds.). Texas Tech Press, Lubbock (in press).
Goodwin, G. G. and A. M, Greenhall. 1961. A review of the bats of
Trinidad and Tobago. Bull, Amer. Mus. Nat. Hist., 122:191-301,
Gould, E, 1955. The feeding efficiency of insectivorous bats. J.
Mamm,, 36:399-407.
Hall, E, R. and W. B Jackson. 1953. Seventeen species of bats recorded
from Barro Colorado island, Panama Canal Zone, Univ, of Kans. Publ.
Mus. Nat. Hist:,, 5:641-646.
Hall, E, R. and K. R, Kelson. 1959. The Mammals of North America. Ronald
Press Co,, New York, 756 pp.
Handley, C. 0,, Jr, 1966. Checklist of the mammals of Panama, j_n Ecto
parasites of Panama (Wenzel, R. L. and V, J, Tipton, eds,). Field
Mus. Nat. Hist., Chicago.
__ _. 1967. Bats of the canopy of an Amazonian forest. Atlas Simp,
Biota Amaznica, 5:211-215.
Harrison, J, L, 1962. The distribution of feeding habits among animals
in a tropical rain forest, J, Animal Ecol,, 31:53-63.
Heithaus, E. R., P. A. Opler, and H, G. Baker. 1974. Bat activity and
pollination of Bauh i nia pau1etia: plant-pollinator coevolution,
Ecol., 55:412-419.
Holdridge, L. R, 1967. Life Zone Ecology. Tropical Science Center,
San Jose, Costa Rica, 206 pp.
Hooper, E. T, and J, H, Brown. 1968, Foraging and breeding in two
sympatric species of Neotropical bats, genus Nocti 1 io. J. Mamm.,
49:310-312.
Howell, D. J. and D Burch, 1974. Food habits of some Costa Rican bats-
Rev. Biol. Trop., 21:281-294.
Humphrey, S. R. 1975a. Nusery roosts and community diversity of
Nearctic bats. J. Mamm., 56: (in press),
. 1975b. Population ecology of the little brown bat (Myotis
1ucifugus) in indiana and north-centra! Kentucky. Amer. Soc.
Mamm, Spec. Pub], (in press).
and F. J. Bonaccorso. Population and community ecology of phyllo-
stomatid bats, _i_n Biology of the New World Leaf-Nosed Bats (Baker,
R. J. and J, K. Jones, eds.). Texas Tech Press, Lubbock (in press).


55
Table \b. Food species in the diet of £. castanea as determined from
frequency of occurrence of seeds in fecal samples. Sampling periods
begin at mid-month.
Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total
Piper aequale 3
JP. cordul atum
_P. ret i cul atum 1
P_. ma rg i natum 3
P_. carri 1 loanum
Piper 109 1
Piper 11b
Piper 120
Piper 122
Pi pe r 150
Carludovica pa 1 mata
Solanum hayse i ?
Markea panamensis
Vismia 1
Brosimum bernadettae
Dipteryx panemensis 1
Aechmeia ti11andsoi des 1
Unknown 10A
Shrubs
3
8 1
3
1 1
1 1
1
1
3
2
T rees
1
2
9 1
2 1
3 6 15
9
1 5
1 6
2
2 b
1 1
1 2
3
2
1
2
1 1 1
3
Unknown
1
1
1
1
Unknown 123
1
1


Appendix 1 continued.
Bat species
Dry
Dry-Wet
T ransition
Early-
Wet
M i d-
Wet
Late-
Wet
Wet-Dry
T ransition
Total
M. brachyotis *
4
8
5
1
2
3
23
M. crenulatum *
5
7
4
6
1
2
25
M. hirsuta
3
2
1
1
7
T. cirrhosus *
10
1
4
2
1
18
T. sylvicola
3
6
4
1
3
1
18
T. bidens *
2
2
3
1
1
9
P. hastatus *
1
3
2
6
R. tmida
1
1
2
M. nigricans
2
4
1
1
4
2
14
S. ieptura
1
1
C. maximi11iani
2
1
1
4
S. bi 1ineata *
2
5
2
1
10
P. kappleri
1
2
2
5
P. suapurensis
1
1
P. parn 1 1 i i
22
64
47
32
33
9
207
* Denotes species
that were
common n
the dry
season, but
rare or
absent in the
m i d-wet
and/or late-wet season (see page 20).


SPECIES DIVERSITY
Considerable variation occurred in the bimonthly measures of species
diversity (Table 3). All three diversity indices, H1, E, and SM, were at
maxima during the dry-to-wet transition sampling period. The three diver
sity measures then declined in each of the next three bimonthly periods
to a minimum in the late-wet season. Whereas 27 bat species were present
in the study area in the d ry-to-wet transition, only 13 species were
sampled in the late-wet season. During this same interval H1 dropped
from 2.33 to 1.52 and equitability from 0.707 to 0.515. In the wet to
dry transition period the diversity values began to increase. Dry season
values were very similar to wet-dry transition values^but SN increased
from 22 to 25 in this period.
The diversity values were lowest in the mid- and late-wet season
samples because 13 of the species common in the dry season became notice
ably rare or absent (indicated by asterisks in Appendix 1) from the study
area in'one or both bimonthly periods. These include seven insectivorous
species (k~]% of the total insectivorous species), five frugivorous
species {kl%), and one nectarivorous species (50%). These species appear
to move to other habitats precisely at the time when bat-dispersed fruits
and nocturnally flying insects, the two most important food resources for
bats in this community, become relatively scarce on the study site (Fig.
2 and Table 2).
Of the seven insectivorous bat species that move out of the
mature forest late in the wet season, six are foliage gleaners and one
20


60
50
40
30
20
10
0
30-i
40'
30-
20-
10
0
20 i
10-
0
5 1
15
13
SECOND GROWTH
9 321 18t32,12 10 22 36
CREEKS
10
3 20 13 19 4 7 23 16 32 6 11' 18 22*29 25 12
MATURE FOREST
32 2 10 5 13 8 7 17 1 3 19 21 26 29 1 20 18 4 22 30 23 28 15 12 11 14


INTRODUCTION
Mention of the words "tropical forest" among ecologists typically
triggers visions of species rich communities, complex competitive inter
actions, and relatively stable environmental conditions. Indeed, faunal
lists in the tropics are large^and food webs are intricately complex.
It is also true that organisms inhabiting tropical latitudes usually are
subjected to less extreme environmental fluctuations than are their
counterparts in temperate or polar regions. However, it is too infre
quently emphasized that even species in tropical forests must possess
behavioral flexibility to counter and survive climatic and biotic
environmenta1 change. There are two major reasons for this general lack
of insight. Firstly, few detailed studies of tropical organisms have
spanned periods of several years or even seasons. And secondly, the
behavioral responses of tropical species to environmental fluctuations
are often quite subtle. Whereas temperate animals commonly exhibit
obvious >and dramatic reactions to seasonal change such as hibernation
or long distance migration, tropical species may only need to switch
food types or microhabitats, or briefly halt reproduction. Nevertheless,
genetic and behavioral flexibility are requisites for survival for most
tropical as well as temperate species.
Tropical bats are particularly worthwhile subjects for studies of
diversity, competitive interaction, and response to environmental fluc
tuation because of their individual abundance and the complex taxonomic
1


Table 2 continued
Plant species
Plant type
Piper aequa1e S
P_. carri loanum S
P_. cordulatum S
_P_. marg inatum S
P_. ret i cul atum S
Piper 109 S
P i pe r 11 4 S
Piper 116 S
Piper 120 S
Piper 122 S
Unknown 104 U
Unknown 110 (Cucurbitaceae) U
Unknown 127 U
Unknown 131 U
Unknown 117 U
Unknown 124 U
Unknown 130 U
Total number of food plant species
a va i 1ab1e
Mar Apr May Jun Jul Aug Sep Oct Nov Dec
17 19 17 12 15 10 11 7 86


PERCENT OF ADULT FEMALES
80
60
40
20
0
j:;;j Nultiparous 99
?? that have given birth
few data j




few data
M-i
32
J-S
21
S-N
19
N-J
5


Table 1. Rainfall (mm) on Barro Colorado Island, 1973 (after Smythe, 197*0
Jan Feb Mar Apr
May Jun J u1 Aug Sep Oct Nov Dec
Rainfall by calendar 58 18 26 19 274 323 231 358 3^1 261 578 45
month
Rainfall corresponding 45 23 11 7 110 370 250 334 278 353 375 346 58
to mid-month bat sampling
pe riod s


44
Table 12. Wet weights in grams of some fruits eaten by bats on
Barro Colorado Island that were collected beneath
fruiting trees.
Plant Species
Range
Fruit Weights
Mean S. D.
N
Ficus inspida
7.1-11 .A
9.1
1.5
10
Ficus obtusifolia
14.2-19.0
17.0
2.5
3
Ficus yoponensis
1.5- 5.6
3.1
1.1
12
Anacardium excel sum
4.2- 6.2
5.1
0.7
7
*
Calophyllum longifolium
9.3-17.7
14.7
3-3
7
Dipteryx panamensis
18.0-26.3
22.3
3-6
5
Spondias radlkoferi
8.6-13-0
10.6
1.4
9
Quararibea asterolepis
4.9- 6.3
5-45
0.6
4
Astrocaryum standleyanum
17.0-20.5
18.8
1.8
4
Piper cordulatum
0.5- 2.0
1 .2
0.5
15


10
Age classes were distinguished as follows. Infants were unable to
fly and were encountered only when carried by the mother. Juveniles were
able to fly but still had the infant pelage. Subadults had the adult
pelage but were smaller in weight than adults and were reproduct ively
immature. Adults possessed both adult pelage and weight.
Pregnancy, lactation, and reproductive inactivity of adult females
were determined by palpation. Additionally, females could be distin
guished as null¡parous or post-1actat¡ng by examining the condition of
the teats.
Fecal pellets obtained from individual animals were placed in
separate glassine envelopes for laboratory identification of food
species. Fruits and pollens in fecal pellets were identified to species
by comparing unknowns with seeds, pulp fibers and pollen grains in a
reference collection assembled by the author. Pellets were collected
from insectivores but remain unidentified because the hard parts of
arthropods eaten by bats are masticated into tiny fragments that are
difficult to identify. Pollen on the fur was collected by swabbing
with a gelatin described by Beattie (1971). The pollen-containing
gelatin'was then melted on slides for microscopic identification.
Frequently, animals were captured with whole fruits held in the mouth.
Additional information on food habits was gathered by placing plastic
sheets under two roost trees of Carol iia perspeciilata to gather
discarded fruits and fecal matter.
Hathematicai Formu1ae
(1) Species Diversity, H1 = £p¡ loge pj, where p¡ is the number of the
i th species divided by sample size (Shannon and Weaver, 1949),


57
Table 15, continued.
Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total
Unknown 101 1 1
Unknown 103 1 1
Unknown 104 1 1
Unknown 125 44
Unknown 127 22
Insects
5
1
6


Orchid
island
Buena Vista
Point
To mainland station
Frijoies
Bay
Pena Blanca
Bay
Colorado
A Point
Gigante
Bay
79 52'
7 95r
7950'


Figure 4. Relative abundance of bat species in three habitats. Numbers along
horizontal axes refer to species as assigned in Fig. 3.


Figure 3. Mean body weights of bat species by feeding guilds.
(Dashed lines seperate members of different families that belong to the
same feeding guilds.) 1, Carol 1ia castanea, 2. C. perspeci 1 lata,
3. Vampyressa pus i 11 a 4, Chirodenna trinitatum, 5. Artibeus phaeotis,
6, Vampyrops he 11eri, 7. Chirodenna vi11 osurn, 8. Vampyrodes caraccioloi,
9. Artibeus j ama icensis, 10. A, l i turatus, 11. Centurio semiex, 12. Glosso-
phaga sor¡cia, 13. Phyl1ostomus discolor, 14, Phylioderma stenops,
15. Desmodus rotundus, 16. Micronycter i s mega 1otis, 17. M. brachyotis,
18, Mimon crenulatum, 19. Micronycteris hirsuta, 20. Trachops cirrhosus,
21. Tonatia sy 1 v i col a 22. T. b i dens 23. Phyl 1 ostomus hastatus 24. Varnpy-
rum spectrum, 25. Rhogeessa tumi da, 26. Myotis nigricans, 27. Saccopteryx
leptura, 28. Centronycteris maximi11?ani, 29. Saccopteryx b i i i neata,
30. Peropteryx kappleri, 31. Pteronotus suapurensis, 32. _P. parn 1 1 i i ,
33. Mol ossus mo lossus, 34. Nocti 1io labial is, 35. _N. 1eporinus


117
Hutchinson, E. G, 1959. Homage to Santa Rosalia, or why are there so
many kinds of animals? Amer. Naturalist, 93:145~161.
Janzen, D. H. 1973. Sweep samples of tropical foliage insects: effects
of seasons, vegetation types, elevation, time of day, and insularity,
Ecol,, 54:687-708.
and T. W. Schoener. 1969. Differences in insect abundance and
diversity between wetter and drier sites during a tropical dry
season. Eco., 49:96-110.
Jeanne, R. L. 1970. Note on a bat (Phylloderma stenops) preying upon the
brood of a social wasp. J, Hamm., 51:624-625.
Kaufmann, J. H, 1962, Ecology and social behavior of the coati (Nasua
na rica) on Barro Colorado Island, Panama. Univ, Calif. Publ. Zool.,
60:95-222.
LaVal, R. K. 1970. Banding returns and activity periods of some Costa
Rican bats. Southwestern Naturalist,, 15:1-10.
Levins, R. 1968. Evolution in Changing Environments. Princeton Univ.
Press, Princeton, 120 pp.
Mares, M, A. and D. E, Wilson, 1971. Bat reproduction during the Costa
Rican dry season. BioScience, 21:471-4-77.
May, R, M. 1973. Stability and Complexity in Model Ecosystems (Ch. 6).
Princeton Univ. Press, Princeton, 355 pp.
McNab, B, K. 1969. The economics of temperature regulation in Neotropical
bats. Comp. Biochem, Physiol,, 31:227-268.
. 1971a. The structure of tropical bat faunas, Ecol., 52:352-358.
. 1971b. On the ecological significance of Bergmann's rule. Ecol,,
52:845-854,
. 1973. Energetics and distribution of vampires, J. Mamm,, 54:131-144.
Miguela, P, 1969. Bioenergetics of pregnancy and lactation in European
common vole. Acta Theriologica, 14:167-179.
Montgomery, G. G, and M. E. Sunquist. 1973. Impact of sloths on
Neotropical forest energy flow and nutrient cycling, _i_n Trends in
Tropical Ecology (Medina, E, and F, Gol ley, eds,), Ecological
Studies 4, Springer-Ver1ag, New York,
Morista, M. 1959. Measuring of interspecific association and similarity
between communities. Mem. Fac. Sci. Kyushu Univ. Ser. E. (Biology),
3:65-80.
Morrison, D. 1975. Foraging and mating strategies of the Jamaican fruit
bat, Artibeus jamaicensis. Ph.D. Diss., Cornell Univ., Ithaca, N, Y.




50
crowding at resource trees presumably is of importance in permitting more
efficient feeding and in making these bats less obvious to the many kinds
of arboreal and aerial predators that eat bats (Humphrey and Bonaccorso,
1975).
A similar pattern of offsetting major activity peaks should be
expected in the small canopy frugivores, all of which feed heavily on
Ficus yoponensis and F_. popenoae i Figure 7 shows that V_. pus i 1 1 a is
most active in the first two hours after sunset, and C_. vi 1 losum is most
active later in the night. Paucity of data prevents comparison of the
other small fig specialists.
A. phaeotis, the feeding generalist, has a much more even distri
bution of activity through the night than any other species (Fig. 7).
Many of the fruits eaten by A_. phaeot i s are not eaten by other stenoder-
mine bats and it need not compromise its activity cycle to avoid crowded
resource trees.
Groundstory Frugivore Guild
Body size
Two species in the subfamily Carollinae of the Phy1lostomatidae
constitute the groundstory frugivore guild on Barro Colorado. They are
Carol 1 i a castanea and C_. persp i c i 1 1 ata These have mean body weights
of 12.A and 17-9 g, thus differing in body weight by a factor of l.^tA
(Table 13).
A few individuals of a third species of the genus Ca rol 1ia,
C. subrufa, were captured and banded by R. K. LaVal in 1972 on Barro
Colorado (pers. comm.). In 1973 and 197^ I recaptured some of LaVal's
banded C_. persp i c i 1 1 ata and _C_. castanea, but I have not encountered any
of the C_. subrufa he marked. It is difficult to distinguish


[:::[ Nylliparous 99
99 that h ave given birth
80-
60-
40-
20-
0-
few data
on
UJ
<
UJ
ro
a
<
u_
O
H-
Z
UJ
U
Q£
UJ
Q.
90
80-
70-
60-
50
40
30-
20-
10-
Pregnanf
Lactating
l-rssj .
Nonreproducing
-t .'
J-M
N-58
M-M
92
M-J
53


Table 2k continued.
Bat species
Jan-Mar Mar-May May-Jul
T. sylvicola
T. bidens
P_. hastatus
C. maxmi 1 1 iani
S. bi 1ineata
P_. kappleri
R_. tumi da
M.* n igr i cans
P_. suapurensis
G. soricina
110 10 0 2 0 0
1 0 0
0 0 1 0 0 1
1 1 0
10 1 2 0 0
0 0 1
1 0 1
0 0 1 0 0 1
0 1 0
Jul-Sep
Sep-Nov
Nov-Jan
0 0 2
1 0 0
CD
cn


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,
A
John H, Kaufmann, Chairman
Professor of Zoology
ru''
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,
Stephen R. Humphrey, Co-Chairman
Assistant Curator in Mammalogy
and Assistant Professor of Zoolog
I certify that 1 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.
VWtZ
Thomas C, Emmel
Associate Professor of Zoology
1 certify that 1 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.
Dav i d H. Hirth
Assistant Professor of Forestry


78
Table 21. Vertical stratification of gleaning carnivore species on
Barro Colorado.
Bat species
No. of bats captured
at ground level,
1 to 3 mm
No. of bats captured
at subcanopy levels,
3 to 12 mm
Mi. mega 1 ot i s
M^. b rachyot s
M. h i rsuta
M. crenulatum
T_. ci rrhosus
T. syl vi col a
T. b i dens
P. hastatus
_V. spectrum +
* Significant by Chi Square Test (_P < .05) .
** Highly significant by Chi Square Test (P_ <.0l).
+ Based on two net captures in Costa Rica and one visual sighting on
on Barro Colorado
Yates Correction for Continuity is used on all Chi Square Tests (Sokall
and Roh1f, 1969).


67
gap in body weight between G_. soricina and P_, discolor exists because
of the recent extirpation of a bat species belonging to this guild. As
recently as the early 1950's, Lonchophy11 a robusta (Glossophaginae),
was alive on Barro Colorado (Hall and Jackson, 1953)- This species eats
nectar, pollen, fruit, and insects (Howell and Burch, 19/4). _L- robusta
from Costa Rica weigh about 17 g,and if this species were still present
on Barro Colorado the ratios between body weights of the four omnivore
guild members would be 1.4, 2.6, 1.4. The large ratio between _L. robusta
and P_. di scolor actual ly would have been somewhat less than 2.6 because
of the sexual dimorphism in body weights of P_. discolor. The dimorphism
in body weights between male and female P_. d i scolor is very slight (Table
18) but significant (P_ <.05, Student's t-test) .
Food selection
Nectar and pollen are consumed by guild members almost exclusively
in the dry season, as large flowers suitable for bat use are in bloom
only then (see Phenology). The few data available suggest that during
the wet season fruit and insects become dietary staples (Table 19).
That insects were not present in the food samples from G_. soricina on
Barro Colorado is probably because of poor sample size and the fact that
this species moved out of the study area during the wet season. Nothing
beyond the observations of Jeanne (1970) of P_. stenops eating social
wasp larvae and my two observations of fruit eating is known about the
diet of this bat.
Phyllostomus discolor is neither an extreme specialist nor generalist
in terms of food species (niche breadth = 1 .65)- Several types of flowers
are visited for pollen and nectar in the dry season. And in addition to
insects, several types of fruits are eaten in the wet season. The


LITERATURE CITED
Alvarez, T, and L, Gonzales Quintero. 1970- Analis polnico del
contenide gstrico de murcilagos G1ossophaginae de Mexico.
An. Esc. Nac. Cine. Biol., Mex., 18:137-165.
Baker, J. R. and Z. Baker. 1936. The seasons in a tropical rain-forest
(New Hebrides).--Part 3- Fruit-bats (Pteropidae), J. Linn. Soc.
Lond., 40:123-141.
Beattie, A. J. 1971- A technique for the study of insect-borne pollen.
Pan-Pacific Entomol., 47:82.
Brown, J. H, 1968, Activity patterns of some Neotropical bats. J.
Mamm., 49:754-757-
and J. Lieberman, 1973- Resource utilization and coexistance of
seed-eating desert rodents in sand dune habitats. Ecol., 54:788-797-
Crespo, R. F., S. B. Linhart, R. J. Burns, and G, C. Mitchell, 19/2,
Foraging behavior of the common vampire bat related to moonlight.
J. Mamm., 52:366-368.
Diamond, J, M. 1973- Distributional ecology of New Guinea birds. Science,
179:759-769-
Findley, J. S. and D, E, Wilson, 1974, Observations on the Neotropical
disk-winged bat, Thyroptera tricolor, Spix, J. Mamm,, 55:562-571-
Fleming, T. H, 1971- Artibeus jamaicensis: delayed embryonic development
in a Neotropical bat. Science, 171:402-404.
. 1973 The reproductive cycles of three species of oppossums and
other mammals in the Panama Canal Zone. J. Mamm., 54:439-455.
, E. T. Hooper, and D. E. Wilson. 1972. Three Central American
bat communities: structure, reproductive cycles, and movement
patterns. Ecol., 53:555-569-
Foster, R. B. 1973- Seasonality of fruit production and seed fall in a
tropical forest ecosystem in Panama. Ph.D. Diss., Duke Univ,,
Durham, N. C., 156 pp.
Frankie, G. W,, H. G. Baker, and P. A. Opler. 1974. Comparative
phenological studies of trees in Tropical Wet and Dry Forests in
the lowlands of Costa Rica. J. Ecol., 63:888-919-
115


Table 19. Seasonal use of pollen and fruit by the omnivore guild on
Barro Colorado.
68
Food species
No. of dry season
samples
No. of wet season
samples
Pol 1en:
Och roma 1agopus
Pseudobombax septenatum
Unknown 202
Fruit:
Cecropi a exima
Unknown \2k
Insects :
Pollen:
Och roma 1agopus
Unknown 201
Fruit:
Cecrop ia exima
Piper 109
Fruit:
Unknown 110
Unknown 151
P. discolor, N = 23
6
6
G. soricina, N = 6
3
1
P_. stenops, N = 2
1
2
3
3
1
1
1
1


60
Table 17* Frequency of occurrence of food species in the diet of C_.
pe rspic i 11 ata as determined from fruit droppings and seeds below day
roosts. Sampling periods begin at mid-month.
Plant species Jan-Mar
Ha r-May
May-Jul
Ju1-Sep
Sep-Nov
Nov-Jar' Total
Anacardium excel sum 5
83
39
127
Piper cordulatum
39
35
9
83
P. reticulatum
'
6
6
Piper 109
6
6
Solanum hayseii
1
1
2
Vismia 1
2
2
A
Quararibea asterolepsis
5
15
20
Cassia undulata
5
1
6
Unknown 155
12
12
Unknown R-1
3
3
No data.


32
Table 6. Weights tn grams of canopy frugivore bats on Barro Colorado.
Species
Mean
(x)
Sample
s i ze
(S.D.)
Sample
s i ze
n
Wgt / Wgt* Remarks
1 g sm
V. pus ilia
8.1
0.6
22
--
Fig specialist
C. trinitatum
12.3
1 .2
7
1.53
very rare fig specialist
A. phaeotis
13.0
1.2
30

food genera list
V. helleri
16.2
2.2
8
1 -31
very rare fig specialist
C. vi 11osum
22.4
2.1
13
1.38
fig specia1ist
V. caraccioloi
36.0
2-3
27
1.61
fig specia1ist
A. jamaicensis
47-2
3-4
30
1.31
fig speca 1ist
A. 1ituratus
69-3
5.6
30
1.47
fig specia 1 ist

mean
ratio of wei<
ght increments.44
* Weight of 1
arger species divided
by weight of
sma11e r spec ies
in the pair compared.


Figure 14. Reproductive timing in female Carol la perspec i 11 ata.


19
for this seasonal change In biomass, with Isoptera, Diptera, and
Lepidoptera among the orders eaten by bats that have particularly drama
tic population increases in the wet season. By contrast, small insects
(< 5 mm in length) were abundant throughout the year.


Table 5- Annual variation in species diversity, equitab i 1ity, and species number of fruit bats in the wet
wet seasons of three years
Year
H'
May-July
E
SN
Samp!e
H
July-September
E SN
Samp 1 e
1971
1.129*
0.630
6
89
0.785
0.341
10
174
1973
1 .695
0.664
13
214
1 -330
0.577
10
205
1974
1.385
0.601
10
196
1.346*
0.647
8
76
* These diversity values are probably slight underestimates because of small sample sizes. Species-
number curves for all other samples reached an asymptote indicating that those samples were adequate for
good diversity estimates (see Fleming et al, 1972)


RESOURCE PARTITIONING
Thirty-five species of bats were found to coexist on Barro Colorado
Island in 1973. Thirty-one species were captured in diversity samples
and four additional species were seen in flight or at roosts. Nocti1io
1 epor ? nus, N_. labial is, and Molossus moiossus restricted their flight
activities to habitats that were not sampled--the shallow inlets of the
lake (Nocti1io) and above the forest canopy (Molossus). The fourth
species not captured in the diversity samples, Vampyrum spectrum, is a
top carnivore and may be represented by very'few. individuals on the
island. A pair of V_. spectrum was netted by A. L. Gardner and D. E.
Wilson on 5 January 1973- 1 saw a single animal in June 1973 flying at
dawn. No other sightings of V_. spectrum were reported in 1973-
A first step at understanding how 35 species of bats coexist on
this small island can be made by dividing the fauna into feeding guilds.
Feeding guilds will be distinguished on the basis of two parameters--
general 'food type and method or place of food procurement. It will be
assumed that little or no competition for food resources occurs between
members of different feeding guilds, though they may compete for roost
ing space. The bats on Barro Colorado may be divided into nine feeding
guilds, each of which contains one to nine species.
Justification for the placement of species into specific feeding
guilds will be provided in succeeding sections. For the moment, the
feeding guilds are defined as follows:
(1) "Canopy frugivores" -- forage mostly on fruits that grow in
27


113
rare on the study site late in the wet season, but return and eat mixed
diets of fruit and insects through the dry season. M_. mega 1 ot i s and
ML brachyotis appear to use this strategy. Tonatia sylvicola, however,
remains in the BCI forest all year eating only insects. Janzen (1973)
and Janzen and Schoener (1969) report that watersheds are dry season
refugia for many insect groups. Perhaps some individuals or populations
of gleaning carnivores move to riverine habitats off the island during
lean times.
The reproduct ive strategy of g1eaning earnivores on Barro Colorado.
Micronycteris, Tonatia, and Trachops bear two litters per year. The first
pregnancy of the year occurs at a time of relative food scarcity, but the
birth pulse occurs as large insects are-becoming abundant. The first
lactation and the entire second reproductive cycle occur within months of
food abundance.
The peak in pregnancy for Mimon crenulatum, a monestrous species,
occurs about two months after those of the above gleaning carnivores.
Thus both pregnancy and lactation occur within the year's peak of insect
abundance. Mimon can time its reproductive activity in this manner
because it does not squeeze two reproductive cycles within the months of
large insect abundance as do the polyestrous species of the guild.
$ 1ow-flying hawk ing j nsectivores
P'esource parti t ion i ng i n the s low-f 1 y ing hawk i ng i nsect i vore guild.
Much less is understood about this guild than the others discussed so
far with respect to resource partitioning, foraging strategy, and repro
ductive strategy. It is possible that each family placed in this guild
should constitute a distinct guild, but we do not know enough to be certain.


37
Table 9* Feeding niche breadths of canopy frugivores.
Bat Species
Number of genera of Number of species of Niche Breadth*
known food plants known food plants (loge
V_. pus ilia 2
trinitatum 3
A. phaeotis 10
_V. he Her 2
C_. vil losum 1
_V. caraccioloi b
j ania i cens i s 9
A. 1 i turatus 5
k
h
12
3
3
5
16
7
0.3b
1.33
2.10
1.01
1.01
1 .Ob
1.61
1.33
*Sample sizes for calculating niche breadths are as in Table 7-


ACKNOWLEDGMENTS
This study was funded by NSF Grant GB-36068 to Dr, J. H, Kaufmann,
NIH Biomedical Sciences Grant No, RR7021-07 from the Division of Spon
sored Research of the University of Florida to Dr, S, R, Humphrey, and
the Environmental Sciences Program of the Smithsonian Tropical Research
Institute, The Florida State Museum and Smithsonian Tropical Research
Institute provided logistical support.
Dr, B. K, McNab, both in his writings and classroom discussions,
induced and encouraged the "germplasm" of interest which launched me
into the study of the ecology of tropical bat communities, Drs, S. R,
Humphrey, J, H, Kaufmann, E, Leigh, N, Smythe, A, F, Carr, D, H. Hirth,
and T, C, Lmmel unselfishly took time to provide constructive guidance.
Dr, Robin Foster verified my seed ident ifications and cultured in me a
deep appreciation for tropical plant ecology, Clark Sandford, Julie
Wiatt, Bill Biven, and Janet Hall faithfully assisted with fieldwork and
laboratory preparations under trying conditions. The creative talents
of Nancy Hall¡day and Sylvia Scudder have rendered the illustrations.
Finally, i wish to thank the scientists, students, and visitors
coinciding with my residence on BC1, as well as the Smithsonian staff,
for bringing encouragement, friendship, intellectual atmosphere, and
volleyball to an isolate field station and making 1973 the most pleasant
and memorable year l have experienced.
i i i


9
the vegetation permitted, harp traps were rigged in subcanopy level
"tunnels".
Nets and traps were open from sunset to sunrise 67 times between
11 January and 31 December 1973- On 28 other nights during that period
sampling was conducted for less than a full night. The total sampling
during 1973 involved 4,376 net-hours, 1,213 trap-hours, and 2,324
captured bats.
In 1971, 347 nefhours of sampling during a pilot study yielded
282 bats between 20 June and 18 August. In 1974, 454 net-hours of
additional sampling yielded 278 bats between 10 June and 17 July. No
harp traps were available during these times for effective sampling of
small insectivorous bats.
Because Crespo et aj_. (1972) and Morrison (1975) have demonstrated
that vampires and fruit bats avoid flying during intense moonlight,
whole-night samples were taken only between the last and first quarters
of the moon. Only such whole-night samples were used to calculate
species diversityf and activity cycles were taken during phases of the
lunar cycle that do not produce enought light to influence bat flight
activity.
Nets and traps were, checked at least twice every hour for the
purpose of removing bats. Whenever possible, checks were made more
frequently to prevent bats from chewing out of nets. Upon removal from
a net or trap each bat was placed in an individual cloth bag. Usually
within an hour after capture the bats were banded and released at the
sampling, station. The following data were recorded for each individual:
species, hour of capture, capture location, sex, age class, reproductive
condition of females, food in feces or mouth, weight, and forearm length.


82
Table 22. Weights in grams of slow-flying hawking insectivore bat
species on Barro Colorado.
Bat species
Mean Standard
) deviation
(S. D.)
Sample Wgt / Wgt*
size lg sm
(N)
Embalonuridae
S. 1eptura ** 4.2 -- 1
C. maxi mi 11iani **
5.2

2
1 -25
S. b i 1ineata males
7.7
0.56
1 1
1.47
S. bil ¡neata females
8.7
0.7
3

P. kappleri **
1 1.2

2
1.46
R. tmida
4.2
Vesperti1 ionidae
2
_ _
M. nigricans
4.4
0.67
1 1
1.05
P. suapurensis
16.5
Mormoopidae
1
_ _
P. parnel1 i
22.6
1.48
30
1 -37
* Weight of larger species divided by weight of smaller species in the
pair compa red.
** Males and females are probably dimorphic in body weight.


~J u
45
40
35
30
25
20
15
10
5
0
ro
HOURS AFTER SUNSET


Figure 12.
Reproductive timing
in female Art ibeus jama ? censis.


REPRODUCTION
Three patterns of reproduction occur in Neotropical bats: seasonal
monestry, seasonal polyestry, and year-round polyestry (Fleming, 1973).
Present information indicates that a single young is born per litter
except in the genus Rhogeessa in which the usual litter size is two
(Humphrey and Bonaccorso, 1975)-
Canopy Frug1vore Guild
Canopy frugivores are seasonally polyestrous, with one birth peak
at the end of the dry-to-wet transition and a second about the middle
of the wet season (Figs. 11-13 and Table 25; Wilson, 1975). The first
birth peak for all species coincides with the beginning of the first
predictably steady rains of the year in late April and Hay, a time of
fruit abundance. Large species such as A_. jamaicensis and A. 1 ituratus
are pregnant (as detectable by palpation) by the first week of January.
Sma 1 1 species 1 ike A_. phaeotus are not in a similar stage of pregnancy
until late January. Lactation then proceeds for one or two months during
a period of food abundance. There is a postpartum estrous,and females
are well advanced in the second pregnancy of the year while lactation is
still underway (Fleming, 1971)-
The second birth and lactation peaks are less synchronized among
species because of differences in gestation and lactation periods; the
same is true to a lesser degree within species because of individual
variation. For example, the second peak of lactation occurs in July-
September for A_. j ama i cens i s and A_. phaeot i s but not until Septembei
87


69
available data are too limited to consider niche breadth values for
P_. stenops and G_. sor i ci na, or to calculate niche overlaps between
guild members.
Vert ica1 stratification
All of the flowers and fruits eaten by P_, discolor and 83% of those
eaten by G_. sor ic i na in this study area grow in the subcanopy and canopy
of the forest. Both species were captured most frequently in the upper
levels of the forest, 3 of 4 for G1ossophaga and 40 of 54 for Phy1losto-
mus. For P_. discolor preference for flying above groundstory shrubs is
highly significant (P_<.01, Chi Square Test).
Habitat select ion
Phyllostomus discolor was common in the mature forest and second
growth but uncommon over creeks. Some of the important tree species
producing flowers and fruits eaten by Phy1lostomus are common only in
second growth (e.g, Ochroma); others are common only in mature forest
(e.g. Pseudobombax); and still others are common in both habitats (e.g.,
Cecropia).
Feed ing behavior
During the dry season bats are frequently captured with pollen
heavily dusted over the anterior parts of the body. It is likely that
these animals visit a number of flowers in succession, consuming nectar
and performing pollination services at each flower, and then later
perch to ingest pollen by grooming it from the fur and skin.
None of the bats in this guild were captured carrying fruit in the
mouth,and it is not known whether they use night feeding roosts.
Sixty-nine percent of all P_. discolor captured in all-night samples
were taken within two hours of sunset. Such a strong unimodal pattern


70
of flight activity (Fig. 9) also is reported by LaVal (1970) and suggested
by Heithaus et_ aj_. (197*0 for this species in Costa Rica. My data are
insufficient for discussing the flight activity cycle of Glossophaga;
however, LaVal (1970) reports a strong peak in activity at dusk and in
the first hour of darkness just before the peak in P_. discolor activity.
Sanguivore Guild
Body s ? ze
Of the three extant vampire species, only Desmodus rotundus, the
common vampire, occurs on Barro Colorado Island and in the surrounding
vicinity. The pre-meal mean body weight of D_. rotundus is 33-5 g.
Food selection
Wild vampires feed only on the blood of homoiothermic vertebrates
(McNab, 1973). While vampire feeding behavior and prey selection is
well documented in agricultural areas where domestic livestock are the
chief food source (Turner, 1975), nothing is known of the prey species
of vampires in remote areas where only wild animals are potential hosts.
Vert i ca 1, stratification
Where domestic animals are the source of food, vampires fly almost
exclusively within 3 m of ground level (Bonaccorso, unpublished data).
It ¡s possible that vampires more commonly fly in the canopy level in
isolated forests where arboreal species (e.g., monkeys and birds) may be
important sources of blood meals for these bats. On Barro Colorado
island two vampires were captured in subcanopy nets and one in a ground
net.
Habitat selection
Vampires were clearly more abundant on Buena Vista Peninsula than on
Barro Colorado Island. Desmodus was the fourth most abundant species in


BIOGRAPHICAL SKETCH
Frank Joseph Bonaccorso was born 23 October 19^-8 in San Fernando,
California. He received his Bachelor of Arts in zoology with Departmental
Highest Honors from the University of California, at Los Angeles, in
June 1970, In September 1970, he began work on the degree of Doctor
of Philosophy in the Zoology Department at the University of Florida.
In August 1975, he will begin teaching as Lecturer in the European
Division, University College of the University of Maryland.
Frank is a member of the American Society of Mamma legists and the
Association for the Study of Animal Behaviour, He was awarded the
Austin Medal by the Associates of the Florida State Museum in 1975
for scholarly achievement and research in field biology. He also has
distinguished himself in the art of film-making for his works ~~ The
Maroon Prune Kid (1973) and The Maroon Prune Kid Goes To Col 1ege (1975).
122


HNOW
INSECT BIOMASS


25
20
15
10
5
0
Artibeus jamaicensis N
829
N = 33
V£>
HOURS AFTER SUNSET


Appendix 1. Seasonal
Bat species
variation in
Dry
captures of each bat
Dry-Wet Early-
Transit ion Wet
species or
Season
M i d-
Wet
i Barro Colorado Island in 1973
Late- Wet-Dry
Wet Transition Total
C. castanea *
12
4
9
8
1
13
47
C perspici11 a ta
19
62
11
8
17
7
124
V. p u s 1 1 a *
8
22
9
5
44
C tr initatum
1
4
2
1
2
10
A. phaeotis *
39
25
23
21
8
23
139
V.- heller i
2
1
7
2
1
1
14
C. vi11osum *
9
11
4
1
3
31
V. caraccioloi
3
8
2
17
5
2
37
A. ¡amaicensis
123
201
123
131
189
81
848
A. 1ituratus *
22
5
15
5
25
16
88
C. senex
1
2
3
G. sor¡cia *
1
2
1
1
5
P. discolor
8
14
6
13
8
10
59
P. stenops
*1
\
-
1
D. rotundus
1
1
1
3
M. meqalotis *
3
3
1
1
1
1
10
120


5
Barro Colorado is in the Tropical Moist Forest life zone (Holdridge,
I967). This 15 km island is covered with mature forest that is over
60 years in age. The only human disturbance to the vegetation results
from re-cutting forest trails and maintaining a small laboratory clear
ing, and an undetermined amount of illegal poaching. Further details
on the geology, climate, biology, and history of the island are given by
Kaufmann (1962) and Foster (1973).


107
entirely on fruits growing in the forest canopy on trees, vines, and epi
phytes. Individuals of most of these plants occur at very low densities
and in patchy distributions within the forest. Most of the resource trees
are very large and produce enough fruit to feed hundreds of bats every
night during their fruiting periods of a week or so. Because a great
range in the size of preferred canopy fruits is available, it is possible
for many bat species to specialize in taking food particles of a particular
size class. Seven species on BCI are fig specialists that partition figs
primarily on the basis of size. The other species is a generalist with
regard to the types of fruit in its diet.
The fig specialists appear to have large home ranges (about 3 km4
for Artibeus jamaicensis) compared to other bats of similar size, and
they travel through much of the home range in the course of a night
searching for widely scattered resource plants (Heithaus et a 1. 1975;
Morrison, 1975; Bonaccorso, unpubl. data). Artibeus phaeotis, the fruit
generalist, appears to have a comparatively small home range for its size,
probably because it feeds on more kinds of fruits and thus is more likely
to encounter a suitable food resource in a smaller area than a fruit
specia 1ist.
The foraging strategy of canopy frugivores on Barro Colorado.
Frugivorous bats consume about their own weight in fruit per night
because they appear to have low assimilation efficiencies and do have
high metabolic rates (McNab, 1969). Each bat must make about a dozen
visits to one or a few resource trees per night. Each visit involves
picking a single fruit and carrying it away to a feeding roost where the
fruit is ingested. Once a tree with mature fruits is located an individ
ual bat may return to it repeatedly for over a week, but much time and


112
Gleaning earn!vores
Resource partitioning in gleaning carnivores. Nearly all gleaning
carnivores depend on large insects as the primary food resource, though
a wide range of vertebrates, invertebrates, and even fruits supplement
the diet. This large feeding guild has a more complex array of parti
tioning mechanisms than any other guild on Barro Colorado, Differences
in body size, general food types, foraging microhabitats, and possibly
activity cycles operate to maintain the ecological distinctness among
these species. Future investigators should consider potential competi
tion between bats and other taxa that prey on large insects such as noc
turnal spiders, caprimulgid birds, and tree frogs.
The foraging st rategy of g 1 ean i ng earni vores o_n_ Barro Colorado.
Gleaning carnivores prey upon food items that are moderately large in
relation to their own body weight just as fruit bats do. Also like fruit
bats they carry individual prey items to feeding roosts whether the food
be large insects (Wilson, 1971b) or birds (Bradbury, pers. comm.). Because
of the high protein content of their diet these bats probably eat a
smaller weight of food in proportion to their body size and also fewer
prey items per night than do frugivores. Thus, gleaning carnivores spend
less time and energy transporting food items between foraging sites and
feeding roosts than do fruit bats. It would be interesting to compare
these guilds in terms of searching effort devoted to foraging, but such
data are not available for gleaning carnivores.
Late in the wet season and in the dry season large insects are rela
tively unavailable to these bats, and some gleaning species alternate
foraging patterns. Several of the smaller and medium sized species become


108
energy are spent scouting for trees that will be in fruit in future days
(Morr ison, 1975)-
For at least a couple of weeks during the beginning of the dry season
when fruits are scarce and bat pollinated flowers are very abundant, at
least three of the canopy frugivores switch partly to pollen and nectar
diets. In drier forest habitats where suitable flowers are available over
a longer dry season, stenodermine bats feed on nectar and pollen through
much of the dry season (Heithaus et_ aj_. 1975) -
The reproductive strategy of canopy frugivores on Barro Co 1 orado.
Adult females have two litters per year. Birth pulses are synchronized
within populations and coincide with the two predictable seasonal peaks in
fruit abundance. Late term pregnancy, lactation, and the learning
processes associated with foraging by young bats, the events of highest
energetic cost in the life cycle of these bats, occur at times of food
abundance. The proximal cues that provide the timing for reproductive
activities are not known but may involve rainfall or photoperiod.
Groundstory frugivores
Resource partitioning in the groundstory f rug ivore guiId. Ground-
story frugivores specialize on eating fruits that grow on shrubs, most of
which are less than 3 m in height. To a lesser extent these bats also
feed on canopy fruits, and in dry forest areas of Belize (Bonaccorso,
unpubl data) and Costa Rica (Heithaus et_ aj_., 1975) guild members also
feed on nectar and pollen in the long dry season.
Two species in the Carol linae, Carol lia castanea and C_. pe rsp i c i 1 1 ata,
form the groundstory frugivore guild on Barro Colorado. In any one place
in closed canopy forest habitat throughout the Neotropical region, this


31
food resources are partitioned largely by particle size as predicted by
the theoretical reasonings of Hutchinson (1959), McNab (1971a and b) and Hay
(1973) These authors postulate that similar species may avoid competi
tion for food by differing in body weights by a factor of at least 1.3
(May, but McNab and Hutchinson used the figure 2.0), each species
specializing in food particles proportional to its body weight (and to
the linear dimensions of its food handling apparatus, e.g., tooth row
length, gape size, tongue length, etc.).
The gleaning carnivore and slow-flying hawking insectivore guilds
each contain some species that are very similar in size to other species
of their guilds. We might expect that such species feed on similar
sized food particles of very different taxa or of similar taxa from
different microhabitats.
The nectar-pol1en-fruit-insect omnivore guild contains species very
different in size; this may partly result from a recent extirpation of
Lonchophylla robusta, a species intermediate in size between Glossophaga
soricina and Phyllostomus discolor. The sexual dimorphism in body
weights of P_. discolor is another complicating factor.
Canopy Frugivore Guild
Body size
Eight species, all in the subfamily Stenoderminae of the Phyllosto-
matidae, constitute the canopy frugivore guild on Barro Colorado. These
eight species range from 8.1 to 69-3 g in mean body weight (Table 6).
There is a mean increment of 1.44 between the body weights of adjacently
sized animals among the seven species designated as fig feeding
specialists in Table 6. Artibeus phaeotis, a feeding generalist, and
Chi roderma trinitatum are nearly the same in size.


Figure 15. Reproductive timing in female Pteronotus parnellii.


Table 2. Monthly availability of fruits and flowers used by bats on Barro Colorado Island, Dashed lines in
dicate food present in fecal samples. Asterisks indicate food known to be available, but not present in
fecal samples. Plant types: T = tree, S = shrub, V vine, E = epiphyte, U = unknown
Plant species
Plant type Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
FI owe rs
Och roma 1agopus
Pseudobombax septena turn
Unknown 201
Unknown 202
Ficus inspida
F.
obtusifolia
F.
popenoae
F.
yoponens i s
_F.
102
Spond ias mombin
S.
rad 1kofe ri
Dipteryx panamensis
Calophyl 1 urn 1 ong i fol ia
Qua ra ribea as te ro1eps i s
T **
T **-- ->
U
U
Fruits
T *****
T
T
T
T
T
T
T
T
T


Figure 7-
for three sma!1
Frequency of capture through
canopy frugivore species.
the night as a measure of
f1ight act ivity


FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUNITY
OF BATS IN PANAMA
By
FRANK JOSEPH 30NACC0RS0
A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL OF
THE UNIVERSITY OF FLORIDA IN PARTIAL
FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
1975

This work ¡s dedicated to Clark Sanford, Julie Wiatt, and Bill
Biven, my field assistants, who endured a year of damp weather, irritat
ing insects, bat bites, tough pork chops, and numerous other tropical
hardships, yet shared the enumerable joys we encountered. We learned
much together of tropical forests and ourselves and are better people
for it.

ACKNOWLEDGMENTS
This study was funded by NSF Grant GB-36068 to Dr, J. H, Kaufmann,
NIH Biomedical Sciences Grant No, RR7021-07 from the Division of Spon
sored Research of the University of Florida to Dr, S, R, Humphrey, and
the Environmental Sciences Program of the Smithsonian Tropical Research
Institute, The Florida State Museum and Smithsonian Tropical Research
Institute provided logistical support.
Dr, B. K, McNab, both in his writings and classroom discussions,
induced and encouraged the "germplasm" of interest which launched me
into the study of the ecology of tropical bat communities, Drs, S. R,
Humphrey, J, H, Kaufmann, E, Leigh, N, Smythe, A, F, Carr, D, H. Hirth,
and T, C, Lmmel unselfishly took time to provide constructive guidance.
Dr, Robin Foster verified my seed ident ifications and cultured in me a
deep appreciation for tropical plant ecology, Clark Sandford, Julie
Wiatt, Bill Biven, and Janet Hall faithfully assisted with fieldwork and
laboratory preparations under trying conditions. The creative talents
of Nancy Hall¡day and Sylvia Scudder have rendered the illustrations.
Finally, i wish to thank the scientists, students, and visitors
coinciding with my residence on BC1, as well as the Smithsonian staff,
for bringing encouragement, friendship, intellectual atmosphere, and
volleyball to an isolate field station and making 1973 the most pleasant
and memorable year l have experienced.
i i i

TABLE OF CONTENTS
Page
AKNOWLEDGEMENTS iii
ABSTRACT v
INTRODUCTION 1
STUDY AREA 3
MATERIALS AND METHODS 6
Mathematical Formulae 10
PHENOLOGY AND FOOD RESOURCES 12
SPECIES DIVERSITY. . 20
RESOURCE PARTITIONING 27
Canopy Frugivore Guild 31
Groundstory Frugivore Guild 50
Scavenging Frugivore Guild 62
Nectar-Pol 1 en-Fru i t-1 nsect Omnivore Guild 65
Sanguivore Guild 70
Gleaning Carnivore Guild 73
Slow-Flying Hawking Insectivore Guild.... 80
REPRODUCTION 87
Canopy Frugivore Guild 87
Groundstory Frugivore Guild 94
.Scavenging Frugivore Guild 97
Nectar-Pol len-Fru i t~ I nsect Omnivore Guild 97
Sanguivore Guild 97
Gleaning Carnivore Guild..,.. 97
Slow-Flying Hawking Insectivore Guild 98
CONCLUSIONS 101
Species Diversity And Phenology.. v 101
Foraging And Reproductive Strategies 104
LITERATURE CITED 115
APPENDIX 120
BIOGRAPHICAL SKETCH 122

Abstract of Dissertation Presented to the
Graduate Council of the University of Florida in Partial
Fulfillment of the Requirements for the Degree of Doctor of Philosophy
FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUNITY
OF BATS IN PANAMA
By
Frank Joseph Bonaccorso
August, 1975
Chairman: Dr. John H. Kaufmann
Major Department: Zoology
Resource partitioning, reproduct ion, species diversity, and
community structure in a forest community of 35 bat species were
studied on Barro Colorado island, Panama Canal Zone, Sixteen months
of field-work were conducted between July 1971 and August 197^. Over
2,800 bats were captured, banded, and released with data collected on
food habits, activity cycles, habitat selection, reproductive timing,
and morphological feeding adaptations for each species. Information on
the seasonality and abundance of fruit, flower, and insect resources
used by bats also was collected.
The diversity of tropical lowland bat communities in any one
habitat changes significantly on a seasonal basis. Fluctuating levels
of food resources require that many species utilize different habitats
and foraging strategies through a year. Competitive interactions,
predator avoidance, and climatic fluctuation further influence the
v

foraging strategies of each species. Tropical bat faunas can be
broken down into feeding guilds on the. basis of general food habits
and method of food procurement. Within the most complex guilds, such
as the canopy frugivore guild, food resources are partitioned in time
and space and by size and quality. Within the simplest guilds food
resources are partitioned primarily by food particle size. The most
important mechanism of resource partitioning separating similar species
is food particle size. Some species complexes appear to be limited not by
absolute amount of food but by the distribution of those resources in
a few concentrated patches accessible to only a limited number of
individuals at a given time. Reproduction coincides with high levels
of available food resources within each feeding guild.

INTRODUCTION
Mention of the words "tropical forest" among ecologists typically
triggers visions of species rich communities, complex competitive inter
actions, and relatively stable environmental conditions. Indeed, faunal
lists in the tropics are large^and food webs are intricately complex.
It is also true that organisms inhabiting tropical latitudes usually are
subjected to less extreme environmental fluctuations than are their
counterparts in temperate or polar regions. However, it is too infre
quently emphasized that even species in tropical forests must possess
behavioral flexibility to counter and survive climatic and biotic
environmenta1 change. There are two major reasons for this general lack
of insight. Firstly, few detailed studies of tropical organisms have
spanned periods of several years or even seasons. And secondly, the
behavioral responses of tropical species to environmental fluctuations
are often quite subtle. Whereas temperate animals commonly exhibit
obvious >and dramatic reactions to seasonal change such as hibernation
or long distance migration, tropical species may only need to switch
food types or microhabitats, or briefly halt reproduction. Nevertheless,
genetic and behavioral flexibility are requisites for survival for most
tropical as well as temperate species.
Tropical bats are particularly worthwhile subjects for studies of
diversity, competitive interaction, and response to environmental fluc
tuation because of their individual abundance and the complex taxonomic
1

2
and ecological communities they form. About 100 species of bats occur
in each of the small countries of Central America (Hall and Kelson,
1959) it is common to find 30 to 50 species in one macrohabitat measur
ing a few square kilometers in area. For example Barro Colorado Island
(15 sq km), Panama, currently supports populations of at least 35 species.
Among tropical bat species, few are known or suspected to reproduce
year round or to specialize on constantly abundant food resources. The
common vampire bat, Desmodus rotundus, is one notable exception (Wimsatt
and Trapido, ¡952). instead, most bats, even in equatorial regions, are
seasonally polyestrous or monestrous in reproduction (Baker and Baker,
1936; Mutere, 1970; Fleming, 1973) and make seasonal shifts in food
habits (Wilson, 1 971b; Flemi ng e_t_ aj_. 1972; Hei thaus et al ., 1975).
The objective of this dissertation is to delineate adaptive strate
gies used by tropical bats that enable them to survive fluctuating
environmental conditions and coexist with numerous similar species in
complex communities. The field work represented herein documents
seasonal changes in diversity, mechanisms of resource partitioning, and
reproductive timing through one complete year and portions of two other
years..

STUDY AREA
The primary research site was on Barro Colorado Island (BCl).
Barro Colorado lies within freshwater Lake Gatun, in the Panama Canal
Zone, at 9 10 North latitude and 79 51' West longitude. This field
site was selected because it has a rich bat fauna, relatively undis
turbed mature moist forest, modern living and laboratory facilities,
and reference collections of animals and plants. A secondary site was
located on the mainland opposite BCl at the base of Buena Vista Penin
sula.
The climate of this lowland area of Panama is warm and humid with
a seven-month wet season and a three-month dry season. Dry season
months, January through March, each receive less than 60 mm of rain.
Wet' season months, May through November, typically receive in excess
of 250 .mm of rain. April and December are months of transition between
dry and wet seasons and receive amounts of rain that vary considerably
from year to year. Thus in years when April and December are very dry,
the dry season may last for five months. Average annual rainfall since
1926 has been 2,820 mm (Smythe, 197^). Monthly sums of rainfall for
1973 are shown in Table 1.
During night time sampling of bats, relative humidity under the
forest canopy never fell below 80 percent. Measurements were made at
2 m above ground with a sling pyschrometer. Daily temperatures on the
forest floor fluctuate from a mean minimum of 22.1 C to a mean maximum
of 28.0 C with no significant seasonal variation (Smythe, 197^).
3

Table 1. Rainfall (mm) on Barro Colorado Island, 1973 (after Smythe, 197*0
Jan Feb Mar Apr
May Jun J u1 Aug Sep Oct Nov Dec
Rainfall by calendar 58 18 26 19 274 323 231 358 3^1 261 578 45
month
Rainfall corresponding 45 23 11 7 110 370 250 334 278 353 375 346 58
to mid-month bat sampling
pe riod s

5
Barro Colorado is in the Tropical Moist Forest life zone (Holdridge,
I967). This 15 km island is covered with mature forest that is over
60 years in age. The only human disturbance to the vegetation results
from re-cutting forest trails and maintaining a small laboratory clear
ing, and an undetermined amount of illegal poaching. Further details
on the geology, climate, biology, and history of the island are given by
Kaufmann (1962) and Foster (1973).

MATERIALS AND METHODS
2
Seventeen sampling stations were located in an approximately 2 km
central strip of Barro Colorado Island and one station was on Buena Vista
Peninsula (Fig. 1). Habitats sampled during the study are classified as
mature forest (14 stations on BCI), creeks (3 stations on BCI), and
second growth (1 station on Buena Vista). The mature forest has a com
pletely closed canopy and is a minimum of 60 years old in all places.
Some tracts within the forest have been undisturbed for 400 years
(Robin Foster, pers. comm.). The creek stations are lined with rich
shrub growth and the creek bed receives direct sunlight. The second
growth habitat at Buena Vista is approximately 20 years old and consists
of thick shrub growth and scattered small trees that form a discontin
uous canopy.
Except on rare occasions when nets were damaged by tree falls or
vandalized by poachers, each sampling station consisted of four or six
6 x 2 m mist nets and one or two Tuttle harp traps (described in Tuttle,
1974) set across permanent trails. Nets were set in pairs at 100 m
intervals, with one of each pair at ground level (0 to 3 m) and the other
at subcanopy and lower canopy level (3 to 12 m). Early in the study nets
were rigged in the canopy as high as 25 m above ground, but use of these
nets was soon discontinued because few bats were captured in them,which
seemed to reflect a lack of much flight activity in the canopy levels.
Harp traps were usually set at ground level in low, narrow tunnel-like
passages created by the vegetation and trails. At a few stations where
6

Figure 1. Barro Colorado study area showing the 17 sampling stations.

Orchid
island
Buena Vista
Point
To mainland station
Frijoies
Bay
Pena Blanca
Bay
Colorado
A Point
Gigante
Bay
79 52'
7 95r
7950'

9
the vegetation permitted, harp traps were rigged in subcanopy level
"tunnels".
Nets and traps were open from sunset to sunrise 67 times between
11 January and 31 December 1973- On 28 other nights during that period
sampling was conducted for less than a full night. The total sampling
during 1973 involved 4,376 net-hours, 1,213 trap-hours, and 2,324
captured bats.
In 1971, 347 nefhours of sampling during a pilot study yielded
282 bats between 20 June and 18 August. In 1974, 454 net-hours of
additional sampling yielded 278 bats between 10 June and 17 July. No
harp traps were available during these times for effective sampling of
small insectivorous bats.
Because Crespo et aj_. (1972) and Morrison (1975) have demonstrated
that vampires and fruit bats avoid flying during intense moonlight,
whole-night samples were taken only between the last and first quarters
of the moon. Only such whole-night samples were used to calculate
species diversityf and activity cycles were taken during phases of the
lunar cycle that do not produce enought light to influence bat flight
activity.
Nets and traps were, checked at least twice every hour for the
purpose of removing bats. Whenever possible, checks were made more
frequently to prevent bats from chewing out of nets. Upon removal from
a net or trap each bat was placed in an individual cloth bag. Usually
within an hour after capture the bats were banded and released at the
sampling, station. The following data were recorded for each individual:
species, hour of capture, capture location, sex, age class, reproductive
condition of females, food in feces or mouth, weight, and forearm length.

10
Age classes were distinguished as follows. Infants were unable to
fly and were encountered only when carried by the mother. Juveniles were
able to fly but still had the infant pelage. Subadults had the adult
pelage but were smaller in weight than adults and were reproduct ively
immature. Adults possessed both adult pelage and weight.
Pregnancy, lactation, and reproductive inactivity of adult females
were determined by palpation. Additionally, females could be distin
guished as null¡parous or post-1actat¡ng by examining the condition of
the teats.
Fecal pellets obtained from individual animals were placed in
separate glassine envelopes for laboratory identification of food
species. Fruits and pollens in fecal pellets were identified to species
by comparing unknowns with seeds, pulp fibers and pollen grains in a
reference collection assembled by the author. Pellets were collected
from insectivores but remain unidentified because the hard parts of
arthropods eaten by bats are masticated into tiny fragments that are
difficult to identify. Pollen on the fur was collected by swabbing
with a gelatin described by Beattie (1971). The pollen-containing
gelatin'was then melted on slides for microscopic identification.
Frequently, animals were captured with whole fruits held in the mouth.
Additional information on food habits was gathered by placing plastic
sheets under two roost trees of Carol iia perspeciilata to gather
discarded fruits and fecal matter.
Hathematicai Formu1ae
(1) Species Diversity, H1 = £p¡ loge pj, where p¡ is the number of the
i th species divided by sample size (Shannon and Weaver, 1949),

11
(2) Equitabi 1 ity, E = H/Hmax, where Hmax is the natural logarithm of
the number of observed species (Sheldon, 1969).
(3) Niche breadth, loge B = ~Zp¡ loge p¡, in which the functions are
the same as described in Equation 1. Values approaching zero indicate
narrow niche breadths and specialists. Values approaching one indicate
wide niche breadths and generalists (Levins, 1968).
a 2 2
(4) Niche overlap, CA= 2£ X¡ Yj/£ X¡ + Y¡ where X¡ is the propor
tion of the ith food species in the diet of bat species X, and Y¡ is the
proportion of the ith food species in the diet of bat species Y (florista,
1959). follow Zaret and Rand (1971) in considering species with over
lap values greater than 0.6 to be critically similar in terms of food
overlap.

PHENOLOGY OF FOOD RESOURCES
Most of the bat species on Barro Colorado depend largely on fruit,
flowers, or insects as food resources. Only a few species feed on the
flesh or blood of vertebrates or non-insect invertebrates. The abundance
and diversity of fruits, flower's, and insects in Central America, even
in moist and wet forests, strongly fluctuate on a seasonal time scale
(Foster, 1973; Smythe, 1974; Frankie et al., 1974).
Pollen and nectar on Barro Colorado are available to bats as reliable
food sources only in the dry season, and only four species of flowering
plants are known to be used by bats (Table 2). Two common species,
Ochroma 1agopus and Pseudobombax septenatum, flower from mid-December to
mid-March, While these two species are in bloom nectar and pollen are
very abundant. The other two pollen types used by bats remain unidenti
fied. One of these is known only from February-March sampling and the
other from August-September.
Fruits from 45 plant species were found to be eaten by bats on the
island (Table 2). Nineteen of these species were trees, 11 were shrubs,
four were vines, four were epiphytes, and seven are unknowns. Mature
fruits of the species eaten by bats are available all year. There are
times, however, when few fruits of only a few species are available.
During 1973 a maximum of 19 fruiting species was available from mid-
March to mid-April, and a minimum of 6 species was available in November-
December (Table 2), Two of the fruits available in November-December,
12

Table 2. Monthly availability of fruits and flowers used by bats on Barro Colorado Island, Dashed lines in
dicate food present in fecal samples. Asterisks indicate food known to be available, but not present in
fecal samples. Plant types: T = tree, S = shrub, V vine, E = epiphyte, U = unknown
Plant species
Plant type Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
FI owe rs
Och roma 1agopus
Pseudobombax septena turn
Unknown 201
Unknown 202
Ficus inspida
F.
obtusifolia
F.
popenoae
F.
yoponens i s
_F.
102
Spond ias mombin
S.
rad 1kofe ri
Dipteryx panamensis
Calophyl 1 urn 1 ong i fol ia
Qua ra ribea as te ro1eps i s
T **
T **-- ->
U
U
Fruits
T *****
T
T
T
T
T
T
T
T
T

Table 2 continued.
Plant species
Plant type Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Cecropia exima
T
C. obtusifolia
T ******
Anacardium excelsum
T
Solanum hayesii
T
Vismia sp-1
T
Vismia sp-2
T
Astrocaryum standleyanum
T ****** *****
Tetrathy1acium Johansen!
T
Poulsenia armata
T
Cassia undulatum
V
Markea panamensis
V
C1 usia odorata
V
Unknown 126 (Pass ifloraceae) V
Unknown 101 (Araceae)
E
Unknown 103 (Araceae)
E
Aechmea t i 11andsiodes
E
Carludovicia palmata
-p~
S
Havetiopsis 125
E

Table 2 continued
Plant species
Plant type
Piper aequa1e S
P_. carri loanum S
P_. cordulatum S
_P_. marg inatum S
P_. ret i cul atum S
Piper 109 S
P i pe r 11 4 S
Piper 116 S
Piper 120 S
Piper 122 S
Unknown 104 U
Unknown 110 (Cucurbitaceae) U
Unknown 127 U
Unknown 131 U
Unknown 117 U
Unknown 124 U
Unknown 130 U
Total number of food plant species
a va i 1ab1e
Mar Apr May Jun Jul Aug Sep Oct Nov Dec
17 19 17 12 15 10 11 7 86

16
Ficus inspida and F_. yoponens i s, were very scarce, but Spond ias
radlkoferi and S. mombin were quite abundant.
Most of the plant species producing fruits eaten by bats produce
ripe fruits for periods of only one to four months. Only three species,
F_. i ns i p i da, F. obtus i fol ia and _F. yoponens i s have ripe fruits avail
able nine or more months per year. individuals in the populations of
these fig species fruit asynchronously once or twice per year.
F_. inspida and f_. yoponens i s populations show three major fruiting peaks
and troughs each year (Morrison, 1975)
The plant genera Cecropi a, Spondias, Vismia, and Piper each have
two or more bat-dispersed species that set fruit in sequential time
periods (Table 2). There are 10 species of pipers on BCI eaten by bats.
Though no one of these species is available for more than a few months,
two or more species have ripe fruit throughout the year. Heithaus et ai.
(1375) report that pipers are important bat fruits in Costa Rica and
that several species are available in similar sequential series. Snow
(1965) reports that 18 species of the bird-dispersed genus Mi conia are
sequentially available throughout the year in Trinidad.
The biomass and numbers of nocturnal insects caught in light traps
in Barro Colorado forest over a three-year period were reported by Smythe
(197^). Though these samples represent all nocturnal flying insects,
not just those eaten by bats, they provide a useful index of the abun
dance and fluctuation of the potential food resources for insectivorous
bats through the year (Fig. 3). The light trap collections show that
nocturnal insect biomass in the early wet season is as much as eight
times that of the biomass at the end of the wet season and during the
dry season (Fig. 2). Large insects (> 5 mm in length) were responsible

Figure 2. Schematic representation of fluctuation in biomass of nocturnal flying
insects through the year (based on samples from three years, after Smythe, 197^).

HNOW
INSECT BIOMASS

19
for this seasonal change In biomass, with Isoptera, Diptera, and
Lepidoptera among the orders eaten by bats that have particularly drama
tic population increases in the wet season. By contrast, small insects
(< 5 mm in length) were abundant throughout the year.

SPECIES DIVERSITY
Considerable variation occurred in the bimonthly measures of species
diversity (Table 3). All three diversity indices, H1, E, and SM, were at
maxima during the dry-to-wet transition sampling period. The three diver
sity measures then declined in each of the next three bimonthly periods
to a minimum in the late-wet season. Whereas 27 bat species were present
in the study area in the d ry-to-wet transition, only 13 species were
sampled in the late-wet season. During this same interval H1 dropped
from 2.33 to 1.52 and equitability from 0.707 to 0.515. In the wet to
dry transition period the diversity values began to increase. Dry season
values were very similar to wet-dry transition values^but SN increased
from 22 to 25 in this period.
The diversity values were lowest in the mid- and late-wet season
samples because 13 of the species common in the dry season became notice
ably rare or absent (indicated by asterisks in Appendix 1) from the study
area in'one or both bimonthly periods. These include seven insectivorous
species (k~]% of the total insectivorous species), five frugivorous
species {kl%), and one nectarivorous species (50%). These species appear
to move to other habitats precisely at the time when bat-dispersed fruits
and nocturnally flying insects, the two most important food resources for
bats in this community, become relatively scarce on the study site (Fig.
2 and Table 2).
Of the seven insectivorous bat species that move out of the
mature forest late in the wet season, six are foliage gleaners and one
20

Table 3- Seasonal variation in species diversity, species number, equitab i 1ity, and sampling abundance of
31 bat species on Barro Colorado Island. Sampling periods begin at about the middle of each cal
endar month and are based on lunar cycles.
Seasons:
Dry
D ry-Wet
transition
Early-
V/e t
M i d-
We t
Late-
Wet
Wet-D ry
T ransition
Months:
Jan-Ma r
Ma r-May
May-Jul
Jul-Sep
Sep-Nov
Nov-Jan
Species .Diversity (Hf)
2.147
2.332
2.175
1 .824
1 -517
2.157
Equitab i 1 ity (E)
0.667
0.707
0.667
0.599
0.515
0.688
Species Number (SN)
25
27
26
21
19
22
Bats Captured/sampling-hr.
0.301
0.425
0.339
0.29S
0.423
0.367
Total Bats Sampled
304
470
291
256
307
185

22
Is an aerial hawker. The foliage gleaners prey chiefly on large insects
such as cicadas, grasshoppers, and roaches (Wilson, 1371b; this study).
Smythe (197*0 has shown that large nocturnal insects (greater than 5 mm
in length) become quite scarce on this same study area beginning in the
middle of the wet season, whereas small insects (smaller than 5 mm in
length) are relatively constant in abundance through the year. It
appears that the foliage-gleaning bats find food resources in the study
area sufficiently depressed in the latter part of the wet season that
they move out of the area. On the other hand, small insects remain an
abundant food resource; and aerial feeding bats remain in the
mature forest of Barro Colorado all year. Peropteryx kappleri, an
aerial feeding bat, is an exception as it does move out of forest habitat
in the late wet season.
Of the two bat species that are primarily nectarivorous in this
community, Glossophaga soricina switches from pollen and nectar to fruits
and insects in the early wet season and then moves out of the area in the
middle wet season, not to return until bat flow'ers appear in the dry
season. Phyllostomus discolor stays in the area the entire year, sub
sisting on fruits and insects during the wet season.
Among the fruit-eating species that seasonally move in and out of
the Barro Col orado mature forest is Vampyressa pusilla, the smallest
species of the 13 frugivorous bats on BCI V_. pus ilia is a feeding
specialist on small fig fruits. This bat left the study area when few
individuals of its most important food species, Ficus yoponensis, were
producing fruits in July-October and returned in November when mature
_F. yoponensis fruits were again abundant. While specific reasons why
other frugivorous species moved in and out of the study site are unclear,

23
their absence in September-November corresponds with the annual period
when few food plants are producing fruit (Table 2).
The abundance of individual bats on the study area, as measured by
the number of bats captured per sampling-hour, showed a pattern of
seasonal change markedly different from the diversity measures pattern.
Bats were captured in greatest numbers relative to sampling effort in
the dryto-wet transition, 0.425 bats/hr, and in the late wet season,
0.423 bats/hr (Table 3) The large numbers of bats captured in the dry-
to-wet transition sampling reflect large populations. Food resources
were abundant then; females of most species were in the latter stages of
lactation; and juveniles were entering the flying population and learn
ing to forage. These latter two activities are among the most energet
ically demanding in mammalian life cycles (Miguela, 1969; Studier et ai.
1973), and the timing of these costly activities seems geared to a period
of food abundance.
The late wet season peak in capture rate does not solely reflect
large numbers of individuals on the study area. Though a number of
species had at this time moved out of the young forest, some of the
remaining frugivorous species were recruiting juveniles into the flying
population from the second birth pulse of the year. Probably much of
the high capture rate is attributable to intense foraging activity
necessitated by low food supplies.
The diversity values for insectivorous and frugivorous species,
when computed separately, change similarly through the seasons (Table 4)
For both groups, species diversity is high from mid-November through
mid-July and low the remainder of the year. Fruit bat diversity rises
and falls in time as does the diversity of fruit (see Table 2). However

Table 4.
Seasonal variation in species diversity, species number, and equitability of frugivorous
and insectivorour bat species on Barro Colorado Island. Sampling periods begin at about
the middle of each calendar month and are based on lunar cycles.
Seasons :
Dry
Dry-Wet
T ransition
Early-
Wet
Mid-
Wet
Late-
Wet
Wet-Dry
Transition
Months:
Jan-Ma r
Mar-May
May-Ju1
Jul-Sep
Sep-Nov
Nov-Jan
F rug ? vores
Species Diversity
(h ')
1.717
1.705
1.695
1.330
1 .094
1 .662
Equitabi1ity
(E)
0.650
0.646
0.661
0.577
0.456
0.693
Species Number
(SN)
12
12
12
10
1 1
10
Total Bats Sampled
249
263
21 4
205
261
162
I nse
ctivores
Species Diversity
(H1)
1.909
1 -587
1.526
1 .278
1 .003
1 .698
Equitabi1ity
(E)
0.796
0.618
0.614
0.555
0.482
0.737
Species Number
(N)
12
Is
13
10
8
10
Total Bats Sampled
55
107
76
43
46
22

insectivore bat diversity sharply rises four months before insect biomass
explosively increases (see Fig. 2). The latter anamoly may be due to
ineffective harp trap placement and particular under-representation of
the abundant species, Pteronotus parnellii, during the first months of
field work. This would cause the dry season diversity value to be higher
than it should be. Most species of fruit bats remain in the BC1 mature
forest habitat throughout the year. On the other hand, the species
number of insect-eating bats in the dry-to-wet transition is nearly
double that of the late wet season because of the movement of foliage-
gleaning species in and out of the forest.
A measure of annual variation is achieved by comparing the diver
sity of frugivorous species in June, July and August of 1971 1973 and
1974 (Table 5). In all three years there is a consistent trend toward
lower diversity as the wet season progresses. However, the magnitude
of the diversity values varies from year to year. This indicates that
some annually variable factor or complex of factors, possibly food
availability, predation, or reproductive success, influences fruit bat
species diversity. Insectivore diversity is not compared because harp
traps for effective sampling were available only in 1973-

Table 5- Annual variation in species diversity, equitab i 1ity, and species number of fruit bats in the wet
wet seasons of three years
Year
H'
May-July
E
SN
Samp!e
H
July-September
E SN
Samp 1 e
1971
1.129*
0.630
6
89
0.785
0.341
10
174
1973
1 .695
0.664
13
214
1 -330
0.577
10
205
1974
1.385
0.601
10
196
1.346*
0.647
8
76
* These diversity values are probably slight underestimates because of small sample sizes. Species-
number curves for all other samples reached an asymptote indicating that those samples were adequate for
good diversity estimates (see Fleming et al, 1972)

RESOURCE PARTITIONING
Thirty-five species of bats were found to coexist on Barro Colorado
Island in 1973. Thirty-one species were captured in diversity samples
and four additional species were seen in flight or at roosts. Nocti1io
1 epor ? nus, N_. labial is, and Molossus moiossus restricted their flight
activities to habitats that were not sampled--the shallow inlets of the
lake (Nocti1io) and above the forest canopy (Molossus). The fourth
species not captured in the diversity samples, Vampyrum spectrum, is a
top carnivore and may be represented by very'few. individuals on the
island. A pair of V_. spectrum was netted by A. L. Gardner and D. E.
Wilson on 5 January 1973- 1 saw a single animal in June 1973 flying at
dawn. No other sightings of V_. spectrum were reported in 1973-
A first step at understanding how 35 species of bats coexist on
this small island can be made by dividing the fauna into feeding guilds.
Feeding guilds will be distinguished on the basis of two parameters--
general 'food type and method or place of food procurement. It will be
assumed that little or no competition for food resources occurs between
members of different feeding guilds, though they may compete for roost
ing space. The bats on Barro Colorado may be divided into nine feeding
guilds, each of which contains one to nine species.
Justification for the placement of species into specific feeding
guilds will be provided in succeeding sections. For the moment, the
feeding guilds are defined as follows:
(1) "Canopy frugivores" -- forage mostly on fruits that grow in
27

28
the trees of the canopy and subcanopy level of the forest, above 3 m from
the ground.
(2) !,Groundstory frugivores" -- forage mostly on fruits of shrubby
groundstory plants, 0 to 3 m above ground level.
(3) "Scavenging frugivores" feed mostly on over-ripe fruit.
(4) "Nectar-pol1en-fruit-insect omnivores" forage for pollen and
nectar from flowering trees when available in the dry season and then
switch to a fruit and insect diet in the wet season.
(5) "Sanguivores" -- feed only on the blood of mammals and birds.
(6) "Gleaning carnivores" -- forage for small animals (arthropods
or vertebrates) that are perching or moving on vegetation or on the
ground.
(7) "Slow-flying hawking insectivores" -- forage for flying insects
in small openings beneath or in the forest canopy or over streams.
(8) "Fast-flying hawking insectivores" -- forage for flying insects
above the forest canopy or in very large open spaces.
(9) "Piscivores" -- forage for fish or aquatic invertebrates at or
just above the surface of lakes and large streams.
The distribution of mean body weights for each bat species on
Barro Colorado by guild is plotted in Figure 3- Three guilds contain
a single species, and i expect that each of these species is sufficiently
unique to preclude serious interspecific competition for food. The
species within the groundstory frugivore, canopy frugivore, and piscivore
guilds increase in body weight with a geometric progression factor of
about 1 ..3 to 1.8 (with one exception in the canopy frugivore guild).
We might expect that the species within each of these guilds exploit
very similar types of food, captured in very similar manners, and that

Figure 3. Mean body weights of bat species by feeding guilds.
(Dashed lines seperate members of different families that belong to the
same feeding guilds.) 1, Carol 1ia castanea, 2. C. perspeci 1 lata,
3. Vampyressa pus i 11 a 4, Chirodenna trinitatum, 5. Artibeus phaeotis,
6, Vampyrops he 11eri, 7. Chirodenna vi11 osurn, 8. Vampyrodes caraccioloi,
9. Artibeus j ama icensis, 10. A, l i turatus, 11. Centurio semiex, 12. Glosso-
phaga sor¡cia, 13. Phyl1ostomus discolor, 14, Phylioderma stenops,
15. Desmodus rotundus, 16. Micronycter i s mega 1otis, 17. M. brachyotis,
18, Mimon crenulatum, 19. Micronycteris hirsuta, 20. Trachops cirrhosus,
21. Tonatia sy 1 v i col a 22. T. b i dens 23. Phyl 1 ostomus hastatus 24. Varnpy-
rum spectrum, 25. Rhogeessa tumi da, 26. Myotis nigricans, 27. Saccopteryx
leptura, 28. Centronycteris maximi11?ani, 29. Saccopteryx b i i i neata,
30. Peropteryx kappleri, 31. Pteronotus suapurensis, 32. _P. parn 1 1 i i ,
33. Mol ossus mo lossus, 34. Nocti 1io labial is, 35. _N. 1eporinus


31
food resources are partitioned largely by particle size as predicted by
the theoretical reasonings of Hutchinson (1959), McNab (1971a and b) and Hay
(1973) These authors postulate that similar species may avoid competi
tion for food by differing in body weights by a factor of at least 1.3
(May, but McNab and Hutchinson used the figure 2.0), each species
specializing in food particles proportional to its body weight (and to
the linear dimensions of its food handling apparatus, e.g., tooth row
length, gape size, tongue length, etc.).
The gleaning carnivore and slow-flying hawking insectivore guilds
each contain some species that are very similar in size to other species
of their guilds. We might expect that such species feed on similar
sized food particles of very different taxa or of similar taxa from
different microhabitats.
The nectar-pol1en-fruit-insect omnivore guild contains species very
different in size; this may partly result from a recent extirpation of
Lonchophylla robusta, a species intermediate in size between Glossophaga
soricina and Phyllostomus discolor. The sexual dimorphism in body
weights of P_. discolor is another complicating factor.
Canopy Frugivore Guild
Body size
Eight species, all in the subfamily Stenoderminae of the Phyllosto-
matidae, constitute the canopy frugivore guild on Barro Colorado. These
eight species range from 8.1 to 69-3 g in mean body weight (Table 6).
There is a mean increment of 1.44 between the body weights of adjacently
sized animals among the seven species designated as fig feeding
specialists in Table 6. Artibeus phaeotis, a feeding generalist, and
Chi roderma trinitatum are nearly the same in size.

32
Table 6. Weights tn grams of canopy frugivore bats on Barro Colorado.
Species
Mean
(x)
Sample
s i ze
(S.D.)
Sample
s i ze
n
Wgt / Wgt* Remarks
1 g sm
V. pus ilia
8.1
0.6
22
--
Fig specialist
C. trinitatum
12.3
1 .2
7
1.53
very rare fig specialist
A. phaeotis
13.0
1.2
30

food genera list
V. helleri
16.2
2.2
8
1 -31
very rare fig specialist
C. vi 11osum
22.4
2.1
13
1.38
fig specia1ist
V. caraccioloi
36.0
2-3
27
1.61
fig specia1ist
A. jamaicensis
47-2
3-4
30
1.31
fig speca 1ist
A. 1ituratus
69-3
5.6
30
1.47
fig specia 1 ist

mean
ratio of wei<
ght increments.44
* Weight of 1
arger species divided
by weight of
sma11e r spec ies
in the pair compared.

33
Food selection
All eight canopy frugivore species feed primarily on fruits of
large canopy and subcanopy trees, in particular figs of the genus Ficus.
Over 60% of the annual diet (by frequency of occurrence in fecal matter)
of seven of these bat species consists of fig fruits (Table 7); these in
clude C_. tr i n i tatum, but not A_. phaeot is of the same weight. A_. phaeot i s
depends on figs for 30% of its diet. Five species of Ficus, all of which
are green colored at maturity, are eaten and dispersed by these steno-
dermines on Barro Colorado. Fig species that produce large fruits are
preferred by large bats, and fig species that produce small fruits are
preferred by Small bats.
Figs form the bulk of the diet of Artibeus jamaicensis throughout
most of the year. However, during the latter part of the wet season
and the very beginning of the dry season mature fig fruits are very
scarce (Morrison, 1975). At this time A_. jama i cens i s turns more heavily
to other fruits and pollen (Table 8). The relative importance of pollen
in the diet of A_. j ama i cens i s is grossly underestimated here because my
sampling schedule did not coincide with the two weeks in late December
and early January when figs were very scarce and flowers were very
abundant. Similar seasonal switches in diet also probably occur for
A_. 1 ? turatus and V_. caraccioloi but the data are weak. No conclusions
can be made from the scant data on the smaller species of canopy frugi-
vores with respect to seasonal switches in diet.
Unlike the fig specialists, A_. phaeotis eats a more even distribu
tion of many types of fruits (Tables 7 and 8) with no one species
strongly dominating the diet. Throughout the year figs are a minor
component of the diet, while other fruits are very important in certain

Table 7. Most important food genera and species for bats in the canopy frugivore guild.
Bat Species
Percent of diet from most
important genera of food plant*
Most important species
of plant food*
N
V. pus i 11 a
92% Ficus
F. yoponensis
13
C. trinitatum
60% Ficus
F. popenoaei
5
A. phaeotis
30% Ficus
Spondias radlkoferi
33
V. he 11e ri
67% Ficus
F. inspida
6
C. villosum
100% Ficus
F. popenoaei
6
V. caraccioloi
76% Ficus
F. inspida
17
A. jamaicensis
78% Ficus
F. i ns idida
185
A. 1 ituratus
65% Ficus
F. inspida
20
* By frequency of occurrence

35
Table 8. Bi-monthly samples of important food species in the diets
of Artibeus and Vampyrodes. Sampling periods begin at
mid-month.
Food Species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan
Artibeus
j ama icensis
Ficus spp.
18
25
25
35
21
17
Cecropia spp.
3
3
Spondias spp.
1
8
6
Quararibea
9
Pollen
1
Total feeding
samples*
20
30
32
39
35
37
Art ibeus
1 i turatus
Ficus spp.
2
4
2
1
4
Spondias spp.
1
1
1
Pollen
1
Total feeding
samples*
3
4
5
2
7
Artibeus
phaeotis
Ficus spp.
2
1
2
1
3
Cecropia spp.
1
5
Spondias spp.
8
Total feeding
samples*
5
6
9
1
11
Vampyrodes
ca race i o 1 oi
Ficus spp.
1
2
4
3
1
Pollen
2
Total feeding
samples*
3
3
4
3
2
'Includes genera of lesser importance not shown here.

36
months. Cecropia exima is an important food item from July to September,
as is Spondias radlkoferi in November to January.
Feeding niche breadths based on food species by frequency of occur
rence. in the diet are presented in Table 9. Large niche breadth values
represent food generalists and small values food specialists.
A_. phaeot i s stands alone at the generalist extreme of this index.
A_. J~ ama i cens i s has an intermediate position between the generalist and
the extreme specialists. The remaining six species are bunched as
extreme specialists. Hereafter, all members of this guild will be
referred to as "fig specialists" except for the feeding generalist,
/\. phaeotis.
Niche overlap in food species is compared in Table 10. The highest
values of overlap in canopy frugivores occur between species most similar
in size (diagonal left edge of Table 10). A. phaeotis overlaps little
with all the fig specialists, except for _V. helleri, which is similar
in size. The high values of overlap between many of the fig specialist
species indicate that some mechanism other than selection of food
species must be operable to reduce behavioral interference and/or inter
specific competition for food in this guild.
Several types of evidence strongly suggest that food is a limiting
factor for fruit bats on Barro Colorado, at least during some parts of
the year. The biomass of fruit and the number of species of fruiting
trees fluctuate quite drastically on a seasonal basis (see Phenology
section). During the late wet season fruit availability is low,and an
increased proportion of captured fruit bats have empty stomachs (83% in
Oct-Nov) as compared to times of fruit abundance (/1% in Har-Apr).

37
Table 9* Feeding niche breadths of canopy frugivores.
Bat Species
Number of genera of Number of species of Niche Breadth*
known food plants known food plants (loge
V_. pus ilia 2
trinitatum 3
A. phaeotis 10
_V. he Her 2
C_. vil losum 1
_V. caraccioloi b
j ania i cens i s 9
A. 1 i turatus 5
k
h
12
3
3
5
16
7
0.3b
1.33
2.10
1.01
1.01
1 .Ob
1.61
1.33
*Sample sizes for calculating niche breadths are as in Table 7-

38
Table 10.
Feeding niche overlaps (C/} ) among species of the
canopy frugivore guild
A. phaeotis
.215** .354* and
V. pus ilia
.968*
C. trinitatus
V. helleri
C. villosum
V. caraccioloi
A. jamaicensis
A. 1ituratus
.615**
.241**
. 465*
. 485**
.518**
.452
.796
.679
.272
.152
.893*
743
.644
.209
.412
.798*
.886
.852 '
.452
.727*
.200
.310
.99** .962
.983*
Denotes species most similar in body weight
Denotes overlap with the feeding generalist

39
Also by the late wet season several species of fruit bats have tempo
rarily moved out of the study area,and the remaining individuals and
species spend a greater part of their nightly time budgets in foraging
(see Species Diversity section). Even when fruit is very abundant in
terms of total biomass, it is concentrated in a limited amount of
space, the few trees fruiting at any moment, and may still be a limit
ing factor for population size.
Vert i cal stratification
Handley (1967) and Harrison (1962) demonstrated a vertical strati
fication of flight activity in Neotropical bat species, with most canopy
frugivores preferring upper levels of the forest. On Barro Colorado,
V_. pus ilia, A_. phaeot i s C_. vi 1 losum, V_. caracci ol i and A_. 1 i turatus
were captured with highly significant frequency in the nets and traps
set above 3 m (Table 11). V_. hel 1 er i and £. tr in i tatum al so were
captured most frequently in subcanopy-canopy levels, but sample sizes
for these species are smal1, and frequency differences are not statis
tically significant. A. j ama icensis is the only species of the guild to
show a significant preference for activity at the groundstory level,
yet h2% of the captures of even this species were in the upper levels
of the forest. Though most of its food items grow in the upper levels
of the forest, A. jamaicens ? s may fly close to the ground to avoid
predators. On the other hand this behavior- may be an artifact of the
human management of the forest, with this species opportunistically
finding it more efficient to fly along cleared trails than to repeat
edly detect and avoid vegetation at higher levels.

40
Table 11. Vertical stratification of canopy frugivore species on
Barro Colorado. Statistical significance indicates pref
erence for one of the two vertical strata.
Bat Species
No. of bats captured at No. of bats captured at
ground level, 0 to 3 mm subcanopy levels, 3 to 12 mm
V. pus ilia
5
25**
C. trinitatum
2
4
A. phaeotis
36
56*
V. hel1eri
3
6
C. vi 1 los urn
4
24**
V. caraccioloi
4
30**
A. jamaicensis
467**
326
A. 1ituratus
23
66**
* Significant by Chi Square Test (P_ <.05).
** Highly significant by Chi Square Test (P < .01).
Yates Correction for Continuity is used on all tests of samples
with N< 200 (Sokall and Rohlf,1969).

41
Habitat selection
Comparison of netting samples from the young open forest of Buena
Vista and the closed canopy forest and creek habitats of Barro Colorado
provide a measure of species preferences for three habitats (Fig. 4).
As a group the fig specialists are much more common in the closed forest
and creeks lined by closed forest than in the shrubby open forest where
few mature trees of their preferred food species are found. A_. phaeot i s
and A. ¡ama i cens i s are common to very abundant in all three habitats, as
would be expected from their more generalized food requirements. None
of the extreme fig specialists are common on Buena Vista Peninsula.
Feeding behavior
Canopy frugivores usually carry fruits by mouth from fruiting trees
to night feeding roosts (Goodwin and Greenhall, 1961; Morrison, 1975)-
On BCI Morrison found that the night feeding roosts of A_. jama i cens i s
are frequently several hundred meters away from the fruiting trees where
they .are picked. Only when feeding on the large fruits of Dipteryx
panamensis did Artibeus feed on fruiting trees. All four most common
canopy frugivore species were observed to carry whole or partially eaten
fruits in flight. These animals presumably were transporting food items
to a night feeding roost for consumption. Whether the less common
species in the guild use night feeding roosts is unknown.
The fruits carried in flight by fruit bats vary in weight from less
than 1 g to about 20 g. Most bats carry fruits that weigh 20 to kOZ of
their own body weight. Table 12 lists the range in weights of some
fruits eaten by stenodermine bats. There is considerable variation in
the weights among and within species for these fruits (even in fruits
from the same individual tree).

Figure 4. Relative abundance of bat species in three habitats. Numbers along
horizontal axes refer to species as assigned in Fig. 3.

60
50
40
30
20
10
0
30-i
40'
30-
20-
10
0
20 i
10-
0
5 1
15
13
SECOND GROWTH
9 321 18t32,12 10 22 36
CREEKS
10
3 20 13 19 4 7 23 16 32 6 11' 18 22*29 25 12
MATURE FOREST
32 2 10 5 13 8 7 17 1 3 19 21 26 29 1 20 18 4 22 30 23 28 15 12 11 14

44
Table 12. Wet weights in grams of some fruits eaten by bats on
Barro Colorado Island that were collected beneath
fruiting trees.
Plant Species
Range
Fruit Weights
Mean S. D.
N
Ficus inspida
7.1-11 .A
9.1
1.5
10
Ficus obtusifolia
14.2-19.0
17.0
2.5
3
Ficus yoponensis
1.5- 5.6
3.1
1.1
12
Anacardium excel sum
4.2- 6.2
5.1
0.7
7
*
Calophyllum longifolium
9.3-17.7
14.7
3-3
7
Dipteryx panamensis
18.0-26.3
22.3
3-6
5
Spondias radlkoferi
8.6-13-0
10.6
1.4
9
Quararibea asterolepis
4.9- 6.3
5-45
0.6
4
Astrocaryum standleyanum
17.0-20.5
18.8
1.8
4
Piper cordulatum
0.5- 2.0
1 .2
0.5
15

45
Food particle size plays an important role in the partitioning of
food resources among similar species in many types of animals (e.g.
Diamond, 1973; Brown and Lieberman, 1973) and may be particularly impor
tant for fruit bats because of the behavior of carrying fruits in flight
to feeding roosts. According to the theory of optimal foraging strategy
(Schoener, 1969)> each bat should attempt to maximize the amount of food
it harvests per unit of time and thus select the largest food particles
it can efficiently find and handle. The weight that a bat can carry in
flight without seriously impeding manuverabi 1ty probably sets the upper
limit on food particle size for these animals.
Figure 5 shows that there is a highly significant correlation (by
F distribution, P <.01) of fruit weight with bat weight for fruits
carried into nets by the three largest species of bats in the canopy
frugivore guild. Most of the points in this figure represent Ficus
inspida fruits, the most important food species in the diet of all
three bat species. Thus even though these three bats have high overlap
in food species (Table 10), they are able to specialize on food particle
sizes proportional to their body weights. The smaller canopy frugivore
species probably do the same thing, but no data are available.
Each species in the canopy frugivore guild has a distinct cycle of
flight activity. The three largest species, V_. caracci oloi /\. jama i -
cens ? s, and A. 1 i turatus, each have their greatest peaks in activity at
different times of the night (Fig. 6). Since all three of these species
feed largely in the same individual trees in the course of the night,
the offsetting cycles of activity probably function to minimize inter
specific aggression from crowding at the resource trees, especially
when resources are concentrated in a few trees per night. Reduced

Figure 5. Linear regression of fruit weight on bat body weight for fruits carried
into nets by _\/. ca race i o 1 o i A. |ama icensis, and /\. 1 i tu ra tus.

4=-

for
Figure 6. Frequency of capture through
three large canopy frugivore species.
the night as a measure of flight activity

25
20
15
10
5
0
Artibeus jamaicensis N
829
N = 33
V£>
HOURS AFTER SUNSET

50
crowding at resource trees presumably is of importance in permitting more
efficient feeding and in making these bats less obvious to the many kinds
of arboreal and aerial predators that eat bats (Humphrey and Bonaccorso,
1975).
A similar pattern of offsetting major activity peaks should be
expected in the small canopy frugivores, all of which feed heavily on
Ficus yoponensis and F_. popenoae i Figure 7 shows that V_. pus i 1 1 a is
most active in the first two hours after sunset, and C_. vi 1 losum is most
active later in the night. Paucity of data prevents comparison of the
other small fig specialists.
A. phaeotis, the feeding generalist, has a much more even distri
bution of activity through the night than any other species (Fig. 7).
Many of the fruits eaten by A_. phaeot i s are not eaten by other stenoder-
mine bats and it need not compromise its activity cycle to avoid crowded
resource trees.
Groundstory Frugivore Guild
Body size
Two species in the subfamily Carollinae of the Phy1lostomatidae
constitute the groundstory frugivore guild on Barro Colorado. They are
Carol 1 i a castanea and C_. persp i c i 1 1 ata These have mean body weights
of 12.A and 17-9 g, thus differing in body weight by a factor of l.^tA
(Table 13).
A few individuals of a third species of the genus Ca rol 1ia,
C. subrufa, were captured and banded by R. K. LaVal in 1972 on Barro
Colorado (pers. comm.). In 1973 and 197^ I recaptured some of LaVal's
banded C_. persp i c i 1 1 ata and _C_. castanea, but I have not encountered any
of the C_. subrufa he marked. It is difficult to distinguish

Figure 7-
for three sma!1
Frequency of capture through
canopy frugivore species.
the night as a measure of
f1ight act ivity

-"*

53
Table 13- Weights of groundstory frugivore bats on Barro Colorado
Bat species
Mean
(x)
Standard
deviation
Sample
s i ze
Weight of larger species
divided by weight of
smaller species in the
par compared
C. castanea
12 .b
1 .8
30

C. perspici11 ata
17-9
1 .8
30
1 M

5b
_C. perspici 1 lata and C_. subrufa by field cha racters, and it is poss i ble
that I lumped a few individuals of C_. subrufa with £. persp i c i 1 lata
because I was not aware that C_. subrufa was present on BCI. I believe
C_. subrufa is very rare on Barro Colorado, and lumping a few of them
with (^. perspici 1 lata would influence the data on this latter species
to a very minor extent.
Food selection
C. castanea and JC. persp i c i 1 1 ata are food generalists in that they
eat a fairly even distribution of a large number of kinds of fruits and
have large niche breadth values (Tables 14, 15, and 16). Though no one
food species dominates their diet in any one season or over a long
portion of the year, eleven species of the shrubby plant genus Piper
(Piperaceae) constitute the bulk of the diet of C_. castanea and nearly
*
one-third of the diet of C_. persp i c i 1 1 ata. Ten species of pipers were
identified in the fecal samples from C_. castanea and nine species from
C. perspici 11 ata. At least one species of piper is available with
mature fruit in every month of the year on Barro Colorado (see Table 2).
C. castanea eats pipers all year long, but no pipers were evident in the
diet of perspici 11 ata from mid-September through mid-November.
C_. persp i c i 1 1 ata appears to feed exclusively on subcanopy and canopy
fruits in the late wet season. Particularly important are Solanum
hayseii, Quararibea asterolepis and Cecropia exima. Other fruiting
trees are important food species along with pipers at other seasons.
Though fruiting shrubs dominate the diet of _C. castanea, fruiting trees
are somewhat more important than shrubs for C_. perspici i lata.
in addition to the fecal samples from captured animals, food habits
data for C_. persp i c i 1 1 ata were obtained by monitoring droppings below

55
Table \b. Food species in the diet of £. castanea as determined from
frequency of occurrence of seeds in fecal samples. Sampling periods
begin at mid-month.
Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total
Piper aequale 3
JP. cordul atum
_P. ret i cul atum 1
P_. ma rg i natum 3
P_. carri 1 loanum
Piper 109 1
Piper 11b
Piper 120
Piper 122
Pi pe r 150
Carludovica pa 1 mata
Solanum hayse i ?
Markea panamensis
Vismia 1
Brosimum bernadettae
Dipteryx panemensis 1
Aechmeia ti11andsoi des 1
Unknown 10A
Shrubs
3
8 1
3
1 1
1 1
1
1
3
2
T rees
1
2
9 1
2 1
3 6 15
9
1 5
1 6
2
2 b
1 1
1 2
3
2
1
2
1 1 1
3
Unknown
1
1
1
1
Unknown 123
1
1

56
Table 15. Food species in the diet of C_. perspici 1 1 ata as determined from
frequency of occurrence of seeds in fecal samples. Sampling periods begin
at mid-month.
Plant species
Jan-Mar
Ma r-l
May May-Jul
Ju1-Sep
Sep-Nov Nov-Jan Total
Shrubs
Piper aequa1e
1
1
P. cordulatum
10
1
1 1
P. reticulatum
7
7
P. marginatum
1
1
1
3
Piper 109
4
1
1 6
Piper 1 1
1
1
2
Piper 116
1
1
Piper 120
2
1 3
Piper 150
2
2
T rees
Carludovica palmata
1
1
Solanum hayseii
1
6
1
1 9
Markea panamensis
1
k
5
Vismia 1
k
5
9
Vismia 2
i
1
2
Cecropia exima
i
1
1 3
Brosimum bernadettae
3
3
Quararibea asterolepis
6 6
Dipteryx panamensis
7
1
8
Cassia undulata
3
3

57
Table 15, continued.
Plant species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan Total
Unknown 101 1 1
Unknown 103 1 1
Unknown 104 1 1
Unknown 125 44
Unknown 127 22
Insects
5
1
6

Tab 1e 16.
Feeding niche breadths of groundstory frugivores.
Bat species
Number
known
of genera of
food plants
Number of species of
known food plants
% of diet composed
of pipers
Niche breadth
(loge B)
Ca rol 1 i a
castanea
8
18
78 (N
= 60)
2.47
Ca rol 1 i a
perspici1 lata
10
24
27 (N
= 103)
2.63
Based on frequency of occurrence of each species in the diet from samples in Tables 14 and 15

59
two day roosts of this species. Both roosts were in hollow Anacard i urn
excel sum trees. With the exception of A_. exce 1 sum all common food items
identified from the day roost droppings appeared as important food items
in the fecal samples from captured bats during the same bimonthly
periods (Table 17).
Why did not A.. excel sum ever show up in the fecal material from
captured bats? Probably A_. excel sum is the only tree species that
commonly serves as both a day roost and an important food resource for
C_. persp i c i 1 1 ata These bats need only fly to the canopy of the roost
tree, pick a fruit, and carry it back inside the roost to eat it. The
bats would usually digest and excrete the fruit before flying away from
the roost to forage for other fruits; thus little chance would exist for
this pulp to show up in netted animals. The Carol 1ia colonies in
A_. excel sum trees consisted only of 6 to 8 bats and each colony probably
had access to more A_. excel sum fruits when in season than they could eat.
Anacardium excelsum is the only fruit 1 know to be eaten by bats
on Barro Colorado that is not dispersed. Not only are the fruits carried
within the hollow parent tree, but it is the single, large seed and not
the fruit' pulp that is eaten. However, a few seeds probably are dis
persed when dropped by mistake.
Overlap between the diets of the two Carol 1ia is moderate in terms
/S
of food species. A CA value of 0.584 is obtained from lumping the food
habits data from fecal samples from the entire year. Pood overlap was
very high in Hay-July sampling, CA = 0.798. This latter value, as well
as the annual value of overlap, would be considerably smaller if it were
possible to correct for Anacardiurn eaten in roost trees by C. perspici 1 -
lata. Even though roosts were not monitored, it is unlikely that

60
Table 17* Frequency of occurrence of food species in the diet of C_.
pe rspic i 11 ata as determined from fruit droppings and seeds below day
roosts. Sampling periods begin at mid-month.
Plant species Jan-Mar
Ha r-May
May-Jul
Ju1-Sep
Sep-Nov
Nov-Jar' Total
Anacardium excel sum 5
83
39
127
Piper cordulatum
39
35
9
83
P. reticulatum
'
6
6
Piper 109
6
6
Solanum hayseii
1
1
2
Vismia 1
2
2
A
Quararibea asterolepsis
5
15
20
Cassia undulata
5
1
6
Unknown 155
12
12
Unknown R-1
3
3
No data.

61
£. castanea eats much of this fruit, as it is larger than all other
important fruits in the diet of C_. castanea.
Habitat select ion
Of the three habitats sampled, the Carollinae were most common in
the second growth forest and least common in the mature forest, as are
their most important food plants. C_. castanea accounted for 21.7% of
all bats captured in the second growth forest, 2.7% of the bats in the
creeks, and 1.4% of the bats in the mature forest (Fig. 6).
£. perspici1 lata constituted 15-8%, 16.0%, and 5.4% of the bat individ
uals captured in those habitats. Whereas many species of pipers grew
abundantly in the sunlight of the open canopy second growth and along
the creeks (though less so along creeks), only one species, P_.
cordu1atum, was abundant in the shade of the mature forest.
Vertical stratification
C_. castanea and C_. perspi ci 11 ata were both captured more frequently
at ground level than at upper levels of the forest (C_. castanea = 20
ground level, 14 upper levels; C_. perspici 1 1 ata = 50 ground level,
34 upper levels), but the difference was not statistically significant.
Both species feed on plants of ground and canopy levels. Known ground-
story fruits make up 78.4% of the diet of C_. castanea and 38% of the
diet of £. perspi ci 1 lata. During seasons when C_. persp ic i 1 1 ata is
feeding mostly on canopy fruits, it also is captured more frequently
in high nets and traps.
Feed ing behavior
Carol 1 ia castanea and C_. perspici 1 lata both have been captured
carrying fruits in the mouth and presumably use night feeding roosts as
do canopy frugivores. Some fruits are carried back to the day roost

62
for consumption as already discussed. The use of day roosts as feeding
places by _C_. perspici 1 lata is mainly a phenomenon related to feeding on
one fruit, Anacardium excel sum, as is evident from the dominance of this
fruit below day roosts and the decrease of dropped fruits and seeds when
exce 1 sum is not in fruit (Table 18). It is likely that temporary
night feeding roosts are used by these bats to avoid making the day
roosts conspicuous to predators and to reduce flight distances between
foraging forays.
The flight activity of Carol 1ia through the night is presented in
Figure 8. Both species show major peaks of flight activity in the first
hour of darkness. This is much earlier than the start of most canopy
frugivores1 flight activity and is probably due to the groundstory
becoming dark about an hour before the canopy level of the forest.
Cycles of flight activity in groundstory frugivores are bimodal or tri-
mod a 1 as are those of canopy frugivores. Two or three such bouts of
diel feeding activity also have been observed in fruit bats by Brown
(1968) and LaVal (1970) and seem characteristic of bats that feed on
foodstuffs that are not efficiently assimilated.
Scavenging Frugivore Guild
Body size
Centurio senex (Stenoderminae, Phy1lostomatidae), the wrinkle-faced
bat, is the sole member of the scavenging frugivore guild. A lactating
female weighed 22 g and a pregnant female weighed 27 g. No other weights
are available from Barro Colorado for this species, nor are there any
useful data on vertical stratification or habitat selection.

Figure 8. Frequency of capture through the night as a measure of flight activity
for two groundstory frugivore species.


65
Food spec ies selection and feeding behavior
From several morphological features, particularly the small teeth
and narrow esophagus, Paradiso (1967) concluded that C_. senex probably
feeds on a "soft fruit or fluid diet". The small teeth, narrow esoph
agus, and lack of facial hair (like vultures) on this bat are suggestive
of its possibly feeding on over-ripe or decaying fruit. Hence I tenta
tively designate it a "scavenging frugivore". The amount of rotting
fruit on the forest floor is incredibly large on Barro Colorado and
potentially could provide an abundant food resource for such a bat.
Goodwin and Greenhall (1961) mentioned finding fruit pulp in stomachs
of £. 5enex from Trinidad. Of the individuals that I captured on Barro
Colorado one defecated an unidentifiable fruit pulp and the other carried
a fresh Spondias radlkoferi fruit in its mouth. At this time it can
neither be confirmed nor disproved that Cen tur io is a scavenging frugi
vore. Though it is very similar to Chiroderma villosum in body size
I have no doubt that this anatomically unusual bat is ecologically quite
different from any other frugivorous species on Barro Colorado with
respect to food habits.
Nectar-Pollen-Fruit-Insect Omnivore GuiId
Body size
The nectar-po11en-fruit-insect omnivore guild (hereafter referred
to as the omnivore guild) contains three species, all of the family
Phy1 lostomatidae -- Glossophaga soricina (Glossophaginae), Phy11ostomus
discolor (Phyllostominae), and Phy11oderma stenops (Phyllostominae).
The mean body weight for P_. d i sco lor on Barro Colorado is 4.36 times
larger than that of G_. sor i c i na (Table 1 8) j a larger difference than
is found between species adjacent in size in any other guild. The large

66
Hable 18.
Weights in grams of omnivore bats on Barro Colorado.
Bat species
Mean
(x)
Standa rd
Deviation
(S. D.)
Sample
s i ze
(N)
Wgt /
ig
G. soricina
9.8
1 .0
9
P. discolor
42.8
3.9
27
4.36
male P. discolor
44.6
3-6
17
female P. discolor
39.7
2.1
10

P. stenops
61.0

1
1 .42
* Weight of larger species divided by weight of smaller species in the pair
compared.

67
gap in body weight between G_. soricina and P_, discolor exists because
of the recent extirpation of a bat species belonging to this guild. As
recently as the early 1950's, Lonchophy11 a robusta (Glossophaginae),
was alive on Barro Colorado (Hall and Jackson, 1953)- This species eats
nectar, pollen, fruit, and insects (Howell and Burch, 19/4). _L- robusta
from Costa Rica weigh about 17 g,and if this species were still present
on Barro Colorado the ratios between body weights of the four omnivore
guild members would be 1.4, 2.6, 1.4. The large ratio between _L. robusta
and P_. di scolor actual ly would have been somewhat less than 2.6 because
of the sexual dimorphism in body weights of P_. discolor. The dimorphism
in body weights between male and female P_. d i scolor is very slight (Table
18) but significant (P_ <.05, Student's t-test) .
Food selection
Nectar and pollen are consumed by guild members almost exclusively
in the dry season, as large flowers suitable for bat use are in bloom
only then (see Phenology). The few data available suggest that during
the wet season fruit and insects become dietary staples (Table 19).
That insects were not present in the food samples from G_. soricina on
Barro Colorado is probably because of poor sample size and the fact that
this species moved out of the study area during the wet season. Nothing
beyond the observations of Jeanne (1970) of P_. stenops eating social
wasp larvae and my two observations of fruit eating is known about the
diet of this bat.
Phyllostomus discolor is neither an extreme specialist nor generalist
in terms of food species (niche breadth = 1 .65)- Several types of flowers
are visited for pollen and nectar in the dry season. And in addition to
insects, several types of fruits are eaten in the wet season. The

Table 19. Seasonal use of pollen and fruit by the omnivore guild on
Barro Colorado.
68
Food species
No. of dry season
samples
No. of wet season
samples
Pol 1en:
Och roma 1agopus
Pseudobombax septenatum
Unknown 202
Fruit:
Cecropi a exima
Unknown \2k
Insects :
Pollen:
Och roma 1agopus
Unknown 201
Fruit:
Cecrop ia exima
Piper 109
Fruit:
Unknown 110
Unknown 151
P. discolor, N = 23
6
6
G. soricina, N = 6
3
1
P_. stenops, N = 2
1
2
3
3
1
1
1
1

69
available data are too limited to consider niche breadth values for
P_. stenops and G_. sor i ci na, or to calculate niche overlaps between
guild members.
Vert ica1 stratification
All of the flowers and fruits eaten by P_, discolor and 83% of those
eaten by G_. sor ic i na in this study area grow in the subcanopy and canopy
of the forest. Both species were captured most frequently in the upper
levels of the forest, 3 of 4 for G1ossophaga and 40 of 54 for Phy1losto-
mus. For P_. discolor preference for flying above groundstory shrubs is
highly significant (P_<.01, Chi Square Test).
Habitat select ion
Phyllostomus discolor was common in the mature forest and second
growth but uncommon over creeks. Some of the important tree species
producing flowers and fruits eaten by Phy1lostomus are common only in
second growth (e.g, Ochroma); others are common only in mature forest
(e.g. Pseudobombax); and still others are common in both habitats (e.g.,
Cecropia).
Feed ing behavior
During the dry season bats are frequently captured with pollen
heavily dusted over the anterior parts of the body. It is likely that
these animals visit a number of flowers in succession, consuming nectar
and performing pollination services at each flower, and then later
perch to ingest pollen by grooming it from the fur and skin.
None of the bats in this guild were captured carrying fruit in the
mouth,and it is not known whether they use night feeding roosts.
Sixty-nine percent of all P_. discolor captured in all-night samples
were taken within two hours of sunset. Such a strong unimodal pattern

70
of flight activity (Fig. 9) also is reported by LaVal (1970) and suggested
by Heithaus et_ aj_. (197*0 for this species in Costa Rica. My data are
insufficient for discussing the flight activity cycle of Glossophaga;
however, LaVal (1970) reports a strong peak in activity at dusk and in
the first hour of darkness just before the peak in P_. discolor activity.
Sanguivore Guild
Body s ? ze
Of the three extant vampire species, only Desmodus rotundus, the
common vampire, occurs on Barro Colorado Island and in the surrounding
vicinity. The pre-meal mean body weight of D_. rotundus is 33-5 g.
Food selection
Wild vampires feed only on the blood of homoiothermic vertebrates
(McNab, 1973). While vampire feeding behavior and prey selection is
well documented in agricultural areas where domestic livestock are the
chief food source (Turner, 1975), nothing is known of the prey species
of vampires in remote areas where only wild animals are potential hosts.
Vert i ca 1, stratification
Where domestic animals are the source of food, vampires fly almost
exclusively within 3 m of ground level (Bonaccorso, unpublished data).
It ¡s possible that vampires more commonly fly in the canopy level in
isolated forests where arboreal species (e.g., monkeys and birds) may be
important sources of blood meals for these bats. On Barro Colorado
island two vampires were captured in subcanopy nets and one in a ground
net.
Habitat selection
Vampires were clearly more abundant on Buena Vista Peninsula than on
Barro Colorado Island. Desmodus was the fourth most abundant species in

for
Figure 9. Frequency of capture through the night as a measure of flight activity
Phy]lostomus discolor.

~J u
45
40
35
30
25
20
15
10
5
0
ro
HOURS AFTER SUNSET

73
the Buena Vista samples (7-9% of the total captures), whereas on Barro
Colorado Desmodus was one of the least commonly captured species (0.2%
of the total captures, and see Fig. 4). Horses, cattle, pigs, and fowl
of the scattered farms in the Buena Vista-Frijoles area provide a
dependable and abundant food source that "los vampiros" constantly para
sitize (Fulo Sanchez, pers. comm.).
Gleaning Camivore Guild
Body size
The largest feeding guild within the bat fauna of Barro Colorado,
the gleaning carnivore guild, is formed by nine species of phyllostomine
bats. This guild also presents the largest range in body size within
any of the BCI feeding guilds (Table 20)* Micronycteris megalotis, one
of the smallest bats on Barro Colorado, has a mean body weight of 6.3 g.,
while Vampyrum spectrum, the largest species on the island, weighs
about 120 g.
The increment in body weight between successively larger species is
more irregular within the gleaning carnivore guild than in any other
guild on the island (see Fig. 3)- Two species have mean body weights
of close 'to 15 g., and three species have mean body weights of 31 to
36 g. On the other hand all three species of the genus Micronycteris
differ from the next smaller species by a factor of 1.5-
Food species selection
Little precise information can be offered at this time concerning
the prey species eaten by members of this guild. Excepting Vampyrum
spectrum, guild members feed predominately on insects most of the year,
i have a large collection of fecal samples from these species but as
yet have found no one able to identify the minutely fragmented insect
exoskeletons that constitute these samples.

74'
Table 20. Weights in grams of gleaning carnivore bat species on
Barro Colorado.
Bat species
Mean
(39
Standard
Deviation
(S. D.)
Sample
s ? ze
(N)
Wgt, ,
ig
M. megalotis
6.3
0.6
6
--
M. brachyotis
9.7
1 .1
3
1.53
M. crenulatum
14.7
0.7
-12
1.52
M. hirsuta
15.2
1 .2
7
1 .03
T. cirrhosus
31 .0
oo
c<\
13
2.09
T. sylvicola
32.6
3-6
10
1.04
T. bidens
35.6
2.3
7
1 .09
P. hastatus
91 .2
4.0
7
2.56
V. spectrum
120.0
--
1
1.31
* Weight of larger species divided by weight of smaller species
in the pair compared.

75
On the basis of characteristics of echolocation, Novick (1971)
hypothesized that large-eared insect- and vertebrate-eating bats, such
as are found in the gleaning carnivore guild, are adapted to distinguish
and capture prey items resting on foliage. Ross (1967) and Wilson (1971b)
have shown in food habit studies that three such large-eared species,
Antrozous pa 11 idus, Macrotus waterhousii and Micronycteris hirsuta do
feed primarily on large insects that spend much of their time perching
on vegetation or on the ground. Gardner's (1975) review of the scattered
information on food habits of the bats in this guild further confirms
that food items such as lizards and large insects probably are gleaned
from fol¡age.
Micronycteris. Wilson (1971b) reported that large roaches, Orthop-
tera, and scarabeid beetles are the most important items in the diet of
M. hirsuta on Orchid Island, a small island adjacent to Barro Colorado.
During the dry season, fruit became an important component of the diet
of this species as indicated by droppings below the study roost. My
food samples show that M_. mega 1 ot i s and M_. brachyot i s also switch in
part to fruit diets in the dry season. M_. brachyot i s also eats nectar
and pollen. An individual captured in mid-December was thoroughly dusted
with the pollen of a balsa tree (Ochroma lagopus).
Tonatia. A very large male cicada (Fidicina mannifera) weighing
2.5 g was carried into a net in the mouth of a Tonatia bidens in July
of 1974. The prothorax of the cicada had been crushed by the bat's
teeth and the cicada was dead when removed from the net. Because this
event occurred in the mating season of the cicadas, amongst the loud
nocturnal chorusing of the males, it posed the question of how Tonatia
locates such insect prey. Do bats locate such prey items via echoioca
tion or sounds produced by the insects?

76
Two T_. bidens, one male and one female, were released in a large
outdoor flight cage, one at a time, on BCI. Both individuals were
immediately attracted to the sounds of calling male cicadas that I held
by forceps inside the cage. The cicadas were plucked from the forceps
by the flying bats and eaten with gusto at a perch. Female cicadas
held so that their wings could not move in the forceps were ignored by
these bats; however, when the wings were allowed to flap nosily, the
bats again were attracted to the cicadas and ate them. During later
experiments large nocturnal grasshoppers, katydids, beetles, and moths
(species not identified) placed on the inside cage screening were
"gleaned" from the screening and eaten by these bats. It is obvious
that Tonatia bidens was able to locate cicadas from sounds produced by
the cicadas, but whether other large foliage-clinging insects, many of
which produce ultrasound, were echolocated or detected from insect-
produced sounds remains an interesting question for future research.
Only insect fragments were found in the fecal samples of T_. b i dens
and T_. sy 1 vi col a from BCI.
Phy11ostomus. Insects and fruits were found in the fecal samples
of Phyl lo'stomus hastatus. It also has been reported by several authors
to eat birds and rodents (Gardner, 1975).
Vampyrum. Vampyrum spectrum, the false vampire bat, is the largest
New World bat. It appears to feed primarily on birds and small mammals,
though investigators report some fruit and insects in its diet (Gardner,
1975)- A hollow tree roost monitored by J. Bradbury (pers. comm.) in
Costa Rica had a steady flow of feathers from parrots, trogons, cuckoos,
anis, and many other birds appearing at its base. D. J. Howell and I
kept a Vampyrum alive in captivity for three weeks on a diet of small bats

t
77
and birds ranging in size to large doves (Howell and Burch, 1974). When
released in a large room with small fruit bats (10-20 g) the false
vampire would fly up behind its flying victim and slap it into its jaws
with a wingtip. One morning at sunrise on Barro Colorado, a false vam
pire circled about an Artibeus jamaicensis I was untangling from a net.
The Vampyrum was apparently attracted by the alarm calls of the fruit
bat and circled for over a minute before leaving.
Mimon. Fecal samples of Mimon crenulatum from BCI appear to contain
only insect chitin.
Trachops. Fecal samples of Trachops cirrhosus from BCI appear to
contain only insect chitin, but this species is reported to eat lizards
such as anoles and geckos that are gleaned from vegetation, as well as
some fruit (Gardner 1975; Howell and Burch, 1974).
Vert ica1 stratification
Mimon crenulatum and Tonati a sy1vicol a show a significant preference
for flight in the groundstory level of the forest,and the small samples
for Micronycteris brachyotis and Tonati a bidens are just barely below
significance levels for showing a preference for flight activity in the
subcanopy-canopy level (Table 21). Thus the two similarly sized species
of Tonatia appear to forage in separate vertical strata.
Should future research increase sample sizes on vertical stratifi
cation it would not surprise me if none of the three species of the
genus M?cronycters show a strong preference for one particular vertical
stratum. All three species are very different in body size and probably
specialize on mutually exclusive sizes of prey items.
Though the data are very limited, the two very large species in this
gui Id, Phy1lostomus hastatus and Vampyrum spectrum were captured or seen

78
Table 21. Vertical stratification of gleaning carnivore species on
Barro Colorado.
Bat species
No. of bats captured
at ground level,
1 to 3 mm
No. of bats captured
at subcanopy levels,
3 to 12 mm
Mi. mega 1 ot i s
M^. b rachyot s
M. h i rsuta
M. crenulatum
T_. ci rrhosus
T. syl vi col a
T. b i dens
P. hastatus
_V. spectrum +
* Significant by Chi Square Test (_P < .05) .
** Highly significant by Chi Square Test (P_ <.0l).
+ Based on two net captures in Costa Rica and one visual sighting on
on Barro Colorado
Yates Correction for Continuity is used on all Chi Square Tests (Sokall
and Roh1f, 1969).

79
I
flying only in the subcanopy-canopy levels of the forest. The ground-
story (0 to 3 m) on Barro Colorado has the most dense foliage cover of
any of the vertical strata of the BCI forest (E. Leigh, unpubl data).
P_. hastatus and V_. spectrum may be too large to maneuver well through
the thick groundstory vegetation.
Habitat selection
Several gleaning carnivore species prefer either creek or forest
habitats on Barro Colorado to the exclusion or near exclusion of the
other habitat. Micronycteris brachyotis and Tonati a sy1vico1 a are both
common species in the forest station samples but were totally absent from
creek samples (Fig. 6). Trachops cirrhosus represents b% of all individ
ual bats sampled at creek stations (8th most abundant species in creek
samples) but only 0.5% of the individuals sampled at forest stations
(17th most abundant species in forest stations). All other species in
the guild are approximately equally abundant in creek and forest samples.
Comparisons with Buena Vista second growth samples are not made because
most species in this guild were under-represented at Buena Vista from lack
of harp-trapping.
So far I show that most bat species within a given feeding guild
partition food resources on the basis of food particle size. However,
some of the gleaning carnivores seem to use additional mechanisms to
partition food resources between similarly sized species.
The existing data make it appear that a spatial mechanism, special
ization in foraging microhabitat, permits Trachops cirrhosus, Tonatia
sylvicola, and Tonatia bidens, all similar sized gleaning carnivores,
to partition food resources within the same macrohabitat. i suggest
that T. cirrhosus specializes on prey items it can glean from low

80
foliage along creeks, that T\ sylvicola specializes on prey items it can
glean from groundstory foliage in the forest, and that T_. bi dens special
izes on prey items it can glean from trees in the forest and along creeks
or from the ground. Future research likely will show that all three
species eat invertebrates and vertebrates weighing between 2 and 15 g,
including lizards, frogs, and large insects.
Feeding behavior
The gleaning carnivores eat rather large prey items relative to
their body weight. It probably is common for them to carry prey to a
feeding roost or day roost for consumption (Wilson, 1971b; Bradbury,
pers. comm.).
Data on activity cycles are too scant for meaningful analysis.
M_. brachyoti s, M_. crenu 1 atum, J_. sylvicola, and T. ci rrhosus appear to
have a major peak of activity in the first two hours after sunset.
Slow-flying Hawking Insectivore Guild
Eight species belonging to three families constitute the guild of
slow-flying hawking insectivores. Four species belong to the Embalonu-
ridae, two to the Vesperti 1 ionidae, and two to the Mormoopidae. An
additiona'l species, Thyroptera tricolor of the Thyropteridae, is known
in recent years only from a single 1973 sighting on BCI. T_. tricolor
perhaps should be included in this guild if a population still exists
on BCi, but the species is probably near extirpation on the island be
cause of plant succession that has resulted in the disappearance of
most large-leafed groundstory plants (e.g. Musa and Cal 1ithea) used as
roosts (Findley and Wilson, 197*0*

81
Body size
Mean body weights of the species in this guild range from 4.2 to
22.6 g (Table 22). Wing morphology and flight behavior (Bonaccorso,
unpubl. data) suggest that species within the same family are most
similar in foraging behavior. Thus, species are grouped in subguilds
by families. The two mormoopids differ in mean body weight by a factor
of 1.37 a figure that suggests these two species may divide food
resources solely on the basis of particle size. The two vesperti 1 ion ids,
on the other hand, are very similar in body size. Analysis of the rela
tionships among body weights of the four embalonurids is complicated by
small sample sizes and sexual dimorphism. The mean body weights of males
of the four species differ by a factor of 1.25 to 1.47.
Food selection
All species of this guild appear to feed on fairly small flying
insects. Prey items are eaten on the wing rather than carried to feed
ing roosts. Some embalonurids hover around tree foliage and probably
feed to some extent on insects attracted to host trees. One BC1 fecal
sample from Pteronotus parnellii examined by Terry Erwin contained leg
parts of a small beetle of the family Alicuidae. All other samples await
analysis.
Vertical stratification
Pteronotus parnellii almost exclusively restricts its flight to
within 3 m of the ground (Table 23) Myotis nigricans and S_. b i 1 i neata
apparently fly with nearly equal frequency in groundstory and subcanopy
levels of the forest. Peropteryx kappleri is probably a specialist on
insects of the subcanopy, as indicated by the capture of all four BCI
individuals in high nets and numerous visual observations made by the
author in Belize (unpubl. data).

82
Table 22. Weights in grams of slow-flying hawking insectivore bat
species on Barro Colorado.
Bat species
Mean Standard
) deviation
(S. D.)
Sample Wgt / Wgt*
size lg sm
(N)
Embalonuridae
S. 1eptura ** 4.2 -- 1
C. maxi mi 11iani **
5.2

2
1 -25
S. b i 1ineata males
7.7
0.56
1 1
1.47
S. bil ¡neata females
8.7
0.7
3

P. kappleri **
1 1.2

2
1.46
R. tmida
4.2
Vesperti1 ionidae
2
_ _
M. nigricans
4.4
0.67
1 1
1.05
P. suapurensis
16.5
Mormoopidae
1
_ _
P. parnel1 i
22.6
1.48
30
1 -37
* Weight of larger species divided by weight of smaller species in the
pair compa red.
** Males and females are probably dimorphic in body weight.

83
Table 23* Vertical stratification of slow-flying hawking insectivore species
on Barro Colorado
Bat species
No.of bats captured at No. of bats captured at
ground level, 1 to 3 ni subcanopy levels, 3 to 12 m
S. b11ineata
7 b
C. maximi11iani
2 0
P. kappleri
0 b
R. tmida
1 0
M. nigricans
3 3
P. parnel 1 i i
7 b** 1
** Highly significant by Chi Square Test (P_<.01) with Yates
Correction for Continuity (Sokall and Rohlf, 1369).

84
Habitat selection
_P. parnel1 ii is the second most abundant species in the forest
station samples but is very rare in the creeks (Fig. 4). The only
specimen of JP. suapurensis was captured in the forest.
Myotis nigricans was captured only at forest stations, whereas
Rhogeesa tmida was captured only at or near creeks. These two
similar-sized species may differ in habitat requirements.
Visual observations of Saccopteryx bi1ineata were possible because
this species is crepuscular. Individuals repeatedly fly in circles around
feeding territories in small clearings of the forest (e.g..treefa11s) or
over creeks (J. Bradbury, pers. comm.). i have frequently watched territory
holders chase intruding conspecifics out of their territories emitting high
pitched audible sounds as they fly.
Flight behavior
Pteronotus parn 11 i i is one of the most commonly seen species on
Barro Colorado, as it flies low along forest trails. Ultrasonic pulses
picked up by a bat detector indicate that _P. parnel1 ii feeds as it flys back
and forth in long loops along the forest trails and groundstory vegetation.
The flight activity of _P. parnel1 i i through the course of the night is
bimodal with a major peak of activity occurring one to four hours after sun
set and a minor peak occurring eight to ten hours after sunset (Fig. 10).
Data on activity cycles of other species are limited, but _P. parnel1 ii
appears to be the only species in the slow-flying hawking guild that has no
strong peak of activity the first hour after sunset. Based on netting,
visual observations, and ultrasonic detection, the emba11onurids are active
from an hour before sunset to an hour after sunset and again at a similar
period about sunrise.

Figure 10. Frequency of capture through the night as a measure of flight activity
for Pteronotus parn!1 ii.

40
35
30
25
20
15
10
5
0

REPRODUCTION
Three patterns of reproduction occur in Neotropical bats: seasonal
monestry, seasonal polyestry, and year-round polyestry (Fleming, 1973).
Present information indicates that a single young is born per litter
except in the genus Rhogeessa in which the usual litter size is two
(Humphrey and Bonaccorso, 1975)-
Canopy Frug1vore Guild
Canopy frugivores are seasonally polyestrous, with one birth peak
at the end of the dry-to-wet transition and a second about the middle
of the wet season (Figs. 11-13 and Table 25; Wilson, 1975). The first
birth peak for all species coincides with the beginning of the first
predictably steady rains of the year in late April and Hay, a time of
fruit abundance. Large species such as A_. jamaicensis and A. 1 ituratus
are pregnant (as detectable by palpation) by the first week of January.
Sma 1 1 species 1 ike A_. phaeotus are not in a similar stage of pregnancy
until late January. Lactation then proceeds for one or two months during
a period of food abundance. There is a postpartum estrous,and females
are well advanced in the second pregnancy of the year while lactation is
still underway (Fleming, 1971)-
The second birth and lactation peaks are less synchronized among
species because of differences in gestation and lactation periods; the
same is true to a lesser degree within species because of individual
variation. For example, the second peak of lactation occurs in July-
September for A_. j ama i cens i s and A_. phaeot i s but not until Septembei
87

Figure 11. Reproductive timing in female Artibeus 1ituratus.

Arfibeus lifuratus
OD

Figure 12.
Reproductive timing
in female Art ibeus jama ? censis.

[:::[ Nylliparous 99
99 that h ave given birth
80-
60-
40-
20-
0-
few data
on
UJ
<
UJ
ro
a
<
u_
O
H-
Z
UJ
U
Q£
UJ
Q.
90
80-
70-
60-
50
40
30-
20-
10-
Pregnanf
Lactating
l-rssj .
Nonreproducing
-t .'
J-M
N-58
M-M
92
M-J
53

Figure 13.
Reproductive timing
in female Art ibeus phaeotis.
' (
|
: i

PERCENT OF ADULT FEMALES
Arfibeus phaeotis
J-S
15
S-N
N-D
19
CD
Co

Table 24. Reproductive timing in female bats on Barro Colorado. Within each bimonthly period the numbers
represent the number of females pregnant, lactating, and nonreproduct ive, in that order. Data for the
common species presented in accompanying figures are not presented here. Data are from this study and from
the bats captured in Panama by Fleming et al., 1972.
Bat species
Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan
C_. castanea
V_. pus ilia
£. trinitatum
_V. hel 1 eri
C_. vi 1 1 osum
V_. caraccioloi
C_. senex
P_. discolor
D. rotundus
* rnegalotal i s
M. brachyotis
J4. crenu 1 atum
M. hirsuta
3 0 8 7 13
2 1 0 5 7 2
2 0 0 0 0 1
2 0 0 111
300 3 10 0
2 0 0 111
1 0 0
1 1 2 0 2 5
0 1 1
1 0 2 3 2 1
10 0 111
10 4 5 0 0
0 0 1 0 0 1
4 0 4 0
2 3 1 8 0 5
3 1 2
10 1 0 10
4 0 0 10 1
0 2 2
0 0 1 0 13
10 0 2 0 0
10 1 0 0 1
0 3 1 0 14
0 0 1 0 0 1
10 0 0 1
0 13 0 0 12
3 0 2
1 2 0
011 101
0 0 2 10 0
0 0 1 0 0 4
0 1 0
12 3 4 11
0 0 1
0 0 1
0 11 10 2
0 0 1 0 0 2
1 0
T. cirrhosus
0
0
0

Table 2k continued.
Bat species
Jan-Mar Mar-May May-Jul
T. sylvicola
T. bidens
P_. hastatus
C. maxmi 1 1 iani
S. bi 1ineata
P_. kappleri
R_. tumi da
M.* n igr i cans
P_. suapurensis
G. soricina
110 10 0 2 0 0
1 0 0
0 0 1 0 0 1
1 1 0
10 1 2 0 0
0 0 1
1 0 1
0 0 1 0 0 1
0 1 0
Jul-Sep
Sep-Nov
Nov-Jan
0 0 2
1 0 0
CD
cn

96
November for the larger A_. 1 i turatus.
All canopy frugivores are reproductively quiescent in the late wet
season. Females of small species appear inactive from October through
December. The two largest species of the guild appear reproductively
inactive from mid-October through December, at least by external signs,
but histological preparations (Fleming, 1971) indicate that A. j ama icensis
females are in the early stages of pregnancy with drastically slowed
embryonic growth occurring in these months. Whether other species also
pass through a period of delayed development at the end of the wet season
is not known. Nevertheless, the energetic budget channeled into repro
duction by each canopy frugivore species is markedly reduced during the
late wet season, a time of fruit scarcity.
During the March-May sampling, 2~¡% of the A. j ama i cens i s adult
females captured were null¡parous (Fig. 14), and nearly all of these
probably had been born in the first or second birth pulse of the previous
year' (8 to 12 months before). Through the next three sampling periods
the perc.entage of nulliparous females in the sampled population steadily
rose to 49% as recruitment occurred from the offspring of the year.
Between November and the following March the proportion of nulliparous
females declined, not from their having given birth, but presumably from
higher mortality and/or dispersal rates than are found in older females.
Such data from other species are too few to provide comparison.
Groundstory Frug?vore Guild
Groundstory frugivores follow a reproductive pattern similar to
canopy frugivores. There are two births per year per female, one in
the dry-to~-wet season transition and the other in mid-wet season (Fig. 14).

Figure 14. Reproductive timing in female Carol la perspec i 11 ata.

30-
fi:l] Nulliparous
_] ?? that have given birth
60-
40-
20-
0 -
few data
N = 40
to
UJ
<
5
UJ
UL.
rj
D
<
u.
o
I
z
UJ
U
c
UJ
Ol.
90 -
Pregnant
80 -
Ej Lactating
| '' Nonreproducing
70 -
60-
50-
40-
30 -
20 -
m
-.I
fe'-i
i; ;i|

O
10-
_ m

^
0-
Scl


J-M M-M
N = 12 42
uaroina perspicif iafa
few data
|-i;f few data
-
M-J
7
S-N
11
few data
CO
CO

99
That females have a postpartum estrous is indicated by simultaneous
pregnancy and lactation in March-May and recaptures of marked individ
uals. Females are reproductively inactive from mid-October through
December.
Scaveng ? ng Frugivore Guild
Though only two female Centurio were captured during the study,
one female pregnant in February and another lactating in November indi
cate that the wrinkle-faced bat is probably seasonally polyestrous like
other fruit bats.
Pollen-Nectar-Fruit-insect Omnivore Guild
The only reproductive data available from Barro Colorado are for
Phyllostomus discolor, which appears to follow the pattern of seasonal
polyestry explained for frugivorous guilds (Table 26).
Sanguivore Guild
Though only six adult female vampires were captured during the
study the appearance of pregnant females in June, July, and August and a
lactating female in January suggest that Desmodus rotundus is either
seasonally polyestrous or, as suggested by Wimsatt and Trapido (1952),
polyestrous year round.
G1 eaning Carn1vore Guild
The fragmentary data available for this guild suggest a bimodal
pattern of seasonal polestry for the genera Micronycteris, Trachops, and
Tonatia. The first birth pulse in these genera coincides with the begin
ning of the wet season (Table 26 and Wilson, 1975). A pregnant and lac
tating female Tonatia sylvicola captured in March provides the first
evidence that this species has two litters per year and a postpartum
estrous.

100
Mimon crenulatum has a monestrous reproductive cycle (Table 26).
The peak in pregnancies occurs in the dry-to-wet season transition with
lactations peaking in the early wet season. Mimon are reproductively
inactive from September through December.
Slowf ly i ng Hawk? ng I nsect i vore Guild
Female Pteronotus parnellii are monestrous (Fig. 15). Pregnancies
occur from late December through mid-April. Lactation proceeds from
mid-March through late October; however, most young bats are weaned by
mid-July. The percentage of females suckling young in the May-July
sampling indicates that at least 53% of the adult females succeed in
raising young to the latter stages of nursing. This latter figure is in
reality much larger because some females have already weaned young by
the end of this sampling period. Unfortunately juvenile P_. parnel 1 i i
cannot be distinguished from adults on the basis of pelage color as is
possible for many other species.
During the March-May sampling 16% of the captured females were
null¡parous adults,and these were probably all one-year-olds. However,
in the next sampling period 50% of the females captured were nulliparous,
indicating that young of the year were entering the flying population
(top graph in Fig. 15). In the July-September sample, 65% of the females
were nulliparous. The number of nulliparous females then declined to
47% by the next sampling period; associated with the fact that only 16%
of the females were nulliparous in March, this pattern suggests a high
mortality for females in the latter half of their first year. Such a
pattern has been found in temperate Myotis (Humphrey, 1975b).

Figure 15. Reproductive timing in female Pteronotus parnellii.

PERCENT OF ADULT FEMALES
80
60
40
20
0
j:;;j Nultiparous 99
?? that have given birth
few data j




few data
M-i
32
J-S
21
S-N
19
N-J
5

CONCLUSIONS
Though tropical forests are relatively stable terrestrial environ
ments, nearly all animal species must seasonally alter their foraging
and reproductive behavior in response to fluctuating environments whether
they be food generalists such as coatis (Kaufmann, 1962) and red-winged
blackbirds (Orians, 1973) or food specialists such as three-toed sloths
(Montgomery and Sunquist, 197^), anteaters (Lubin and Montgomery, unpubl.
data) and hummingbirds (Wolf, 1970; Snow and Snow, 1972). Several recent
papers have discussed how Central American bats respond to seasonal
changes by altering foraging and reproductive behavior (Mares and Wilson,
1971; Fleming et a 1., 1972; Heithaus e_t_ aj_.; 1975; Humphrey and
Bonaccorso, 1975). The present study shows that on Barro Colorado Island,
Panama, bat species diversity, as well as foraging and reproductive stra
tegies of individual bat species, all undergo marked seasonal variation
in the moist tropical forest.
Spec ies Diversity and Pheno1ogy
Maximal diversity in the bat community of Barro Colorado occurs from
March through July, the principal growing season. During this time rains
are frequent yet mild and many plants and insects, having passed through
reproductive inactivity in the dry season (except for flowering activity),
undergo rapid growth and reproduction. Deciduous trees flush new leaves
and mature fruits become abundant both in diversity and biomass. Most
of the large orders of insects including Coleptera, Lepidoptera, and
103

Hymenoptera explosively increase in numbers of individuals and biomass.
In general most of the food resources eaten by bats, with the exception
of flowers, are abundant during the March-July period and many species
of bats that move out of this forest habitat in the late wet season
return by March.
Minimal diversity within the bat community occurs in the late wet
season. Fruit is scarce in both kinds of mature fruits and total biomass,
and fruit bat species diversity is lowest during this period. The species
diversity of insectivorous bat species also reaches a minimum during the
late wet season, and though the actual total numbers and biomass of in
sects are probably slightly lower in the dry season, the availability of
insects as food for bats is probably lowest in the late wet season, when
frequent heavy rains often curtail insect and bat activity.
Annual variation of physical and biotic factors in the tropical
forest also appears to affect the diversity of the bat community. Rain
fall may fluctuate drastically from year to year in absolute amount and
distribution through the year (Smythe, 197^). An extended wet season may
prevent or destroy flowers in a given year and a late dry season may hin
der or delay fruit production or insect reproduction. Furthermore some
species of plants do not reproduce every year (Foster, 1973; Frankie
et a 1., 1974). The diversity and abundance of bat spec ies were somewhat
different in magnitude each of the three years on Barro Colorado. The
causal factors that influence annual variation in the bat community are
unclear but probably involve predation, food supply, and competition.
At the ordinal level, the communities formed by tropical bats are
by far the most complex assemblages of sympatric mammalian species occur
ring anywhere in the world. Much simpler communities of bats are found

105
in temperate latitudes. For example, Panama supports 104 known species
of bats (Handley, 1967), whereas similarly sized South Carolina contains
only l*f species and the whole of the United States and Canada contains
only 29 species (Hall and Kelson, 1959)- Furthermore, 35 to 50 species of
bats are commonly found coexisting within an area of a few square miles in
Neotropical forests. Why are there so many more species of bats in tropi
cal regions than are found in temperate regions of similar size? What
mechanisms permit so many similar species to coexist in tropical forest
communities?
Orians (1969) concluded that tropical forests,support more bird
species than temperate forests because of two attributes unique to the
tropics. Firstly, many kinds of food items that are ephemeral in supply
in temperate latitudes are available year-round in tropical latitudes
*
(e.g. fruits and flowers). Secondly, the structure of the vegetation in
tropical forests is much more heterogenous than in temperate forests, thus
providing more foraging microhabits for specialization (e.g. bromeliads
and 1 i anas).
The great variety of year-round food items and habitat heterogeneity
in tropical forests go a long way toward explaining the abundant numbers
and kinds of bat species in the tropics. Forty-one species in Panama are
probably fully insectivorous and the other 63 species feed on fruit, pollen
and nectar, fish, vertebrates, blood, or some combination of the above.
All Nearctic bats north 32 N latitude are fully insectivorous in food
habits. Still there are three times as many insectivorous bats in Panama
as in South Carolina. Future research may explain this as being due to a
greater variety and size range in Panamanian insects and additional kinds

106
of microhabitats in which to capture insects. It is notable that at
least 10 species in Panama probably feed to some extent by gleaning
foliage whereas only one bat species in South Carolina does so. A number
of emba11onurids appear to feed much of the time on aerial insects that
are flying around foliage, flowers, or fruits. Several species feed
chiefly on insects found over water or on its surface (Hooper and Brown,
1968; Gardner, 1975).
Foraging and Reproduct ive Strategies
Canopy frugiyores
Resource partitioning in the canopy frugivore guild. Most fruits
preferred by bats have attributes of color, odor, taste, etc. that make
them unavailable to or not preferred by other kinds of fruit-eating
animals (Humphrey and Bonaccorso, 1975)- Hence, most of the competitive
interactions any bat species encounters over fruit resources, either in
ecological or recent evolutionary time, are with other species of bats
of its own feeding guild. The foraging strategies of fruit bats should
optimize the intake of energy with respect to the density, abundance,
spatial distribution, and particle sizes of available bat fruits. Addi
tionally,' temporal partitioning of the access to fruits may arise when
the resource is concentrated in a small space (e.g. one large fruit tree
with many fruits). Of course, fruits themselves do not have activity
cycles that limit a bat's access to them,and once a fruit is mature it is
available to any animal that would eat it.
Moist forest si tes throughout Central America usually contain eight
to ten species of canopy frugivores. Eight species of stenodermine bats
form the canopy frugivore guild on Barro Colorado. These bats feed almost

107
entirely on fruits growing in the forest canopy on trees, vines, and epi
phytes. Individuals of most of these plants occur at very low densities
and in patchy distributions within the forest. Most of the resource trees
are very large and produce enough fruit to feed hundreds of bats every
night during their fruiting periods of a week or so. Because a great
range in the size of preferred canopy fruits is available, it is possible
for many bat species to specialize in taking food particles of a particular
size class. Seven species on BCI are fig specialists that partition figs
primarily on the basis of size. The other species is a generalist with
regard to the types of fruit in its diet.
The fig specialists appear to have large home ranges (about 3 km4
for Artibeus jamaicensis) compared to other bats of similar size, and
they travel through much of the home range in the course of a night
searching for widely scattered resource plants (Heithaus et a 1. 1975;
Morrison, 1975; Bonaccorso, unpubl. data). Artibeus phaeotis, the fruit
generalist, appears to have a comparatively small home range for its size,
probably because it feeds on more kinds of fruits and thus is more likely
to encounter a suitable food resource in a smaller area than a fruit
specia 1ist.
The foraging strategy of canopy frugivores on Barro Colorado.
Frugivorous bats consume about their own weight in fruit per night
because they appear to have low assimilation efficiencies and do have
high metabolic rates (McNab, 1969). Each bat must make about a dozen
visits to one or a few resource trees per night. Each visit involves
picking a single fruit and carrying it away to a feeding roost where the
fruit is ingested. Once a tree with mature fruits is located an individ
ual bat may return to it repeatedly for over a week, but much time and

108
energy are spent scouting for trees that will be in fruit in future days
(Morr ison, 1975)-
For at least a couple of weeks during the beginning of the dry season
when fruits are scarce and bat pollinated flowers are very abundant, at
least three of the canopy frugivores switch partly to pollen and nectar
diets. In drier forest habitats where suitable flowers are available over
a longer dry season, stenodermine bats feed on nectar and pollen through
much of the dry season (Heithaus et_ aj_. 1975) -
The reproductive strategy of canopy frugivores on Barro Co 1 orado.
Adult females have two litters per year. Birth pulses are synchronized
within populations and coincide with the two predictable seasonal peaks in
fruit abundance. Late term pregnancy, lactation, and the learning
processes associated with foraging by young bats, the events of highest
energetic cost in the life cycle of these bats, occur at times of food
abundance. The proximal cues that provide the timing for reproductive
activities are not known but may involve rainfall or photoperiod.
Groundstory frugivores
Resource partitioning in the groundstory f rug ivore guiId. Ground-
story frugivores specialize on eating fruits that grow on shrubs, most of
which are less than 3 m in height. To a lesser extent these bats also
feed on canopy fruits, and in dry forest areas of Belize (Bonaccorso,
unpubl data) and Costa Rica (Heithaus et_ aj_., 1975) guild members also
feed on nectar and pollen in the long dry season.
Two species in the Carol linae, Carol lia castanea and C_. pe rsp i c i 1 1 ata,
form the groundstory frugivore guild on Barro Colorado. In any one place
in closed canopy forest habitat throughout the Neotropical region, this

109
guild contains fewer species than the canopy frugivore guild. In South
America the other genus in the subfamily Carollinae, Rhinophy11a, appears
to fit into the groundstory guild from information in Handley (1967) that
they are captured mostly in ground level nets. Some species of the
stenodermine genus Sturnira may also fit into the groundstory guild.
Far fewer shrub species than tree species produce bat-dispersed
fruits in tropical forests of Central America (12 versus 27 known species
on BCI; and see Heithaus et_ a_K 1975)- Also, shrubs produce a much
smaller range of fruit sizes than do trees. On Barro Colorado shrub
fruits preferred by bats range from about 0.2 to 2.0 g, a tenfold range;
whereas tree fruits preferred by bats range from about 2.0 to 30 g, a
fifteenfold range. Finally most shrub fruits are soft berries or catkins,
but tree fruits additionally may be drupes, monkeypods, and other forms.
Because of the greater variation in kinds, sizes, and shapes of canopy
fruits there are many more ways to specialize on canopy fruits than on
groundstory fruits, hence the larger numbers of species in the canopy
frugivore guild.
The foraging strategy of groundstory frugivores on Barro Co 1 orado.
Groundstory frugivores have small home ranges in comparison to large bats
that specialize on canopy fruits. This probably occurs because shrub food
species are abundant as individual plants and uniform in distribution
compared to tree species. It is probable that a large number of shrubs
must be visited each night by a groundstory frugivore in order for it to
find sufficient food. Each shrub has only a few small mature fruits
available per night (especially true of pipers) and a given shrub may be
stripped of fruits by other bats before an individual visits it or between

no
return trips from the feeding roost. When a suitable canopy species with
in the home range is in fruit it is included in the diet and offers a
source of fruit for several days. Fruits are picked from the resource
plant and carried to feeding roosts for eating. Most fruits eaten by
these bats are mature only from one to three months consecutively; thus
groundstory frugivores must frequently change food species and search
images. Some insects are eaten, but it is not clear whether these are
taken with fruits or are independently hunted.
The reproductive strategy of the groundstory frugivores on Barro
Colorado is essentially the same as that of canopy frugivores.
Pol 1en-Nectar-Frui t:-Insect pfnnivores
Resource partition ing in the pollen-nectar-fruit-insect omnivore
guild. Moist and wet tropical forests tend to have few kinds of large
flowers suitable for bats to pollinate and use as nectar and pollen food
resources, and these are available essentially only in the dry season
(late December through March on BCI). Extreme nectar-pollen specialists
among the Microchiroptera are common only in dry tropical forests and
deserts (Humphrey and Bonaccorso, 1975)- Only species like Phyi1 ostomus
discolor and Glossophaga soricina that switch to other types of food in
the wet season make prolonged use of dry season flowers in moist forest,
though some frugivores occasionally visit flowers.
The mechanisms of resource partitioning among nectarivorous bats
are poorly understood. My data and those of Heithaus et a 1. (1975) and
Alvarez and Gonzales (1970) indicate almost complete overlap among bat
species in use of flowering plant species. Flowers do have activity
cycles with respect to nectar product ion, and it is suggested from the

111
data of Heithaus et al. that temporal partitioning of floral resources is
an important means of partitioning flowers among bats. On Barro Colorado
the foraging activity of P_. discolor is compacted into the twilight and
first hours of darkness, probably as a response to inter- and intraspeci
fic competition over nectar. The first bats that arrive at a flower each
night receive a maximal supply of nectar and successive visitors receive
lesser amounts (Heithaus et_ a_ 1_. 1974).
The foraging strategy of pollen-nectar-fruit-insect omnivores on
Barro Colorado. Both G1ossophaga and Rhyllostomus appear to feed primar-
ily on nectar and pollen as long as flowers are available. As the wet
season begins, Rhyllostomus switches to fruit and insects, and Cecropia
fruits become particularly important. In dry forests where Cecropia is
not a common tree, Phy1lostomus disappears after the dry season flowering
and does not reappear until the next flowering season (Heithaus et al.,
1975; Bradbury, pers. comm.); I expect that they are migrating to and from
habitats that have Cecropia fruits available in the wet season and large
flowers .available in the dry season.
Glossophaga too switches to fruit in the wet season, and other authors
have found it also eating insects then (Fleming e_t_ aj 1972; Howel 1 and
Burch, 19/4) JG. soricina is a rare bat on BCI and becomes even rarer in
the wet season, indicating that it may undergo habitat shifts on a seasonal
basis.
The reproductive strategy of P_. discolor appears to be fairly similar
to that of the fruglvorous bats. Two birth pulses occur each year, the
first of which is toward the end of the peak in flowering and at the begin
ning of the peak in fruiting. It appears that females are eating fruit
and insects during both yearly periods of lactation.

112
Gleaning earn!vores
Resource partitioning in gleaning carnivores. Nearly all gleaning
carnivores depend on large insects as the primary food resource, though
a wide range of vertebrates, invertebrates, and even fruits supplement
the diet. This large feeding guild has a more complex array of parti
tioning mechanisms than any other guild on Barro Colorado, Differences
in body size, general food types, foraging microhabitats, and possibly
activity cycles operate to maintain the ecological distinctness among
these species. Future investigators should consider potential competi
tion between bats and other taxa that prey on large insects such as noc
turnal spiders, caprimulgid birds, and tree frogs.
The foraging st rategy of g 1 ean i ng earni vores o_n_ Barro Colorado.
Gleaning carnivores prey upon food items that are moderately large in
relation to their own body weight just as fruit bats do. Also like fruit
bats they carry individual prey items to feeding roosts whether the food
be large insects (Wilson, 1971b) or birds (Bradbury, pers. comm.). Because
of the high protein content of their diet these bats probably eat a
smaller weight of food in proportion to their body size and also fewer
prey items per night than do frugivores. Thus, gleaning carnivores spend
less time and energy transporting food items between foraging sites and
feeding roosts than do fruit bats. It would be interesting to compare
these guilds in terms of searching effort devoted to foraging, but such
data are not available for gleaning carnivores.
Late in the wet season and in the dry season large insects are rela
tively unavailable to these bats, and some gleaning species alternate
foraging patterns. Several of the smaller and medium sized species become

113
rare on the study site late in the wet season, but return and eat mixed
diets of fruit and insects through the dry season. M_. mega 1 ot i s and
ML brachyotis appear to use this strategy. Tonatia sylvicola, however,
remains in the BCI forest all year eating only insects. Janzen (1973)
and Janzen and Schoener (1969) report that watersheds are dry season
refugia for many insect groups. Perhaps some individuals or populations
of gleaning carnivores move to riverine habitats off the island during
lean times.
The reproduct ive strategy of g1eaning earnivores on Barro Colorado.
Micronycteris, Tonatia, and Trachops bear two litters per year. The first
pregnancy of the year occurs at a time of relative food scarcity, but the
birth pulse occurs as large insects are-becoming abundant. The first
lactation and the entire second reproductive cycle occur within months of
food abundance.
The peak in pregnancy for Mimon crenulatum, a monestrous species,
occurs about two months after those of the above gleaning carnivores.
Thus both pregnancy and lactation occur within the year's peak of insect
abundance. Mimon can time its reproductive activity in this manner
because it does not squeeze two reproductive cycles within the months of
large insect abundance as do the polyestrous species of the guild.
$ 1ow-flying hawk ing j nsectivores
P'esource parti t ion i ng i n the s low-f 1 y ing hawk i ng i nsect i vore guild.
Much less is understood about this guild than the others discussed so
far with respect to resource partitioning, foraging strategy, and repro
ductive strategy. It is possible that each family placed in this guild
should constitute a distinct guild, but we do not know enough to be certain.

114
A common denominator among ail these species is that they capture small
aerial insects and eat them while flying. All guild members probably
have individual or group feeding territories. Territorial defense of
foraging areas may serve as the primary means of decreasing intraspecific
interference over food. Body size, microhabitat, and activity cycle
differences appear to serve as the primary mechanisms that minimize inter
specific competition over food within the hawking insectivores.
The foraging strategy of s1ow-f1 ying hawk ing insectivores on Barro
Colorado. Small insects are abundant all year long though specific kinds
may fluctuate in abundance. These bats do not undergo major shifts in
diet as many other guilds are forced to do. Die! foraging activity
appears to occur in bimodal periods on a nocturnal or crepuscular regime.
Hundreds of very small food items must be eaten each night requiring
very high capture and feeding rates compared to other bat guilds (Gould,
1955). During foraging periods these bats appear to patrol the feeding
territory constantly searching for food items via echolocation.
The reproduct i ve strategies of slow-fly ing hawking insectivores.
_M. nigricans is seasonally polyestrous with reproductive inactivity during
the heavy rains late in the wet season (Wilson, 1971a). Perhaps this is
the only time when small insects are not abundantly available to Myotis.
The other members of the guild appear to be monestrous. For example,
most Pteronotus parnellii females are reproduct i ve 1y active only from
January through July, even though small insects are abundant all year
round. Precise data on food habits and the availability of food species
must be gathered before generalizations can be made on the reproductive
strategies of slow-flying hawking insectivores.

LITERATURE CITED
Alvarez, T, and L, Gonzales Quintero. 1970- Analis polnico del
contenide gstrico de murcilagos G1ossophaginae de Mexico.
An. Esc. Nac. Cine. Biol., Mex., 18:137-165.
Baker, J. R. and Z. Baker. 1936. The seasons in a tropical rain-forest
(New Hebrides).--Part 3- Fruit-bats (Pteropidae), J. Linn. Soc.
Lond., 40:123-141.
Beattie, A. J. 1971- A technique for the study of insect-borne pollen.
Pan-Pacific Entomol., 47:82.
Brown, J. H, 1968, Activity patterns of some Neotropical bats. J.
Mamm., 49:754-757-
and J. Lieberman, 1973- Resource utilization and coexistance of
seed-eating desert rodents in sand dune habitats. Ecol., 54:788-797-
Crespo, R. F., S. B. Linhart, R. J. Burns, and G, C. Mitchell, 19/2,
Foraging behavior of the common vampire bat related to moonlight.
J. Mamm., 52:366-368.
Diamond, J, M. 1973- Distributional ecology of New Guinea birds. Science,
179:759-769-
Findley, J. S. and D, E, Wilson, 1974, Observations on the Neotropical
disk-winged bat, Thyroptera tricolor, Spix, J. Mamm,, 55:562-571-
Fleming, T. H, 1971- Artibeus jamaicensis: delayed embryonic development
in a Neotropical bat. Science, 171:402-404.
. 1973 The reproductive cycles of three species of oppossums and
other mammals in the Panama Canal Zone. J. Mamm., 54:439-455.
, E. T. Hooper, and D. E. Wilson. 1972. Three Central American
bat communities: structure, reproductive cycles, and movement
patterns. Ecol., 53:555-569-
Foster, R. B. 1973- Seasonality of fruit production and seed fall in a
tropical forest ecosystem in Panama. Ph.D. Diss., Duke Univ,,
Durham, N. C., 156 pp.
Frankie, G. W,, H. G. Baker, and P. A. Opler. 1974. Comparative
phenological studies of trees in Tropical Wet and Dry Forests in
the lowlands of Costa Rica. J. Ecol., 63:888-919-
115

116
Gardner, A, L. 1975. Feeding habits of New World leaf-nosed bats, _i_n
Biology of the New World Leaf-Nosed Bats (Baker, R. J. and J. K.
Jones, eds.). Texas Tech Press, Lubbock (in press).
Goodwin, G. G. and A. M, Greenhall. 1961. A review of the bats of
Trinidad and Tobago. Bull, Amer. Mus. Nat. Hist., 122:191-301,
Gould, E, 1955. The feeding efficiency of insectivorous bats. J.
Mamm,, 36:399-407.
Hall, E, R. and W. B Jackson. 1953. Seventeen species of bats recorded
from Barro Colorado island, Panama Canal Zone, Univ, of Kans. Publ.
Mus. Nat. Hist:,, 5:641-646.
Hall, E, R. and K. R, Kelson. 1959. The Mammals of North America. Ronald
Press Co,, New York, 756 pp.
Handley, C. 0,, Jr, 1966. Checklist of the mammals of Panama, j_n Ecto
parasites of Panama (Wenzel, R. L. and V, J, Tipton, eds,). Field
Mus. Nat. Hist., Chicago.
__ _. 1967. Bats of the canopy of an Amazonian forest. Atlas Simp,
Biota Amaznica, 5:211-215.
Harrison, J, L, 1962. The distribution of feeding habits among animals
in a tropical rain forest, J, Animal Ecol,, 31:53-63.
Heithaus, E. R., P. A. Opler, and H, G. Baker. 1974. Bat activity and
pollination of Bauh i nia pau1etia: plant-pollinator coevolution,
Ecol., 55:412-419.
Holdridge, L. R, 1967. Life Zone Ecology. Tropical Science Center,
San Jose, Costa Rica, 206 pp.
Hooper, E. T, and J, H, Brown. 1968, Foraging and breeding in two
sympatric species of Neotropical bats, genus Nocti 1 io. J. Mamm.,
49:310-312.
Howell, D. J. and D Burch, 1974. Food habits of some Costa Rican bats-
Rev. Biol. Trop., 21:281-294.
Humphrey, S. R. 1975a. Nusery roosts and community diversity of
Nearctic bats. J. Mamm., 56: (in press),
. 1975b. Population ecology of the little brown bat (Myotis
1ucifugus) in indiana and north-centra! Kentucky. Amer. Soc.
Mamm, Spec. Pub], (in press).
and F. J. Bonaccorso. Population and community ecology of phyllo-
stomatid bats, _i_n Biology of the New World Leaf-Nosed Bats (Baker,
R. J. and J, K. Jones, eds.). Texas Tech Press, Lubbock (in press).

117
Hutchinson, E. G, 1959. Homage to Santa Rosalia, or why are there so
many kinds of animals? Amer. Naturalist, 93:145~161.
Janzen, D. H. 1973. Sweep samples of tropical foliage insects: effects
of seasons, vegetation types, elevation, time of day, and insularity,
Ecol,, 54:687-708.
and T. W. Schoener. 1969. Differences in insect abundance and
diversity between wetter and drier sites during a tropical dry
season. Eco., 49:96-110.
Jeanne, R. L. 1970. Note on a bat (Phylloderma stenops) preying upon the
brood of a social wasp. J, Hamm., 51:624-625.
Kaufmann, J. H, 1962, Ecology and social behavior of the coati (Nasua
na rica) on Barro Colorado Island, Panama. Univ, Calif. Publ. Zool.,
60:95-222.
LaVal, R. K. 1970. Banding returns and activity periods of some Costa
Rican bats. Southwestern Naturalist,, 15:1-10.
Levins, R. 1968. Evolution in Changing Environments. Princeton Univ.
Press, Princeton, 120 pp.
Mares, M, A. and D. E, Wilson, 1971. Bat reproduction during the Costa
Rican dry season. BioScience, 21:471-4-77.
May, R, M. 1973. Stability and Complexity in Model Ecosystems (Ch. 6).
Princeton Univ. Press, Princeton, 355 pp.
McNab, B, K. 1969. The economics of temperature regulation in Neotropical
bats. Comp. Biochem, Physiol,, 31:227-268.
. 1971a. The structure of tropical bat faunas, Ecol., 52:352-358.
. 1971b. On the ecological significance of Bergmann's rule. Ecol,,
52:845-854,
. 1973. Energetics and distribution of vampires, J. Mamm,, 54:131-144.
Miguela, P, 1969. Bioenergetics of pregnancy and lactation in European
common vole. Acta Theriologica, 14:167-179.
Montgomery, G. G, and M. E. Sunquist. 1973. Impact of sloths on
Neotropical forest energy flow and nutrient cycling, _i_n Trends in
Tropical Ecology (Medina, E, and F, Gol ley, eds,), Ecological
Studies 4, Springer-Ver1ag, New York,
Morista, M. 1959. Measuring of interspecific association and similarity
between communities. Mem. Fac. Sci. Kyushu Univ. Ser. E. (Biology),
3:65-80.
Morrison, D. 1975. Foraging and mating strategies of the Jamaican fruit
bat, Artibeus jamaicensis. Ph.D. Diss., Cornell Univ., Ithaca, N, Y.

118
Mutere, F. A. 1970. The breeding biology of equatorial vertebrates:
reproduction in the insectivorous bat, Hipposideros caffer, living
at 0 27' N, Bijd. Dierk,, 40:56-58.
Novick, A, 1971. Echolocation in bats--soine aspects of pulse design,
Amer. Scientist, 59:198-209.
Orians, G, H. 1969- The number of bird species in some tropical forests.
Eco 1., 50:783-801.
, 1973. The red-winged blackbird in tropical marshes. Condor, 75:
28-42,
Paradiso, J, L, 1967. A review of the wrinkle-faced bats (Centurio
senex Gray), with a description of a new species. Mammalia,
31:595-604.
Ross, A. 1967. Ecological aspects of the food habits of insectivorous
bats. Proc. West. Found, Vert. Zool., 1:205-263.
Schoener, T, W. 1969. Optimal size and specialization in constant and
fluctuating envoronments: an energy-time approach, _i_n Diversity and
Stability in Ecological Systems. Brookhaven Symposia in Biology:
22:103-114.
Shannon, C, E, and V/, Weaver, 1949. The mathematical theory of communication.
Univ. Ill, Press, Urbana, 117 pp.
Sheldon, A. L, 1969. Equibility indices: dependence on the species count,
Ecol., 50:466-467.
Smythe, N. 1974. Terrestrial studies--Barro Colorado Island, in
Environmental Monitoring and Baseline Data (Rubinoff, R., ed,),
Smithsonian Institution, Washington, D.C., 465 pp.
Snow, D. W, 1965. A possible selective factor in the evolution of
fruiting seasons in tropical forest. Oikos, 15:274-281,
and B, W. Snow. 1972, Feeding niches of hummingbirds in a
Trinidad valley, J. Animal. Ecol., 41:471-485.
Sokall, R, R, and F. G. Rohlf, 1969. Biometry. H. V/, Freeman and Co.,
San Francisco, 776 pp.
Studier, E, H., V, L, Lysengen, and M, J, O'Farrell, 1973. Biology of
Myotis thysanodes and M. 1uc i fugus (Chiroptera: Vesperti 1ion idae)--!I.
Bioenergetics of pregnancy and lactation. Comp. Biochem. Physiol.,
44:467-471.
Turner, D. C.
160 pp.
1975.
The
vampire
bat.
Johns Hopkins Press, Baltimore,
Tuttle, M. D.
1974,
An
improved
trap
for bats, J. Mamm., 55:475-477-

119
Wilson, D. E. 19/1a. Ecology of Myotis nigricans (Mammalia: Chiroptera)
on Barro Colorado Island, Pamama Canal Zone. J. Zool. Lond., 163:1-13.
, 1971b. Food habits of Micronycteris hirsuta (Chiroptera: Phyllo-
stomatidae). Mamm., 35:107-110.
. 1975- Reproductive strategies, _i_n Biology of the New World
Leaf-Nosed Bats (Baker, R, J. and J. K, Jones, eds.). Texas Tech
Press, Lubbock, (in press).
Wimsatt, W, A, and H, Trapido. 1952, Reproduction and the female
reproductive cycle in the tropical American vampire bat, Desmodus
rotundus murinus. Amer. J, Anat., 91 :415-446,
Wolf, L, L. 1970. The impact of seasonal flowering on the biology of
some tropical hummingbirds. Condor, 72:1-14.
Zaret, T, M, and A, S. Rand, 1971. Competition in tropical stream fishes:
support for the competitive exclusion principle. Ecol., 52:336-342,

Appendix 1. Seasonal
Bat species
variation in
Dry
captures of each bat
Dry-Wet Early-
Transit ion Wet
species or
Season
M i d-
Wet
i Barro Colorado Island in 1973
Late- Wet-Dry
Wet Transition Total
C. castanea *
12
4
9
8
1
13
47
C perspici11 a ta
19
62
11
8
17
7
124
V. p u s 1 1 a *
8
22
9
5
44
C tr initatum
1
4
2
1
2
10
A. phaeotis *
39
25
23
21
8
23
139
V.- heller i
2
1
7
2
1
1
14
C. vi11osum *
9
11
4
1
3
31
V. caraccioloi
3
8
2
17
5
2
37
A. ¡amaicensis
123
201
123
131
189
81
848
A. 1ituratus *
22
5
15
5
25
16
88
C. senex
1
2
3
G. sor¡cia *
1
2
1
1
5
P. discolor
8
14
6
13
8
10
59
P. stenops
*1
\
-
1
D. rotundus
1
1
1
3
M. meqalotis *
3
3
1
1
1
1
10
120

Appendix 1 continued.
Bat species
Dry
Dry-Wet
T ransition
Early-
Wet
M i d-
Wet
Late-
Wet
Wet-Dry
T ransition
Total
M. brachyotis *
4
8
5
1
2
3
23
M. crenulatum *
5
7
4
6
1
2
25
M. hirsuta
3
2
1
1
7
T. cirrhosus *
10
1
4
2
1
18
T. sylvicola
3
6
4
1
3
1
18
T. bidens *
2
2
3
1
1
9
P. hastatus *
1
3
2
6
R. tmida
1
1
2
M. nigricans
2
4
1
1
4
2
14
S. ieptura
1
1
C. maximi11iani
2
1
1
4
S. bi 1ineata *
2
5
2
1
10
P. kappleri
1
2
2
5
P. suapurensis
1
1
P. parn 1 1 i i
22
64
47
32
33
9
207
* Denotes species
that were
common n
the dry
season, but
rare or
absent in the
m i d-wet
and/or late-wet season (see page 20).

BIOGRAPHICAL SKETCH
Frank Joseph Bonaccorso was born 23 October 19^-8 in San Fernando,
California. He received his Bachelor of Arts in zoology with Departmental
Highest Honors from the University of California, at Los Angeles, in
June 1970, In September 1970, he began work on the degree of Doctor
of Philosophy in the Zoology Department at the University of Florida.
In August 1975, he will begin teaching as Lecturer in the European
Division, University College of the University of Maryland.
Frank is a member of the American Society of Mamma legists and the
Association for the Study of Animal Behaviour, He was awarded the
Austin Medal by the Associates of the Florida State Museum in 1975
for scholarly achievement and research in field biology. He also has
distinguished himself in the art of film-making for his works ~~ The
Maroon Prune Kid (1973) and The Maroon Prune Kid Goes To Col 1ege (1975).
122

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,
A
John H, Kaufmann, Chairman
Professor of Zoology
ru''
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,
Stephen R. Humphrey, Co-Chairman
Assistant Curator in Mammalogy
and Assistant Professor of Zoolog
I certify that 1 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.
VWtZ
Thomas C, Emmel
Associate Professor of Zoology
1 certify that 1 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.
Dav i d H. Hirth
Assistant Professor of Forestry

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.
Brian K. McNab
^ Professor of Zoology
Thi5 dissertation was submitted to the Department of Zoology in the
College of Arts and Sciences and to the Graduate Council, and was accepted as
partial fulfillment of the requirements for the degree of Doctor of
Philosopny.
August, 1975
Dean, Graduate School



36
months. Cecropia exima is an important food item from July to September,
as is Spondias radlkoferi in November to January.
Feeding niche breadths based on food species by frequency of occur
rence. in the diet are presented in Table 9. Large niche breadth values
represent food generalists and small values food specialists.
A_. phaeot i s stands alone at the generalist extreme of this index.
A_. J~ ama i cens i s has an intermediate position between the generalist and
the extreme specialists. The remaining six species are bunched as
extreme specialists. Hereafter, all members of this guild will be
referred to as "fig specialists" except for the feeding generalist,
/\. phaeotis.
Niche overlap in food species is compared in Table 10. The highest
values of overlap in canopy frugivores occur between species most similar
in size (diagonal left edge of Table 10). A. phaeotis overlaps little
with all the fig specialists, except for _V. helleri, which is similar
in size. The high values of overlap between many of the fig specialist
species indicate that some mechanism other than selection of food
species must be operable to reduce behavioral interference and/or inter
specific competition for food in this guild.
Several types of evidence strongly suggest that food is a limiting
factor for fruit bats on Barro Colorado, at least during some parts of
the year. The biomass of fruit and the number of species of fruiting
trees fluctuate quite drastically on a seasonal basis (see Phenology
section). During the late wet season fruit availability is low,and an
increased proportion of captured fruit bats have empty stomachs (83% in
Oct-Nov) as compared to times of fruit abundance (/1% in Har-Apr).


53
Table 13- Weights of groundstory frugivore bats on Barro Colorado
Bat species
Mean
(x)
Standard
deviation
Sample
s i ze
Weight of larger species
divided by weight of
smaller species in the
par compared
C. castanea
12 .b
1 .8
30

C. perspici11 ata
17-9
1 .8
30
1 M


22
Is an aerial hawker. The foliage gleaners prey chiefly on large insects
such as cicadas, grasshoppers, and roaches (Wilson, 1371b; this study).
Smythe (197*0 has shown that large nocturnal insects (greater than 5 mm
in length) become quite scarce on this same study area beginning in the
middle of the wet season, whereas small insects (smaller than 5 mm in
length) are relatively constant in abundance through the year. It
appears that the foliage-gleaning bats find food resources in the study
area sufficiently depressed in the latter part of the wet season that
they move out of the area. On the other hand, small insects remain an
abundant food resource; and aerial feeding bats remain in the
mature forest of Barro Colorado all year. Peropteryx kappleri, an
aerial feeding bat, is an exception as it does move out of forest habitat
in the late wet season.
Of the two bat species that are primarily nectarivorous in this
community, Glossophaga soricina switches from pollen and nectar to fruits
and insects in the early wet season and then moves out of the area in the
middle wet season, not to return until bat flow'ers appear in the dry
season. Phyllostomus discolor stays in the area the entire year, sub
sisting on fruits and insects during the wet season.
Among the fruit-eating species that seasonally move in and out of
the Barro Col orado mature forest is Vampyressa pusilla, the smallest
species of the 13 frugivorous bats on BCI V_. pus ilia is a feeding
specialist on small fig fruits. This bat left the study area when few
individuals of its most important food species, Ficus yoponensis, were
producing fruits in July-October and returned in November when mature
_F. yoponensis fruits were again abundant. While specific reasons why
other frugivorous species moved in and out of the study site are unclear,


23
their absence in September-November corresponds with the annual period
when few food plants are producing fruit (Table 2).
The abundance of individual bats on the study area, as measured by
the number of bats captured per sampling-hour, showed a pattern of
seasonal change markedly different from the diversity measures pattern.
Bats were captured in greatest numbers relative to sampling effort in
the dryto-wet transition, 0.425 bats/hr, and in the late wet season,
0.423 bats/hr (Table 3) The large numbers of bats captured in the dry-
to-wet transition sampling reflect large populations. Food resources
were abundant then; females of most species were in the latter stages of
lactation; and juveniles were entering the flying population and learn
ing to forage. These latter two activities are among the most energet
ically demanding in mammalian life cycles (Miguela, 1969; Studier et ai.
1973), and the timing of these costly activities seems geared to a period
of food abundance.
The late wet season peak in capture rate does not solely reflect
large numbers of individuals on the study area. Though a number of
species had at this time moved out of the young forest, some of the
remaining frugivorous species were recruiting juveniles into the flying
population from the second birth pulse of the year. Probably much of
the high capture rate is attributable to intense foraging activity
necessitated by low food supplies.
The diversity values for insectivorous and frugivorous species,
when computed separately, change similarly through the seasons (Table 4)
For both groups, species diversity is high from mid-November through
mid-July and low the remainder of the year. Fruit bat diversity rises
and falls in time as does the diversity of fruit (see Table 2). However


45
Food particle size plays an important role in the partitioning of
food resources among similar species in many types of animals (e.g.
Diamond, 1973; Brown and Lieberman, 1973) and may be particularly impor
tant for fruit bats because of the behavior of carrying fruits in flight
to feeding roosts. According to the theory of optimal foraging strategy
(Schoener, 1969)> each bat should attempt to maximize the amount of food
it harvests per unit of time and thus select the largest food particles
it can efficiently find and handle. The weight that a bat can carry in
flight without seriously impeding manuverabi 1ty probably sets the upper
limit on food particle size for these animals.
Figure 5 shows that there is a highly significant correlation (by
F distribution, P <.01) of fruit weight with bat weight for fruits
carried into nets by the three largest species of bats in the canopy
frugivore guild. Most of the points in this figure represent Ficus
inspida fruits, the most important food species in the diet of all
three bat species. Thus even though these three bats have high overlap
in food species (Table 10), they are able to specialize on food particle
sizes proportional to their body weights. The smaller canopy frugivore
species probably do the same thing, but no data are available.
Each species in the canopy frugivore guild has a distinct cycle of
flight activity. The three largest species, V_. caracci oloi /\. jama i -
cens ? s, and A. 1 i turatus, each have their greatest peaks in activity at
different times of the night (Fig. 6). Since all three of these species
feed largely in the same individual trees in the course of the night,
the offsetting cycles of activity probably function to minimize inter
specific aggression from crowding at the resource trees, especially
when resources are concentrated in a few trees per night. Reduced


40
35
30
25
20
15
10
5
0


111
data of Heithaus et al. that temporal partitioning of floral resources is
an important means of partitioning flowers among bats. On Barro Colorado
the foraging activity of P_. discolor is compacted into the twilight and
first hours of darkness, probably as a response to inter- and intraspeci
fic competition over nectar. The first bats that arrive at a flower each
night receive a maximal supply of nectar and successive visitors receive
lesser amounts (Heithaus et_ a_ 1_. 1974).
The foraging strategy of pollen-nectar-fruit-insect omnivores on
Barro Colorado. Both G1ossophaga and Rhyllostomus appear to feed primar-
ily on nectar and pollen as long as flowers are available. As the wet
season begins, Rhyllostomus switches to fruit and insects, and Cecropia
fruits become particularly important. In dry forests where Cecropia is
not a common tree, Phy1lostomus disappears after the dry season flowering
and does not reappear until the next flowering season (Heithaus et al.,
1975; Bradbury, pers. comm.); I expect that they are migrating to and from
habitats that have Cecropia fruits available in the wet season and large
flowers .available in the dry season.
Glossophaga too switches to fruit in the wet season, and other authors
have found it also eating insects then (Fleming e_t_ aj 1972; Howel 1 and
Burch, 19/4) JG. soricina is a rare bat on BCI and becomes even rarer in
the wet season, indicating that it may undergo habitat shifts on a seasonal
basis.
The reproductive strategy of P_. discolor appears to be fairly similar
to that of the fruglvorous bats. Two birth pulses occur each year, the
first of which is toward the end of the peak in flowering and at the begin
ning of the peak in fruiting. It appears that females are eating fruit
and insects during both yearly periods of lactation.


74'
Table 20. Weights in grams of gleaning carnivore bat species on
Barro Colorado.
Bat species
Mean
(39
Standard
Deviation
(S. D.)
Sample
s ? ze
(N)
Wgt, ,
ig
M. megalotis
6.3
0.6
6
--
M. brachyotis
9.7
1 .1
3
1.53
M. crenulatum
14.7
0.7
-12
1.52
M. hirsuta
15.2
1 .2
7
1 .03
T. cirrhosus
31 .0
oo
c<\
13
2.09
T. sylvicola
32.6
3-6
10
1.04
T. bidens
35.6
2.3
7
1 .09
P. hastatus
91 .2
4.0
7
2.56
V. spectrum
120.0
--
1
1.31
* Weight of larger species divided by weight of smaller species
in the pair compared.


84
Habitat selection
_P. parnel1 ii is the second most abundant species in the forest
station samples but is very rare in the creeks (Fig. 4). The only
specimen of JP. suapurensis was captured in the forest.
Myotis nigricans was captured only at forest stations, whereas
Rhogeesa tmida was captured only at or near creeks. These two
similar-sized species may differ in habitat requirements.
Visual observations of Saccopteryx bi1ineata were possible because
this species is crepuscular. Individuals repeatedly fly in circles around
feeding territories in small clearings of the forest (e.g..treefa11s) or
over creeks (J. Bradbury, pers. comm.). i have frequently watched territory
holders chase intruding conspecifics out of their territories emitting high
pitched audible sounds as they fly.
Flight behavior
Pteronotus parn 11 i i is one of the most commonly seen species on
Barro Colorado, as it flies low along forest trails. Ultrasonic pulses
picked up by a bat detector indicate that _P. parnel1 ii feeds as it flys back
and forth in long loops along the forest trails and groundstory vegetation.
The flight activity of _P. parnel1 i i through the course of the night is
bimodal with a major peak of activity occurring one to four hours after sun
set and a minor peak occurring eight to ten hours after sunset (Fig. 10).
Data on activity cycles of other species are limited, but _P. parnel1 ii
appears to be the only species in the slow-flying hawking guild that has no
strong peak of activity the first hour after sunset. Based on netting,
visual observations, and ultrasonic detection, the emba11onurids are active
from an hour before sunset to an hour after sunset and again at a similar
period about sunrise.


Table 2 continued.
Plant species
Plant type Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Cecropia exima
T
C. obtusifolia
T ******
Anacardium excelsum
T
Solanum hayesii
T
Vismia sp-1
T
Vismia sp-2
T
Astrocaryum standleyanum
T ****** *****
Tetrathy1acium Johansen!
T
Poulsenia armata
T
Cassia undulatum
V
Markea panamensis
V
C1 usia odorata
V
Unknown 126 (Pass ifloraceae) V
Unknown 101 (Araceae)
E
Unknown 103 (Araceae)
E
Aechmea t i 11andsiodes
E
Carludovicia palmata
-p~
S
Havetiopsis 125
E


39
Also by the late wet season several species of fruit bats have tempo
rarily moved out of the study area,and the remaining individuals and
species spend a greater part of their nightly time budgets in foraging
(see Species Diversity section). Even when fruit is very abundant in
terms of total biomass, it is concentrated in a limited amount of
space, the few trees fruiting at any moment, and may still be a limit
ing factor for population size.
Vert i cal stratification
Handley (1967) and Harrison (1962) demonstrated a vertical strati
fication of flight activity in Neotropical bat species, with most canopy
frugivores preferring upper levels of the forest. On Barro Colorado,
V_. pus ilia, A_. phaeot i s C_. vi 1 losum, V_. caracci ol i and A_. 1 i turatus
were captured with highly significant frequency in the nets and traps
set above 3 m (Table 11). V_. hel 1 er i and £. tr in i tatum al so were
captured most frequently in subcanopy-canopy levels, but sample sizes
for these species are smal1, and frequency differences are not statis
tically significant. A. j ama icensis is the only species of the guild to
show a significant preference for activity at the groundstory level,
yet h2% of the captures of even this species were in the upper levels
of the forest. Though most of its food items grow in the upper levels
of the forest, A. jamaicens ? s may fly close to the ground to avoid
predators. On the other hand this behavior- may be an artifact of the
human management of the forest, with this species opportunistically
finding it more efficient to fly along cleared trails than to repeat
edly detect and avoid vegetation at higher levels.


59
two day roosts of this species. Both roosts were in hollow Anacard i urn
excel sum trees. With the exception of A_. exce 1 sum all common food items
identified from the day roost droppings appeared as important food items
in the fecal samples from captured bats during the same bimonthly
periods (Table 17).
Why did not A.. excel sum ever show up in the fecal material from
captured bats? Probably A_. excel sum is the only tree species that
commonly serves as both a day roost and an important food resource for
C_. persp i c i 1 1 ata These bats need only fly to the canopy of the roost
tree, pick a fruit, and carry it back inside the roost to eat it. The
bats would usually digest and excrete the fruit before flying away from
the roost to forage for other fruits; thus little chance would exist for
this pulp to show up in netted animals. The Carol 1ia colonies in
A_. excel sum trees consisted only of 6 to 8 bats and each colony probably
had access to more A_. excel sum fruits when in season than they could eat.
Anacardium excelsum is the only fruit 1 know to be eaten by bats
on Barro Colorado that is not dispersed. Not only are the fruits carried
within the hollow parent tree, but it is the single, large seed and not
the fruit' pulp that is eaten. However, a few seeds probably are dis
persed when dropped by mistake.
Overlap between the diets of the two Carol 1ia is moderate in terms
/S
of food species. A CA value of 0.584 is obtained from lumping the food
habits data from fecal samples from the entire year. Pood overlap was
very high in Hay-July sampling, CA = 0.798. This latter value, as well
as the annual value of overlap, would be considerably smaller if it were
possible to correct for Anacardiurn eaten in roost trees by C. perspici 1 -
lata. Even though roosts were not monitored, it is unlikely that




Table 3- Seasonal variation in species diversity, species number, equitab i 1ity, and sampling abundance of
31 bat species on Barro Colorado Island. Sampling periods begin at about the middle of each cal
endar month and are based on lunar cycles.
Seasons:
Dry
D ry-Wet
transition
Early-
V/e t
M i d-
We t
Late-
Wet
Wet-D ry
T ransition
Months:
Jan-Ma r
Ma r-May
May-Jul
Jul-Sep
Sep-Nov
Nov-Jan
Species .Diversity (Hf)
2.147
2.332
2.175
1 .824
1 -517
2.157
Equitab i 1 ity (E)
0.667
0.707
0.667
0.599
0.515
0.688
Species Number (SN)
25
27
26
21
19
22
Bats Captured/sampling-hr.
0.301
0.425
0.339
0.29S
0.423
0.367
Total Bats Sampled
304
470
291
256
307
185


insectivore bat diversity sharply rises four months before insect biomass
explosively increases (see Fig. 2). The latter anamoly may be due to
ineffective harp trap placement and particular under-representation of
the abundant species, Pteronotus parnellii, during the first months of
field work. This would cause the dry season diversity value to be higher
than it should be. Most species of fruit bats remain in the BC1 mature
forest habitat throughout the year. On the other hand, the species
number of insect-eating bats in the dry-to-wet transition is nearly
double that of the late wet season because of the movement of foliage-
gleaning species in and out of the forest.
A measure of annual variation is achieved by comparing the diver
sity of frugivorous species in June, July and August of 1971 1973 and
1974 (Table 5). In all three years there is a consistent trend toward
lower diversity as the wet season progresses. However, the magnitude
of the diversity values varies from year to year. This indicates that
some annually variable factor or complex of factors, possibly food
availability, predation, or reproductive success, influences fruit bat
species diversity. Insectivore diversity is not compared because harp
traps for effective sampling were available only in 1973-


96
November for the larger A_. 1 i turatus.
All canopy frugivores are reproductively quiescent in the late wet
season. Females of small species appear inactive from October through
December. The two largest species of the guild appear reproductively
inactive from mid-October through December, at least by external signs,
but histological preparations (Fleming, 1971) indicate that A. j ama icensis
females are in the early stages of pregnancy with drastically slowed
embryonic growth occurring in these months. Whether other species also
pass through a period of delayed development at the end of the wet season
is not known. Nevertheless, the energetic budget channeled into repro
duction by each canopy frugivore species is markedly reduced during the
late wet season, a time of fruit scarcity.
During the March-May sampling, 2~¡% of the A. j ama i cens i s adult
females captured were null¡parous (Fig. 14), and nearly all of these
probably had been born in the first or second birth pulse of the previous
year' (8 to 12 months before). Through the next three sampling periods
the perc.entage of nulliparous females in the sampled population steadily
rose to 49% as recruitment occurred from the offspring of the year.
Between November and the following March the proportion of nulliparous
females declined, not from their having given birth, but presumably from
higher mortality and/or dispersal rates than are found in older females.
Such data from other species are too few to provide comparison.
Groundstory Frug?vore Guild
Groundstory frugivores follow a reproductive pattern similar to
canopy frugivores. There are two births per year per female, one in
the dry-to~-wet season transition and the other in mid-wet season (Fig. 14).


Table 24. Reproductive timing in female bats on Barro Colorado. Within each bimonthly period the numbers
represent the number of females pregnant, lactating, and nonreproduct ive, in that order. Data for the
common species presented in accompanying figures are not presented here. Data are from this study and from
the bats captured in Panama by Fleming et al., 1972.
Bat species
Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan
C_. castanea
V_. pus ilia
£. trinitatum
_V. hel 1 eri
C_. vi 1 1 osum
V_. caraccioloi
C_. senex
P_. discolor
D. rotundus
* rnegalotal i s
M. brachyotis
J4. crenu 1 atum
M. hirsuta
3 0 8 7 13
2 1 0 5 7 2
2 0 0 0 0 1
2 0 0 111
300 3 10 0
2 0 0 111
1 0 0
1 1 2 0 2 5
0 1 1
1 0 2 3 2 1
10 0 111
10 4 5 0 0
0 0 1 0 0 1
4 0 4 0
2 3 1 8 0 5
3 1 2
10 1 0 10
4 0 0 10 1
0 2 2
0 0 1 0 13
10 0 2 0 0
10 1 0 0 1
0 3 1 0 14
0 0 1 0 0 1
10 0 0 1
0 13 0 0 12
3 0 2
1 2 0
011 101
0 0 2 10 0
0 0 1 0 0 4
0 1 0
12 3 4 11
0 0 1
0 0 1
0 11 10 2
0 0 1 0 0 2
1 0
T. cirrhosus
0
0
0


118
Mutere, F. A. 1970. The breeding biology of equatorial vertebrates:
reproduction in the insectivorous bat, Hipposideros caffer, living
at 0 27' N, Bijd. Dierk,, 40:56-58.
Novick, A, 1971. Echolocation in bats--soine aspects of pulse design,
Amer. Scientist, 59:198-209.
Orians, G, H. 1969- The number of bird species in some tropical forests.
Eco 1., 50:783-801.
, 1973. The red-winged blackbird in tropical marshes. Condor, 75:
28-42,
Paradiso, J, L, 1967. A review of the wrinkle-faced bats (Centurio
senex Gray), with a description of a new species. Mammalia,
31:595-604.
Ross, A. 1967. Ecological aspects of the food habits of insectivorous
bats. Proc. West. Found, Vert. Zool., 1:205-263.
Schoener, T, W. 1969. Optimal size and specialization in constant and
fluctuating envoronments: an energy-time approach, _i_n Diversity and
Stability in Ecological Systems. Brookhaven Symposia in Biology:
22:103-114.
Shannon, C, E, and V/, Weaver, 1949. The mathematical theory of communication.
Univ. Ill, Press, Urbana, 117 pp.
Sheldon, A. L, 1969. Equibility indices: dependence on the species count,
Ecol., 50:466-467.
Smythe, N. 1974. Terrestrial studies--Barro Colorado Island, in
Environmental Monitoring and Baseline Data (Rubinoff, R., ed,),
Smithsonian Institution, Washington, D.C., 465 pp.
Snow, D. W, 1965. A possible selective factor in the evolution of
fruiting seasons in tropical forest. Oikos, 15:274-281,
and B, W. Snow. 1972, Feeding niches of hummingbirds in a
Trinidad valley, J. Animal. Ecol., 41:471-485.
Sokall, R, R, and F. G. Rohlf, 1969. Biometry. H. V/, Freeman and Co.,
San Francisco, 776 pp.
Studier, E, H., V, L, Lysengen, and M, J, O'Farrell, 1973. Biology of
Myotis thysanodes and M. 1uc i fugus (Chiroptera: Vesperti 1ion idae)--!I.
Bioenergetics of pregnancy and lactation. Comp. Biochem. Physiol.,
44:467-471.
Turner, D. C.
160 pp.
1975.
The
vampire
bat.
Johns Hopkins Press, Baltimore,
Tuttle, M. D.
1974,
An
improved
trap
for bats, J. Mamm., 55:475-477-


no
return trips from the feeding roost. When a suitable canopy species with
in the home range is in fruit it is included in the diet and offers a
source of fruit for several days. Fruits are picked from the resource
plant and carried to feeding roosts for eating. Most fruits eaten by
these bats are mature only from one to three months consecutively; thus
groundstory frugivores must frequently change food species and search
images. Some insects are eaten, but it is not clear whether these are
taken with fruits or are independently hunted.
The reproductive strategy of the groundstory frugivores on Barro
Colorado is essentially the same as that of canopy frugivores.
Pol 1en-Nectar-Frui t:-Insect pfnnivores
Resource partition ing in the pollen-nectar-fruit-insect omnivore
guild. Moist and wet tropical forests tend to have few kinds of large
flowers suitable for bats to pollinate and use as nectar and pollen food
resources, and these are available essentially only in the dry season
(late December through March on BCI). Extreme nectar-pollen specialists
among the Microchiroptera are common only in dry tropical forests and
deserts (Humphrey and Bonaccorso, 1975)- Only species like Phyi1 ostomus
discolor and Glossophaga soricina that switch to other types of food in
the wet season make prolonged use of dry season flowers in moist forest,
though some frugivores occasionally visit flowers.
The mechanisms of resource partitioning among nectarivorous bats
are poorly understood. My data and those of Heithaus et a 1. (1975) and
Alvarez and Gonzales (1970) indicate almost complete overlap among bat
species in use of flowering plant species. Flowers do have activity
cycles with respect to nectar product ion, and it is suggested from the


Figure 1. Barro Colorado study area showing the 17 sampling stations.


105
in temperate latitudes. For example, Panama supports 104 known species
of bats (Handley, 1967), whereas similarly sized South Carolina contains
only l*f species and the whole of the United States and Canada contains
only 29 species (Hall and Kelson, 1959)- Furthermore, 35 to 50 species of
bats are commonly found coexisting within an area of a few square miles in
Neotropical forests. Why are there so many more species of bats in tropi
cal regions than are found in temperate regions of similar size? What
mechanisms permit so many similar species to coexist in tropical forest
communities?
Orians (1969) concluded that tropical forests,support more bird
species than temperate forests because of two attributes unique to the
tropics. Firstly, many kinds of food items that are ephemeral in supply
in temperate latitudes are available year-round in tropical latitudes
*
(e.g. fruits and flowers). Secondly, the structure of the vegetation in
tropical forests is much more heterogenous than in temperate forests, thus
providing more foraging microhabits for specialization (e.g. bromeliads
and 1 i anas).
The great variety of year-round food items and habitat heterogeneity
in tropical forests go a long way toward explaining the abundant numbers
and kinds of bat species in the tropics. Forty-one species in Panama are
probably fully insectivorous and the other 63 species feed on fruit, pollen
and nectar, fish, vertebrates, blood, or some combination of the above.
All Nearctic bats north 32 N latitude are fully insectivorous in food
habits. Still there are three times as many insectivorous bats in Panama
as in South Carolina. Future research may explain this as being due to a
greater variety and size range in Panamanian insects and additional kinds


66
Hable 18.
Weights in grams of omnivore bats on Barro Colorado.
Bat species
Mean
(x)
Standa rd
Deviation
(S. D.)
Sample
s i ze
(N)
Wgt /
ig
G. soricina
9.8
1 .0
9
P. discolor
42.8
3.9
27
4.36
male P. discolor
44.6
3-6
17
female P. discolor
39.7
2.1
10

P. stenops
61.0

1
1 .42
* Weight of larger species divided by weight of smaller species in the pair
compared.


35
Table 8. Bi-monthly samples of important food species in the diets
of Artibeus and Vampyrodes. Sampling periods begin at
mid-month.
Food Species Jan-Mar Mar-May May-Jul Jul-Sep Sep-Nov Nov-Jan
Artibeus
j ama icensis
Ficus spp.
18
25
25
35
21
17
Cecropia spp.
3
3
Spondias spp.
1
8
6
Quararibea
9
Pollen
1
Total feeding
samples*
20
30
32
39
35
37
Art ibeus
1 i turatus
Ficus spp.
2
4
2
1
4
Spondias spp.
1
1
1
Pollen
1
Total feeding
samples*
3
4
5
2
7
Artibeus
phaeotis
Ficus spp.
2
1
2
1
3
Cecropia spp.
1
5
Spondias spp.
8
Total feeding
samples*
5
6
9
1
11
Vampyrodes
ca race i o 1 oi
Ficus spp.
1
2
4
3
1
Pollen
2
Total feeding
samples*
3
3
4
3
2
'Includes genera of lesser importance not shown here.


114
A common denominator among ail these species is that they capture small
aerial insects and eat them while flying. All guild members probably
have individual or group feeding territories. Territorial defense of
foraging areas may serve as the primary means of decreasing intraspecific
interference over food. Body size, microhabitat, and activity cycle
differences appear to serve as the primary mechanisms that minimize inter
specific competition over food within the hawking insectivores.
The foraging strategy of s1ow-f1 ying hawk ing insectivores on Barro
Colorado. Small insects are abundant all year long though specific kinds
may fluctuate in abundance. These bats do not undergo major shifts in
diet as many other guilds are forced to do. Die! foraging activity
appears to occur in bimodal periods on a nocturnal or crepuscular regime.
Hundreds of very small food items must be eaten each night requiring
very high capture and feeding rates compared to other bat guilds (Gould,
1955). During foraging periods these bats appear to patrol the feeding
territory constantly searching for food items via echolocation.
The reproduct i ve strategies of slow-fly ing hawking insectivores.
_M. nigricans is seasonally polyestrous with reproductive inactivity during
the heavy rains late in the wet season (Wilson, 1971a). Perhaps this is
the only time when small insects are not abundantly available to Myotis.
The other members of the guild appear to be monestrous. For example,
most Pteronotus parnellii females are reproduct i ve 1y active only from
January through July, even though small insects are abundant all year
round. Precise data on food habits and the availability of food species
must be gathered before generalizations can be made on the reproductive
strategies of slow-flying hawking insectivores.


for
Figure 6. Frequency of capture through
three large canopy frugivore species.
the night as a measure of flight activity


PHENOLOGY OF FOOD RESOURCES
Most of the bat species on Barro Colorado depend largely on fruit,
flowers, or insects as food resources. Only a few species feed on the
flesh or blood of vertebrates or non-insect invertebrates. The abundance
and diversity of fruits, flower's, and insects in Central America, even
in moist and wet forests, strongly fluctuate on a seasonal time scale
(Foster, 1973; Smythe, 1974; Frankie et al., 1974).
Pollen and nectar on Barro Colorado are available to bats as reliable
food sources only in the dry season, and only four species of flowering
plants are known to be used by bats (Table 2). Two common species,
Ochroma 1agopus and Pseudobombax septenatum, flower from mid-December to
mid-March, While these two species are in bloom nectar and pollen are
very abundant. The other two pollen types used by bats remain unidenti
fied. One of these is known only from February-March sampling and the
other from August-September.
Fruits from 45 plant species were found to be eaten by bats on the
island (Table 2). Nineteen of these species were trees, 11 were shrubs,
four were vines, four were epiphytes, and seven are unknowns. Mature
fruits of the species eaten by bats are available all year. There are
times, however, when few fruits of only a few species are available.
During 1973 a maximum of 19 fruiting species was available from mid-
March to mid-April, and a minimum of 6 species was available in November-
December (Table 2), Two of the fruits available in November-December,
12


4=-


81
Body size
Mean body weights of the species in this guild range from 4.2 to
22.6 g (Table 22). Wing morphology and flight behavior (Bonaccorso,
unpubl. data) suggest that species within the same family are most
similar in foraging behavior. Thus, species are grouped in subguilds
by families. The two mormoopids differ in mean body weight by a factor
of 1.37 a figure that suggests these two species may divide food
resources solely on the basis of particle size. The two vesperti 1 ion ids,
on the other hand, are very similar in body size. Analysis of the rela
tionships among body weights of the four embalonurids is complicated by
small sample sizes and sexual dimorphism. The mean body weights of males
of the four species differ by a factor of 1.25 to 1.47.
Food selection
All species of this guild appear to feed on fairly small flying
insects. Prey items are eaten on the wing rather than carried to feed
ing roosts. Some embalonurids hover around tree foliage and probably
feed to some extent on insects attracted to host trees. One BC1 fecal
sample from Pteronotus parnellii examined by Terry Erwin contained leg
parts of a small beetle of the family Alicuidae. All other samples await
analysis.
Vertical stratification
Pteronotus parnellii almost exclusively restricts its flight to
within 3 m of the ground (Table 23) Myotis nigricans and S_. b i 1 i neata
apparently fly with nearly equal frequency in groundstory and subcanopy
levels of the forest. Peropteryx kappleri is probably a specialist on
insects of the subcanopy, as indicated by the capture of all four BCI
individuals in high nets and numerous visual observations made by the
author in Belize (unpubl. data).


106
of microhabitats in which to capture insects. It is notable that at
least 10 species in Panama probably feed to some extent by gleaning
foliage whereas only one bat species in South Carolina does so. A number
of emba11onurids appear to feed much of the time on aerial insects that
are flying around foliage, flowers, or fruits. Several species feed
chiefly on insects found over water or on its surface (Hooper and Brown,
1968; Gardner, 1975).
Foraging and Reproduct ive Strategies
Canopy frugiyores
Resource partitioning in the canopy frugivore guild. Most fruits
preferred by bats have attributes of color, odor, taste, etc. that make
them unavailable to or not preferred by other kinds of fruit-eating
animals (Humphrey and Bonaccorso, 1975)- Hence, most of the competitive
interactions any bat species encounters over fruit resources, either in
ecological or recent evolutionary time, are with other species of bats
of its own feeding guild. The foraging strategies of fruit bats should
optimize the intake of energy with respect to the density, abundance,
spatial distribution, and particle sizes of available bat fruits. Addi
tionally,' temporal partitioning of the access to fruits may arise when
the resource is concentrated in a small space (e.g. one large fruit tree
with many fruits). Of course, fruits themselves do not have activity
cycles that limit a bat's access to them,and once a fruit is mature it is
available to any animal that would eat it.
Moist forest si tes throughout Central America usually contain eight
to ten species of canopy frugivores. Eight species of stenodermine bats
form the canopy frugivore guild on Barro Colorado. These bats feed almost


75
On the basis of characteristics of echolocation, Novick (1971)
hypothesized that large-eared insect- and vertebrate-eating bats, such
as are found in the gleaning carnivore guild, are adapted to distinguish
and capture prey items resting on foliage. Ross (1967) and Wilson (1971b)
have shown in food habit studies that three such large-eared species,
Antrozous pa 11 idus, Macrotus waterhousii and Micronycteris hirsuta do
feed primarily on large insects that spend much of their time perching
on vegetation or on the ground. Gardner's (1975) review of the scattered
information on food habits of the bats in this guild further confirms
that food items such as lizards and large insects probably are gleaned
from fol¡age.
Micronycteris. Wilson (1971b) reported that large roaches, Orthop-
tera, and scarabeid beetles are the most important items in the diet of
M. hirsuta on Orchid Island, a small island adjacent to Barro Colorado.
During the dry season, fruit became an important component of the diet
of this species as indicated by droppings below the study roost. My
food samples show that M_. mega 1 ot i s and M_. brachyot i s also switch in
part to fruit diets in the dry season. M_. brachyot i s also eats nectar
and pollen. An individual captured in mid-December was thoroughly dusted
with the pollen of a balsa tree (Ochroma lagopus).
Tonatia. A very large male cicada (Fidicina mannifera) weighing
2.5 g was carried into a net in the mouth of a Tonatia bidens in July
of 1974. The prothorax of the cicada had been crushed by the bat's
teeth and the cicada was dead when removed from the net. Because this
event occurred in the mating season of the cicadas, amongst the loud
nocturnal chorusing of the males, it posed the question of how Tonatia
locates such insect prey. Do bats locate such prey items via echoioca
tion or sounds produced by the insects?


-"*


62
for consumption as already discussed. The use of day roosts as feeding
places by _C_. perspici 1 lata is mainly a phenomenon related to feeding on
one fruit, Anacardium excel sum, as is evident from the dominance of this
fruit below day roosts and the decrease of dropped fruits and seeds when
exce 1 sum is not in fruit (Table 18). It is likely that temporary
night feeding roosts are used by these bats to avoid making the day
roosts conspicuous to predators and to reduce flight distances between
foraging forays.
The flight activity of Carol 1ia through the night is presented in
Figure 8. Both species show major peaks of flight activity in the first
hour of darkness. This is much earlier than the start of most canopy
frugivores1 flight activity and is probably due to the groundstory
becoming dark about an hour before the canopy level of the forest.
Cycles of flight activity in groundstory frugivores are bimodal or tri-
mod a 1 as are those of canopy frugivores. Two or three such bouts of
diel feeding activity also have been observed in fruit bats by Brown
(1968) and LaVal (1970) and seem characteristic of bats that feed on
foodstuffs that are not efficiently assimilated.
Scavenging Frugivore Guild
Body size
Centurio senex (Stenoderminae, Phy1lostomatidae), the wrinkle-faced
bat, is the sole member of the scavenging frugivore guild. A lactating
female weighed 22 g and a pregnant female weighed 27 g. No other weights
are available from Barro Colorado for this species, nor are there any
useful data on vertical stratification or habitat selection.


Hymenoptera explosively increase in numbers of individuals and biomass.
In general most of the food resources eaten by bats, with the exception
of flowers, are abundant during the March-July period and many species
of bats that move out of this forest habitat in the late wet season
return by March.
Minimal diversity within the bat community occurs in the late wet
season. Fruit is scarce in both kinds of mature fruits and total biomass,
and fruit bat species diversity is lowest during this period. The species
diversity of insectivorous bat species also reaches a minimum during the
late wet season, and though the actual total numbers and biomass of in
sects are probably slightly lower in the dry season, the availability of
insects as food for bats is probably lowest in the late wet season, when
frequent heavy rains often curtail insect and bat activity.
Annual variation of physical and biotic factors in the tropical
forest also appears to affect the diversity of the bat community. Rain
fall may fluctuate drastically from year to year in absolute amount and
distribution through the year (Smythe, 197^). An extended wet season may
prevent or destroy flowers in a given year and a late dry season may hin
der or delay fruit production or insect reproduction. Furthermore some
species of plants do not reproduce every year (Foster, 1973; Frankie
et a 1., 1974). The diversity and abundance of bat spec ies were somewhat
different in magnitude each of the three years on Barro Colorado. The
causal factors that influence annual variation in the bat community are
unclear but probably involve predation, food supply, and competition.
At the ordinal level, the communities formed by tropical bats are
by far the most complex assemblages of sympatric mammalian species occur
ring anywhere in the world. Much simpler communities of bats are found


Figure 11. Reproductive timing in female Artibeus 1ituratus.


38
Table 10.
Feeding niche overlaps (C/} ) among species of the
canopy frugivore guild
A. phaeotis
.215** .354* and
V. pus ilia
.968*
C. trinitatus
V. helleri
C. villosum
V. caraccioloi
A. jamaicensis
A. 1ituratus
.615**
.241**
. 465*
. 485**
.518**
.452
.796
.679
.272
.152
.893*
743
.644
.209
.412
.798*
.886
.852 '
.452
.727*
.200
.310
.99** .962
.983*
Denotes species most similar in body weight
Denotes overlap with the feeding generalist


MATERIALS AND METHODS
2
Seventeen sampling stations were located in an approximately 2 km
central strip of Barro Colorado Island and one station was on Buena Vista
Peninsula (Fig. 1). Habitats sampled during the study are classified as
mature forest (14 stations on BCI), creeks (3 stations on BCI), and
second growth (1 station on Buena Vista). The mature forest has a com
pletely closed canopy and is a minimum of 60 years old in all places.
Some tracts within the forest have been undisturbed for 400 years
(Robin Foster, pers. comm.). The creek stations are lined with rich
shrub growth and the creek bed receives direct sunlight. The second
growth habitat at Buena Vista is approximately 20 years old and consists
of thick shrub growth and scattered small trees that form a discontin
uous canopy.
Except on rare occasions when nets were damaged by tree falls or
vandalized by poachers, each sampling station consisted of four or six
6 x 2 m mist nets and one or two Tuttle harp traps (described in Tuttle,
1974) set across permanent trails. Nets were set in pairs at 100 m
intervals, with one of each pair at ground level (0 to 3 m) and the other
at subcanopy and lower canopy level (3 to 12 m). Early in the study nets
were rigged in the canopy as high as 25 m above ground, but use of these
nets was soon discontinued because few bats were captured in them,which
seemed to reflect a lack of much flight activity in the canopy levels.
Harp traps were usually set at ground level in low, narrow tunnel-like
passages created by the vegetation and trails. At a few stations where
6


This work ¡s dedicated to Clark Sanford, Julie Wiatt, and Bill
Biven, my field assistants, who endured a year of damp weather, irritat
ing insects, bat bites, tough pork chops, and numerous other tropical
hardships, yet shared the enumerable joys we encountered. We learned
much together of tropical forests and ourselves and are better people
for it.


41
Habitat selection
Comparison of netting samples from the young open forest of Buena
Vista and the closed canopy forest and creek habitats of Barro Colorado
provide a measure of species preferences for three habitats (Fig. 4).
As a group the fig specialists are much more common in the closed forest
and creeks lined by closed forest than in the shrubby open forest where
few mature trees of their preferred food species are found. A_. phaeot i s
and A. ¡ama i cens i s are common to very abundant in all three habitats, as
would be expected from their more generalized food requirements. None
of the extreme fig specialists are common on Buena Vista Peninsula.
Feeding behavior
Canopy frugivores usually carry fruits by mouth from fruiting trees
to night feeding roosts (Goodwin and Greenhall, 1961; Morrison, 1975)-
On BCI Morrison found that the night feeding roosts of A_. jama i cens i s
are frequently several hundred meters away from the fruiting trees where
they .are picked. Only when feeding on the large fruits of Dipteryx
panamensis did Artibeus feed on fruiting trees. All four most common
canopy frugivore species were observed to carry whole or partially eaten
fruits in flight. These animals presumably were transporting food items
to a night feeding roost for consumption. Whether the less common
species in the guild use night feeding roosts is unknown.
The fruits carried in flight by fruit bats vary in weight from less
than 1 g to about 20 g. Most bats carry fruits that weigh 20 to kOZ of
their own body weight. Table 12 lists the range in weights of some
fruits eaten by stenodermine bats. There is considerable variation in
the weights among and within species for these fruits (even in fruits
from the same individual tree).


Abstract of Dissertation Presented to the
Graduate Council of the University of Florida in Partial
Fulfillment of the Requirements for the Degree of Doctor of Philosophy
FORAGING AND REPRODUCTIVE ECOLOGY IN A COMMUNITY
OF BATS IN PANAMA
By
Frank Joseph Bonaccorso
August, 1975
Chairman: Dr. John H. Kaufmann
Major Department: Zoology
Resource partitioning, reproduct ion, species diversity, and
community structure in a forest community of 35 bat species were
studied on Barro Colorado island, Panama Canal Zone, Sixteen months
of field-work were conducted between July 1971 and August 197^. Over
2,800 bats were captured, banded, and released with data collected on
food habits, activity cycles, habitat selection, reproductive timing,
and morphological feeding adaptations for each species. Information on
the seasonality and abundance of fruit, flower, and insect resources
used by bats also was collected.
The diversity of tropical lowland bat communities in any one
habitat changes significantly on a seasonal basis. Fluctuating levels
of food resources require that many species utilize different habitats
and foraging strategies through a year. Competitive interactions,
predator avoidance, and climatic fluctuation further influence the
v


PERCENT OF ADULT FEMALES
Arfibeus phaeotis
J-S
15
S-N
N-D
19
CD
Co