Title: Importance of organic color, bacterioplankton and planktivore grazing in structuring ciliated protozoan communities in subtropical lakes /
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Title: Importance of organic color, bacterioplankton and planktivore grazing in structuring ciliated protozoan communities in subtropical lakes /
Physical Description: vi, 227 leaves : ill. ; 29 cm.
Language: English
Creator: Beaver, John R ( John Randolph ), 1955-
Publication Date: 1990
Copyright Date: 1990
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Subject: Environmental Engineering Sciences thesis Ph. D   ( lcsh )
Dissertations, Academic -- Environmental Engineering Sciences -- UF   ( lcsh )
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Thesis: Thesis (Ph. D.)--University of Florida, 1990.
Bibliography: Includes bibliographical references (leaves 205-226).
General Note: Typescript.
General Note: Vita.
Statement of Responsibility: by John R. Beaver.
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Volume ID: VID00001
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IMPORTANCE OF ORGANIC COLOR, BACTERIOPLANKTON AND PLANKTIVORE
GRAZING IN STRUCTURING CILIATED PROTOZOAN COMMUNITIES IN
SUBTROPICAL LAKES
















By



JOHN R. BEAVER


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



UNIVERSITY OF FLORIDA


1990
















ACKNOWLEDGMENTS

A number of individuals contributed to the completion of

this study.

Drs. Gabriel Bitton, Daniel Canfield, Jr., Edward Phlips and

Frank Nordlie served on my supervisory committee and made

constructive comments on an earlier draft. Their assistance is

gratefully acknowledged. Dr. Thomas Crisman provided financial

support and his friendship throughout my graduate studies. He

deserves special thanks for tolerating the many days when "Snapping

Dog" reared his ugly head in the lab.

My Student Assistants, John Kiefer, Lisa Modola, and Jacqueline

Smyre, provided their respective expertise at critical times during

the completion of this work. Adolph Coors contributed countless

beverages. Members of my family--Heidi, Amber, Wilma, Terri, Cisco,

Spec, Bucky, Bud and Gus--have supported me throughout my Ph.D work.

Finally, this work would not have been possible without the

encouragement of my wife, Karen, and our daughter, Danielle. Their

extraordinary understanding and sacrifices are appreciated.

















TABLE OF CONTENTS


ACKNOWLEDGMENTS............................................... ii

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

CHAPTERS

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

II LITERATURE REVIEW..... .................................. 6

Introduction.............................................. 6
Taxonomic Replacements Associated with
Increased Eutrophication.............................. 6
Ciliate Community Structure Relative to Lake Acidity..... 8
Temporal Variation of Small Ciliate Populations........... 13
Spatial Distribution of Small Ciliate Populations within
the Water Column...................................... 15
Temporal and Spatial Distribution of Large Meroplanktonic
Ciliate Populations................................... 17
Ciliates as Prey for Zooplankton......................... 21
Planktonic Ciliates as Grazers of Phytoplankton.......... 22
Planktonic Ciliates as Grazers of Bacteria............... 23
Importance of Myxotrophic Ciliates in the Plankton........ 28
Ciliate Importance in Phosphorus Regeneration............. 30
Ciliate Importance in Nitrogen Regeneration.............. 35
Ciliate Importance in Carbon and Energy Flow.............. 36

III COMMUNITY STRUCTURE OF CILIATES IN FLORIDA LAKES......... 39

Introduction.. ........................................... 39
Methods.................................................. 40
Results and Discussion.................................. 43

IV SEASONALITY OF PLANKTONIC CILIATES IN FLORIDA LAKES...... 62

Introduction.. ........................................... 62
Methods.................................................. 63
Results................................................... 64
Discussion.. ............................. ................ 74














V CILIATE POPULATIONS IN HIGHLY COLORED FLORIDA LAKES...... 79


Introduction ....................... ...................... 79
Methods .................................................. 80
Results......... .............................. .......... 84
Discussion.................................... ................. 97


VI BACTERIOPLANKTON POPULATIONS OF FLORIDA LAKES............ 102


Introduction...............
Methods..................
Results ....................
Discussion.................


102
103
104
110


VII PATTERNS IN PRIMARY PRODUCTIVITY IN FLORIDA LAKES........ 121


Introduction...........................
Methods......... ........................
Results and Discussion..................
Conclusions.............................


VIII EFFECTS OF PUMP-FILTER (DOROSOMA CEPEDIANUM) AND
FACULTATIVE OMNIVOROUS (TILAPIA AUREA) FISH ON CILIATED
PROTOZOAN COMMUNITIES IN FLORIDA LAKES .................


Introduction...........................
Methods.......... ......................
Results..................................
Discussion..............................


IX SUMMARY AND CONCLUSIONS................................. 182


Summary........................................................ 182
Conclusions............................................. 186
Areas for Future Research................................ 189


APPENDIX A SUMMARY STATISTICS FOR BACTERIAL ABUNDANCE
BY SEASON ................................................. 191


APPENDIX B SUMMARY STATISTICS FOR BACTERIAL ABUNDANCE BY LAKE.. 194


APPENDIX C SUMMARY STATISTICS FOR PRIMARY PRODUCTIVITY AND
CHLOROPHYLL........... ...... ............... .................. 197


APPENDIX D SUMMARY STATISTICS FOR ENCLOSURE STUDY.............. 201


BIBLIOGRAPHY...... ............................................. 205


BIOGRAPHICAL SKETCH........................................... 227


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


IMPORTANCE OF ORGANIC COLOR, BACTERIOPLANKTON AND PLANKTIVORE
GRAZING IN STRUCTURING CILIATED PROTOZOAN COMMUNITIES IN
SUBTROPICAL LAKES



by


JOHN R. BEAVER


MAY 1990


Chairman: Thomas L. Crisman
Major Department: Environmental Engineering Sciences

The planktonic ciliate communities of 37 Florida lakes were

analyzed along gradients of organic color and trophic state.

Mean annual ciliate abundance and biomass were both strongly

related to algal biomass (as measured by chlorophyll a). Small-

bodied taxa progressively dominated Florida with increasing trophy.

Only minor taxonomic differences were noted between ciliate

communities of clear and colored Florida lakes of similar trophy.

Ciliate community diversity and species richness was lowest in

acidic, oligotrophic systems and increased with trophic state.

Florida lakes had ciliate biomass comparable to the north temperate

zone, but the average ciliate size was smaller in subtropical lakes.

Detailed patterns in bacterioplankton abundance and primary

productivity in Florida lakes were presented. Temporal changes










in ciliate communities were largely a function of color and trophic

state classification. Seasonal dynamics of ciliate populations in

clear water Florida lakes corresponded to seasonal dynamics of their

principal food (bacteria). Little temporal correspondence was noted

between ciliates and bacteria in colored lakes. Food quality and

quanitity were believed to control temporal dynamics of ciliate

populations, particularly in oligotrophic and mesotrophic lakes.

The effects of facultative omnivorous (Tilapia aurea) and pump-

filter feeding (Dorosoma cepedianum) fish on ciliate community

stucture were determined in large, field mesocosms. Dorosoma

cepedianum promoted the biomass of ciliates relative to Tilapia. It

was suggested that the increased importance of small-bodied ciliate

taxa (principally scuticociliates) in productive lakes is directly or

indirectly linked to fish grazing activities.

















CHAPTER I
INTRODUCTION

Planktonic ciliated protozoa have been ignored historically in

studies of freshwater plankton ecology. It is now apparent that they

both form an integral part of the planktonic food web (Porter et al.

1985) and contribute significantly to the total zooplankton standing

crop (Gates 1984; Pace 1986). This plankton group has been

overlooked by both phytoplankton and zooplankton specialists.

Logically, protozoa should be studied by zooplankton ecologists, but

they typically collect samples with nets through which most ciliates

pass. The methodology used to enumerate planktonic protozoa is most

suitable to the phytoplankton specialist; however, they seldom record

protozoan taxa. Futhermore, the preservation techniques employed for

both phytoplankton and zooplankton (ethanol, Lugol's solution,

formalin) are extremely disruptive to ciliates and render their cells

unrecognizable.

The general data base on planktonic ciliates in lake

environments is scant. Recently, development of improved

preservation techniques and an increased enthusiasm on the part of

limnologists and protozoan ecologists have contributed to a modest

but growing list of studies dealing with ciliate distributions.

The relationship between the abundance and biomass of the

total ciliate community and trophic state has been investigated by

several researchers (Beaver 1980; Gates 1984; Pace 1986). Included













among the limnological variables commonly used to assess trophic

state, both total phosphorus and chlorophyll a concentrations are

significantly related to ciliate abundance with the latter being more

strongly correlated with ciliate abundance in lakes (Beaver 1980;

Pace 1986). Typically, oligotrophic lakes are characterized by

modest ciliate populations while more productive lakes exhibit

greater abundance.

Three orders of ciliates-Haptorida (e.g. Mesodinium,

Askenasia), Scuticociliatida (e.g. Cyclidium), and Oligotrichida

(e.g. Strombidium, Strobilidium, Halteria)-typically dominate

planktonic communities. Although the mean annual abundance of all

three orders generally increases along the trophic gradient, their

rank-dominance changes markedly. Oligotrichs are usually the

dominant order in oligotrophic situations (Hecky et al. 1978; Hunt

and Chein 1983), but are progressively replaced by the

scuticociliates in more productive lakes (Beaver and Crisman 1982;

Pace 1982). The occurrence of large numbers of scuticociliates in

oligotrophic lakes is usually limited to the often observed fall

maximum in total ciliate abundance (Hecky et al. 1978). The

contribution of haptorids does not appear to change markedly with

trophic state (Beaver and Crisman 1982).

Ciliates in the size class 20-30 microns (mostly

scuticociliates) are numerically dominant in most Florida lakes,

but their importance generally increases with higher trophic state

(Beaver 1980). Conversely, the importance of the 40-50 microns

size class (mostly oligotrichs) decreases with higher productivity.












The above trends in ciliate distribution have usually been

determined in isolation from other plankton components. Few attempts

have been made to relate structural and functional characteristics of

plankton assemblages to ciliate composition.

Based on my previous work (Beaver 1980), I determined that

ciliate abundance in Florida lakes was positively related to lake

trophic state. I also described in general terms a broad taxonomic

replacement series whereby small-bodied ciliates progessively

replaced larger forms with increased eutrophication. The study base

I used consisted of 30 lakes ranging from acidic oligotrophic to

hypereutrophic. Of these lakes, five could be considered highly

colored (>100 Pt units). These systems appeared to have

significantly different seasonalities when contrasted with clear

water lakes of comparable trophy. Due to the small number of colored

lakes, I was unable to statistically define these differences.

Thus, my first hypothesis was that planktonic ciliates in highly

colored Florida lakes display different seasonality and biomass than

clear water lakes. To test this hypothesis, my original data set was

supplemented with ciliate data from an additional seven colored

lakes, and contrasted with a comparable gradient of clear water

lakes.

The majority of planktonic ciliates are bactivorus (Porter et

al. 1985), and the temporal dynamics of bacterioplankton are believed

to strongly influence ciliate populations. In addition, most

planktonic ciliates utilize suspension-feeding as a nutrition

mode. Fenchel (1980a) predicted that suspension feeding bactivorous












ciliates should be largely excluded from lakes with reduced

bacterioplankton populations. Given this evidence, I have

hypothesized that ciliate community structure in clear and colored

lakes may be related to bacterioplankton densities. To test this

hypothesis, I assessed the relationship between bacterial abundance

and lake trophic state for Florida lakes along gradients of color and

trophy, and related the seasonal dynamics of bacteria to temporal

changes in planktonic ciliate populations.

The third hypothesis I tested involved the effects of

planktivorous fish grazing on the character of ciliate communities.

Bays and Crisman (1983) concluded that the major factor structuring

zooplankton communities in eutrophic and hypereutrophic Florida lakes

was the grazing activities of gizzard shad (Dorosoma cepedianum).

This fish exhibits a pump-filter feeding nutritional mode with

greatest predation effects falling on non-evasive zooplankters and

algae >40 microns (Drenner et al. 1986). Given that small-bodied

(<30 microns) ciliates dominate the ciliate communities of most

productive Florida lakes, I hypothesized that this correlation may be

related to indirect or direct grazing effects of gizzard shad upon

the microbial food web. To assess the effects of planktivore

activities on ciliate populations, an enclosure experiment was

conducted in a productive lake in which zooplankton, ciliated

protozoa, phytoplankton and bacteria community responses to Dorosoma

cepedianum and Tilapia aurea were determined. Primary productivity

measurements were also made and related to plankton composition in

the enclosure experiment.






5





Finally, I related my results delineating ciliate community

structure, bacterioplankton, and primary production in Florida lakes

to comparable data bases from the temperate zone. In doing this, I

shall be able to describe potential differences between the microbial

food web in Florida and temperate lakes and allow an assessment of

structural and functional differences based on climatic region.


















CHAPTER II
LITERATURE REVIEW

Introduction

This chapter reviews the data on the structure and role of

ciliated protozoa, accumulated primarily during the last ten years,

with special emphasis on the role of ciliates as trophic linkages in

freshwater planktonic food webs.

Taxonomic Replacements Associated with Increasing Eutrophication

The relationship between the abundance and biomass of the

total ciliate community and trophic state has been investigated by

several researchers (Beaver 1980; Gates 1984; Pace 1986). Included

among the limnological variables commonly used to assess trophic

state, both total phosphorus and chlorophyll a concentrations are

significantly related to ciliate abundance, with the latter being the

most accurate predictor of total ciliate abundance in lakes (Beaver

1980; Pace 1986). Typically, oligotrophic lakes are characterized by

modest ciliate populations (<10 cells/ml), while more productive

lakes exhibit greater abundance (Table 2-1).

Three orders of ciliates--Haptorida (e.g. Mesodinium,

Askenasia), Scuticociliatida (e.g. Cyclidium), and Oligotrichida

(e.g. Strombidium, Strobilidium, Halteria)--typically dominate

planktonic communities. Although the mean annual abundance of all

three orders generally increases along the trophic gradient,

their rank dominance changes markedly. Oligotrichs are usually



















Table 2-1. Summary of data on annual abundances of planktonic
ciliates in lakesa


Trophic State


Range of observed
values (cells/ml)


Chlorophyll a values
(mg/cubic meter)


Ultraoligotrophic

Oligotrophic

Mesotrophic

Eutrophic

Hypereutrophic


2.4

2.3 10.8

18.0 70.9

55.5 145.1

90.0 215.0


a modified from Porter (1984)


1 5

5 10

10 56

> 56












the dominant order in oligotrophic situations (Hecky et al. 1978;

Hunt and Chein 1983), but are progressively replaced by the

scuticociliates in more productive lakes (Beaver and Crisman 1982;

Pace 1982). The occurrence of large numbers of scuticociliates in

oligotrophic lakes is usually limited to the often observed fall

maximum in total ciliate abundance (Hecky et al. 1978). The

contribution of haptorids does not appear to change markedly with

trophic state (Beaver and Crisman 1982).

Ciliates in the size class 20-30 microns (mostly

scuticociliates) are numerically dominant in most Florida lakes

(Figure 2-1), but their importance generally increases with higher

trophic state (Beaver 1980). Conversely, the importance of the 40-

50 microns size class (mostly oligotrichs) decreases with higher

productivity. In contrast to the subtropics, small ciliates (18-24

microns) are more important in oligotrophic Canadian lakes (Gates

1984; Gates and Lewg 1984) than in comparable oligotrophic Florida

lakes (Beaver 1980).

Ciliate Community Structure Relative to Lake Acidity

The historical development of acid precipitation and the

biotic response in softwater lakes of Scandinavia (Braekke 1976)

and the United States (Cogbill and Likens 1974) have been well

documented. Major differences have been noted in zooplankton

community structure between comparably acidic temperate and

subtropical lakes (Brezonik et al. 1984). Increased acidity is

accompanied by a reduction in both the number of species and the

abundance of total zooplankton in both temperate (Hendrey and Wright



















< 20 qm E
20-30 qm *
30-40 qm ]
40-50 Lm i]
> 50 qtm


OA ON M -E H


Figure 2-1. Size partitioning of ciliate communities by trophic
classification for 30 Florida lakes (from Beaver 1980).












1976) and subtropical (Crisman and Brezonik 1980) lakes. Important

macrozooplankton taxa such as Daphnia are often eliminated from

highly acidic temperate lakes (Sprules 1975), but not in comparable

subtropical lakes (Brezonik et al. 1984).

Beaver and Crisman (1981) investigated planktonic ciliate

communities in softwater subtropical lakes (pH 4.7-6.8) and noted

that both the abundance and biomass of total ciliates generally

decreased with increased acidity. The sharpest reduction was seen in

lakes <5.0 pH. The orders Oligotrichida, Haptorida, and

Scuticociliatida co-dominated ciliate assemblages of lakes >pH 5.0,

but were replaced by the Oligotrichida in more acidic lakes (Table 2-

2). The percentage contribution of ciliated protozoa to total

zooplankton biomass decreased with decreasing pH (Brezonik et al.

1984), but only minor taxonomic replacements were observed for

rotifers and crustaceans.

In addition to the observed compositional shift, smaller

ciliates (especially 20-30 microns) were progressively replaced by

larger ciliates (40-50 microns) with increasing acidity. The

smaller size class contained most of the scuticociliates (Cyclidium),

while a majority of the oligotrichs (Strombidium, Strobilidium) and

some of the haptorids (Askenasia) fell into the larger size class.

A recent investigation of an acidic Florida system (Bienert

1987) suggests that a relatively large-sized ciliate (150-200

microns), Stentor niqer (Heterotrichida), appears to be a good

indicator of acidic conditions. Stentor niger is quite sensitive to

distortion during preservation, and precise identification requires




















Table 2-2. Annual mean percentage composition (+ SD) of ciliate
communities examined for response to lake acidification


pH Interval


Haptorida


Oligotrichida


Scuticociliatida


6.0 7.0

5.5 6.0

5.0 5.5

< 5.0


28.3 + 7.3

21.7 + 1.7

14.9 +14.2

11.9 + 6.7


37.7 +18.0

48.3 +12.9

49.1 +18.7

73.2 +16.6


17.9 +13.9

26.0 + 7.8

10.6 +14.8

5.2 + 9.1


a taken from Beaver and Crisman (1981)












collection of live specimens. Its reaction to a variety of

preservatives gives it the appearance of detrital material, and

unless inspected closely, it may be easily overlooked.

The functional role of S. niger in the microbial food web of

lakes in which it dominates is probably very substantial since all

specimens were densely packed with zoochlorellae. Its myxotrophic

mode of nutrition (utilization of particulate, photosynthetically

fixed, and dissolved organic carbon) (Porter et al. 1985; Porter

1987) is likely an adaptation to nutrient limited conditions. The

fact that peak densities of this species occur only during thermal

stratification in summer further supports this interpretation

(Bienert 1987).

Bick and Drews (1973) suggested that physiochemical exclusion

may be important for limiting the distribution of ciliates with many

species reaching their tolerance limit between pH 4.0-5.0. While

direct physiological exclusion must exert some influence on ciliate

distributions, food availability may be the principal governing

factor. Bacterial biomass in temperate lakes often declines with

decreasing pH (Bick and Drews 1973), and those ciliate taxa dependent

on bacteria as their principal food should also decline with

increased acidity. The reduced importance of scuticociliate and

haptorid taxa in such acidic lakes probably reflects the inefficiency

of these ciliates to concentrate bacteria from a dilute suspension

(Fenchel 1980b). In contrast, the larger-bodied oligotrichs can

subsist due to their ability to utilize nannoplanktonic algae in

addition to bacteria.












It is important to note that our understanding of ciliate

community structure in acidic lakes is limited to subtropical Florida

lakes. Comparable data from the temperate zone do not exist.

Temporal Variation of Small Ciliate Populations

The seasonal dynamics of small planktonic ciliate populations

are poorly understood, but recent evidence indicates that lake

thermal regimes (especially timing and duration of thermal

stratification) may indirectly influence protozoa by leading to

localized enhancement of food resources within the water column (Pace

1982).

Oligotrophic lakes, which are often deep, are characterized by

maxima of total abundance and biomass in the fall (Hecky and Kling

1981; Hunt and Chein 1983; Lewis 1983). The population pulses in

these nutrient-poor systems are invariably dominated by the

oligotrichs. Members of the Haptorida and Scuticociliatida, although

poorly represented, generally peak simultaneously with the

oligotrichs (Hecky and Kling 1981). Mesotrophic lakes, which are

usually moderately deep and nutrient enriched, often display a

bimodal pattern of ciliate abundance and biomass dominated by the

Scuticociliatida (Sorokin and Paveljeva 1972) population peaks in

both temperate and subtropical lakes occur in late spring and early

fall, corresponding to the periods of initial thermal stratification

and destratification, respectively.

Detailed seasonality data for small ciliates in productive lakes

are sparse, but it appears that protozoan communities often peak

during summer and are associated with metalimnetic and hypolimnetic











plates of senescing algal and bacterial cells (Pace and Orcutt 1981;

Pace 1982).

Food resources probably are the major regulator of ciliate

populations (diversity, abundance, biomass) in general and the

temporal succession of ciliate communities in particular (Pace 1982).

Systems poor in nutrients tend to have population surges associated

with thermal overturn--the time of highest productivity.

Populations tend to be densest in the epilimnion instead of being

associated with metalimnetic plates of algae and bacteria (Hecky and

Kling 1981; Hunt and Chein 1983). Like oligotrophic systems,

mesotrophic lakes also experience a peak of abundance and biomass

during fall associated with mixis. An additional late spring surge

is probably due to the accumulation of organic matter in the

metalimnion after stratification (Sorokin and Paveljeva 1972), and

the subsequent development of bacterial densities exceeding the

threshold concentrations necessary for growth of scuticociliate and

other bactivorous ciliate populations (Fenchel 1980a).

Finally, unlike lower trophic states, populations of small-

bodied ciliates in eutrophic-hypereutrophic lakes displayed midsummer

maxima that are likely associated with the accumulation of detritus

and bacteria from the photic zone column in the lower water column.

In addition, the relative shallowness of most productive systems

dictates a more rapid warming of both the water column and sediments

which hastens growth rates of both ciliates and bacteria (Finlay 1977).

Various components of limnetic ciliate communities are

significantly correlated with their food resources both temporally











(Gates 1984) and spatially (Sorokin and Paveljeva 1972; Pace 1982).

Consequently, the interrelated factors of lake depth, nutrient

concentrations, and the thermal regimes of lakes substantially

determine both potential food sources for ciliates and patterns in

seasonal succession.

Spatial Distribution of Small Ciliate Populations
within the Water Column

Relatively little information is available on the factors

controlling the distribution of small ciliate taxa within the water

column. The notable exception is investigations conducted in a

eutrophic Georgia reservoir (Pace and Orcutt 1981; Pace 1982). In

this system, the vertical distribution of ciliate abundance was

nearly uniform during winter mixis, although there was a tendency

towards slightly higher values near the surface. After development

of stable thermal stratification, protozoan numbers increased in the

warming epilimnion and decreased in the hypolimnion. A bloom of

scuticociliates began in the metalimnion and hypolimnion during

midsummer and was sustained until early fall. Peak abundances were

recorded just below the thermocline. Concurrent with this bloom of

scuticociliates in the lower water column, the density and diversity

of epilimnetic ciliates increased until destratification.

The vertical distribution of individual species in this

reservoir was also influenced by stratification. During winter

mixis few vertical distribution gradients were evident, but after

stratification and subsequent oxygen reduction in the hypolimnion,

individual taxa were confined to specific sections of the water

column. Small oligotrichs were restricted to the epilimnion while












scuticociliates and an omnivorous Coleps sp. were largely found in

the metalimnion and hypolimnion and were significantly correlated

with high algal and bacterial activity (Pace 1982). Strombidium

viride, however, was always located near the surface because its

symbiotic zoochlorellae imposed a partial dependence on a light

source. It was suggested that nutrition is the major determinant for

the vertical distribution of small ciliates-myxotrophic ciliates

were found in the photic zone and primarily bactivorous forms (e.g.

scuticociliates) were located in the metalimnion where bacterial

densities were high.

A similar relationship between abundance of ciliates and thermal

stratification has been demonstrated for two large oligotrophic

lakes. Hunt and Chein (1983) reported that small ciliates,

principally oligotrichs, were distributed throughout the water column

of a temperate lake during holomixis but tended to concentrate in the

epilimnion as the thermocline deepened during summer. Hecky and

Kling (1981) reported that most ciliates in tropical Lake Tanganyika

were confined to the epilimnion during stratification. Their biomass

frequently equalled or exceeded phytoplankton biomass because of the

contribution of myxotrophic ciliates to total autotrophic standing crop.

Sorokin and Paveljeva (1972) reported that ciliates formed a

substantial portion of the zooplankton biomass in a mesotrophic

Soviet lake. Maximum ciliate concentrations were found in the

metalimnion with biomass reaching approximately 3 g C m-3, close to

the total biomass of other zooplankton forms. Numerical abundance in

this region ranged from 87 to 192 ciliates ml- The development of











metalimnetic protozoan plates coincided with elevated bacterial

densities associated with decaying algal cells. Large increases in

the predatory rotifer Asplanchna were noted within specific regions

of the water column subsequent to ciliate population blooms, strongly

suggesting a predator-prey relationship.

Temporal and Spatial Distribution of Large
Meroplanktonic Ciliate Populations

The best understood area of freshwater protozoan ecology is the

vertical and seasonal distribution of large (>100 microns) ciliates

in very productive water bodies (cf. Goulder 1980; Bark 1985; Finlay

1985). The occurrence of large ciliates in the plankton is a

predictable event directly related to thermal stratification and the

resulting deoxygenation and accumulation of reducing compounds in the

hypolimnion and at the sediment-water interface.

Goulder (1971a, 1971b, 1974, 1975) extensively investigated the

distribution of large ciliates within the water column of shallow

hypereutrophic Priest Pot and determined that ciliate densities were

correlated with oxygen concentrations. During summer stratification,

the displacement of otherwise hibernal benthic species in the

hypolimnion was related to anoxia at the sediment-water interface

(Goulder 1971b).

Typically, the large benthic ciliates, Frontonia leucas,

Spirostomum teres, S. minor, and Loxodes magnus regularly migrated

from anoxic sediments during summer stratification and moved

progressively higher in the water column (5-6 m from the sediments)

as the zone of deoxygenation expanded upwards (Bark 1981; Finlay

1981) (Figure 2-2). As stratification deteriorated, this population












migrated downwards and returned to the sediments. A second

association of large thiobiotic ciliates that are obligate anaerobes

(Brachonella spiralis, Caenomorpha medusula, and Metopus es) appeared

and occupied a region of the hypolimnion just previously vacated by

the first group. Finally, peritrich ciliates (Vorticella,

Epistvlis), which are epiphytic and epizootic on large phytoplankton

and zooplankton, usually remained in the epilimnion (Bark 1981).

Consequently, there was an absence of significant spatial overlap

within the water column by the large ciliates (Bark 1985) (Figure

2-3). Finlay (1980) demonstrated that vertical migration both within

the sediments and into the water column of hypereutrophic lakes is

governed by the development of the redox discontinuity profile.

The ability of these large ciliates to survive anaerobic

conditions indicates that they are facultative or obligate anaerobes.

Goulder (1972a) suggested that these ciliates may undergo pronounced

diel vertical migration to the overlying oxygenated water. An

alternative explanation for the occurrence of large ciliates in

anoxic waters is that oxygen may be present at very small

concentrations in the hypolimnion due to eddy diffusion and

production by photosynthetic bacteria and phytoplankton (Bark and

Goodfellow 1985). Finlay et al. (1983) reported the capacity of

Loxodes for anaerobic respiration using nitrate reduction on the

mitochondrial membrane as an energy source.

Finlay and Fenchel (1986) noted for species of Loxodes that

increased light intensities aggravated oxygen toxicity. Exposure of

cells to light at the oxic-anoxic boundary induced downward
















E 15 14 13 910 10 11 10
15
te-i

w
W



1 0

,, oi'" "
.. 0 i&:h
a o d n E w i I
S6-10 .
< e-o "" i i"
2-- r I
H3 ,/'" *

O 13 10 5 1 1011
F A J 0 D









Figure 2-2. Migration of large ciliated protozoa coupled to the
availability of dissolved oxygen in Esthwaite Water in 1979. Symbols
refer to total numbers of ciliates in each sample. Isopleths of
dissolved oxygen concentration in steps of 1 mg/L with the exception
of the lowest, thick line representing 0.3 mg/L (from Finlay 1981).




























































Figure 2-3. Vertical distribution of various planktonic ciliates
on 31 August 1977 in Esthwaite Water (from Bark 1985).










migration. Photosensitivity and oxygen toxicity are thus

biochemically linked, and removal of Loxodes from a supply of oxygen

inhibits photosensitivity. This tendency towards microaerophily by

Loxodes and similar ciliates allows them to occupy an area of the

water column devoid of potential predators and competitors rotiferss

and crustaceans). The latter are eliminated from the hypolimnion

because of their dependence on oxygen (Psenner and Schlott-Idl 1985;

Finlay et al. 1986).

Large ciliates (>100 microns) in hypereutrophic lakes therefore

display pronounced vertical distribution within the water column.

Some taxa live exclusively in the oxygenated epilimnion (Bark 1981),

others may be found only in the anoxic hypolimnion (Finlay 1985), and

yet another group straddles the boundary between oxygenation-

deoxygenation (Bark 1981) (Figure 2-3).

Ciliates as Prey for Zooplankton

The possibility that ciliates are a prey item for

macrozooplankton has been recognized (Porter et al. 1979), but the

extent of this interaction is uncertain because protozoa are rarely

recognizable in the gut contents of metazoa. Many laboratory studies

have determined that rotifers (Gilbert 1980), cladocerans (Tezuka

1974; Porter et al. 1979), and copepods (Korniyenko 1976; Archbold

and Berger 1985) effectively ingest ciliates as prey. A major

criticism of most of these studies is that they often are limited to

the genus Paramecium which is not a common component of the plankton.

Moreover, prey and predator concentrations are experimentally elevated

over those encountered in situ to achieve some measurable effect.












The studies which have used common representatives of the

ciliate plankton, Cyclidium glaucoma (Porter et al. 1979) and

Halteria grandinella (Archbold and Berger 1985), allow some

qualitative assessment of a possible trophic relationship. Porter et

al. (1979) demonstrated that Daphnia magna had higher rates of

filtering and ingestion when fed Cyclidium than when fed Paramecium,

although assimilation rates were comparable. Archbold and Berger

(1985) have shown in laboratory studies that crustaceans and naupliar

stages of cyclopoid copepods are effective predators on Halteria

grandinella. There is also some in situ evidence for

macrozooplankton cropping of ciliate populations (Sorokin and

Paveljeva 1972; Berk et al. 1977).

The importance of this predation link is that ciliates may

transform the picoplankton (bacteria) into a larger form available to

higher trophic levels. Since most metazoa are inefficient at grazing

bacteria (Crisman et al. 1981; Porter et al. 1983; Porter 1984), this

relationship likely represents a significant but poorly quantified

carbon and energy pathway in the freshwater plankton.

Planktonic Ciliates as Grazers of Phvtoplankton

Ample evidence suggests that algovorous activity by ciliates is

common (Bick 1972; Goulder 1972b; Heinbokel and Beers 1979). Peak

abundance of potential algal-grazing ciliates (large-bodied

oligotrichs) and their prey often coincide within the water column.

Nauwerck (1963) recorded peaks in oligotrich numbers simultaneously

with those of three small chlorophytes--Chlamydomonas, Stichococcus,

and Chlorella. Other investigators have observed the same












relationship in tropical and subtropical lakes (Kimor 1969; Hecky and

Kling 1981).

It has been hypothesized that oligotrichs may influence the

population dynamics of phytoplankton by grazing nannoplanktonic

chlorophytes (Beaver and Crisman 1982; Skogstad et al. 1987).

Heinbokel and Beers (1979) have demonstrated that marine oligotrichs

may graze as much as 20% of the phytoplankton crop daily. In

addition, Fenchel (1980a) has shown that ciliates which feed on

larger (>1 micron) particles compare favorably with metazoan

suspension feeders in the ability to concentrate particles from

dilute suspension. Finally, Finlay and Berninger (1984) noted that

different species of Loxodes partition their algal food sources on

the basis of particle size, and that this greatly influences spatial

and seasonal distributions.

Planktonic Ciliates as Grazers of Bacteria

Most free-living ciliates are bactivorous with each species

having a distinct particle size range which is retained and ingested

(Fenchel 1980b). The size spectrum preferred by each species is a

function of mouth size and morphology (Fenchel 1980c). Ciliates

which feed on the smallest (<1 micron) particles require high minimum

densities of bacteria to sustain growth. In the plankton of lakes,

there is a strong empirical relationship between bacterial densities

and chlorophyll concentrations (Bird and Kalff 1984). The small

bactivorous ciliates (e.g. species of Cyclidium) which are

specialized on extremely small cells (0.2-1 micron) require much

higher concentrations (5 x 10 6-5 x 10 8 cells ml-) than ciliates













specializing on larger particles. These densities of bacteria are

usually only encountered in eutrophic waters; however, during a

declining algal bloom in less productive waters the necessary

concentrations of bacteria may be found in localized areas such as

the metalimnion (e.g Sorokin and Paveljeva 1972). Therefore,

bacteria grazers such as the scuticociliates and other small taxa

could best be classified as opportunistic plankters exploiting areas

of dense microbial activity.

An empirical relationship exists between ciliate growth rates

and cell size with smaller ciliates growing proportionally more

rapidly than larger ones (Fenchel 1968). Taylor (1978) has confirmed

this relationship for pond ciliates and noted that the dominant forms

have a strategy for persistence based on size and growth rate (Taylor

1979a). Thus, the most successful ciliates may not always be

opportunistic. In addition, it has been suggested that ciliates may

actively flocculate bacteria prior to ingestion causing microspatial

heterogeneity in distribution (Taylor and Berger 1980). Finally, the

nutritional value of bacteria differ between ciliate taxa, and some

ciliates can utilize only a few bacterial strains (Taylor 1979b).

I suggest that limited food resources control both the

composition and body size of ciliated protozoan assemblages in the

plankton of freshwater lakes. All ciliates have a distinct particle

size range (determined by mouth size and morphology) that is most

efficiently grazed (Fenchel 1980b). Small-bodied ciliates, including

most of the Scuticociliatida, are principally bactivorous and can











retain particles as small as 0.2 micron, but display maximum grazing

efficiency on particles between 0.3 and 1.0 micron (Fenchel 1980a).

Evidence suggests that small ciliates ingest 80-120% of their body

volume per hour vs. 10-30% for large ciliates and are largely

excluded from lakes having <5 x 10 bacteria ml- : a concentration

normally found only in more productive systems (Fenchel 1980b).

Large-bodied planktonic ciliates are predominately phytophagous

(Fenchel 1980a) and generally are inefficient at grazing bacteria-

sized particles (<1.0 micron). The quantitative importance of

ultraplanktonic algae (<20 microns) as prey for either large or small

ciliates has not been adequately investigated.

Given the apparent resource partitioning by ciliates on the

basis of body size, it is not surprising that large-bodied

oligotrichs dominate oligotrophic lakes. Such lakes are

characterized by reduced phytoplankton populations composed primarily

of nannoplankton-sized taxa (Kalff and Knoechel 1978) and have

bacterial concentrations lower than those necessary to maintain

bactivorous ciliates (Porter et al. 1979). Although the abundance of

all ciliates would be reduced, small-bodied bactivorous taxa would be

expected to be more resource-limited in oligotrophic lakes due to

their dependence on higher ingestion rates (Fenchel 1980a).

The abundance of both large-bodied and small-bodied ciliates

increases with increasing lake trophic state, but the response is

more pronounced for the latter group, resulting in dominance of

eutrophic assemblages by small taxa. The principal food of

algovorous ciliates (nannoplankton) should also increase in eutrophic











lakes in spite of a shift in phytoplankton dominance to larger net

plankton (Kalff and Knoechel 1978). It has been suggested that only

in eutrophic systems are bacterial productivity and concentrations

not limiting to bactivorous ciliates (Porter et al. 1979; Fenchel

1980a). Freed by the constraints of limiting food resources,

populations of bactivorous ciliates should increase faster than those

of larger algovorous ciliates because of their faster turnover rates,

2-4 hours vs. 10-30 (Fenchel 1980a). In addition, the food

requirements of algovorous ciliates may overlap with those of larger

zooplankton. Food-related changes in resource competition between

these consumers could possibly further depress the population

response of algovorous ciliates to allow dominance of small (<30

microns) ciliates in eutrophic lakes. It is unlikely that similar

resource overlap exists between bactivorous ciliates and larger

zooplankton (Porter 1984). Fenchel (1986a, 1987) noted that filter

feeding by ciliates is the most efficient mechanism when the food

particle spectra is skewed towards smaller particles. The ratio of

volume of water filtered to cell volume ('volume specific clearance')

can approach 105, but ciliates specialized on very small particles

may have clearance values as much as ten times less. The size

spectra of retained particles show a sharply defined lower size range

(Figure 2-4). Consequently, many scuticociliates specializing on

smaller particles have greatly reduced clearance rates and are

dependent on high bacterial concentrations to survive.

Sherr and Sherr (1987) have recently measured bacterial grazing

by marine ciliates, including scuticociliates, to be 102-103 higher
























100 0







50






0 diameter, pm
0.1 05 1 5 10 40






















Figure 2-4. Retention efficiencies for the lower size of
intercepted particles in some filter-feeding ciliates. A:
Cyclidium glaucoma, B: Colpidium colpoda, C: Uronema marinum, D:
Halteria grandinella, E: Euplotes moebiusu, F: Blepharisma
japonicum, G: Bursaria truncatella (from Fenchel 1986a).













than earlier estimates in marine situations. Heterotrophic

microflagellates (Fenchel 1986b) and phagotrophic phytoflagellates

(Porter 1987) also strongly compete with ciliates for bacterial food,

but their role in the plankton is poorly described (Fenchel 1986b).

Importance of Myxotrophic Ciliates in the Plankton

Ciliates utilizing myxotrophy (forms containing symbiotic

zoochlorellae, most often Chlorella) as an alternative mode of

nutrition are quite common in a wide range of trophic conditions

(Hecky and Kling 1981; Berninger et al. 1986). The ecological

advantages for endosymbiotic algae include a continuous supply of

nutrients (CO2 and nitrogenous metabolites from the host) and freedom

from grazing pressure exerted by herbivorous zooplankton. The host

ciliate profits by reduced dependence on heterotrophic nutrition (Lee

et al. 1985) and occasional total reliance on the symbiont for

nutrients (probably in the form of maltose) (Meier et al. 1980).

There is strong evidence that several myxotrophic ciliates in

very productive ponds are seasonally dependent on their symbionts for

nutrition (Berninger et al. 1986). During summer stratification

benthic zoochlorellae-bearing species of Euplotes and Frontonia

migrated to a position in the water column near the oxic-anoxic

boundary and became densely packed with zoochlorellae. After fall

mixis, most of the symbionts were lost, and the ciliates returned to

a predominantly heterotrophic nutrition mode in the sediments.

Stokesia vernalis was exclusively epilimnetic during summer

stratification and probably encysted and disappeared once mixis

began. Acaryophyra and Disematostoma were always found in the water












column and concentrated near the oxic-anoxic boundary during

stratification. The abundance of zoochlorellae observed was

variable, but most individuals of the latter two species contained

captured dinoflagellate cells, indicating the dependence on the

symbiont was not total. Acarvophyra and Disematostoma became

homogeneously distributed during winter and switched totally to

heterotrophy (Berninger et al. 1986).

The vertical distribution of the above taxa resulted in some

spatial separation in the water column. The mechanism that achieves

this segregation is believed to be related to different behavioral

responses and photobehavior acquired by the host after establishment

of the symbiont (Berninger et al. 1986).

Attempts have been made both to quantify the extent of

myxotrophy in planktonic ciliate communities and to assess its

contribution to total autotrophic biomass (Hecky and Kling 1981;

Bienert 1987). In oligotrophic Lake Tanganyika, Hecky and Kling

(1981) noted that a prominent component of the plankton, myxotrophic

Strombidium cf viride, whose algal symbionts had a biomass that

nearly equalled or exceeded phytoplankton standing crop during stable

thermal stratification. Conversely, the proportion of myxotrophic

individuals was much lower during mixis and associated high algal

productivity. The greatest densities of S. viride occurred in the

nutrient-depleted photic zone (Hecky et al. 1978), similar to that

noted for marine oligotrichs (McManus and Fuhrman 1986). Similarly,

Bienert (1987) reported that myxotrophic Stentor niqer constituted

>90% of the annual mean ciliate biomass and 37% of zooplankton











biomass in a softwater acidic Florida lake. Its occurrence was

usually limited to spring and summer periods, a pattern considered an

adaptation to nutrient-limited conditions (Bienert 1987).

Although poorly quantified, the potential importance of these

facultative autotrophs is recognized (Porter et al. 1985).

Possession of algal symbionts is advantageous in nutrient poor

environments because of the great energy conservation and efficient

nutrient recycling characteristic of the relationship between host

and symbiont (Hallock 1981). The ecological significance of this

association rests in the ability of the ciliate to exploit

heterotrophic and/or autotrophic nutrition, adjusting the relative

importance seasonally and diurnally as environmental conditions

change, and represents a distinct competitive advantage for

opportunistic species.

Ciliate Importance in Phosphorus Regeneration

Phosphorus has long been considered the limiting nutrient for

freshwater phytoplankton productivity (Schindler 1977), and the

dynamics and transformations between trophic levels are recognized as

important determinants of the biomass and composition of

phytoplankton standing crops (Lean 1973; Lean and Nalewajko 1976).

Phytoplankton are the major excreters of phosphorus among the

freshwater plankton (Lean and Nalewajko 1976). Recent studies

indicate that bacterioplankton have significantly higher

orthophosphate uptake affinities compared to co-occurring

phytoplankton (Currie and Kalff 1984a, 1984b), and thus could

effectively limit algal growth by sequestering available phosphorus.












Moreover, bacteria possess higher absolute phosphorus assimilation

rates than competing phytoplankton cells at low phosphorus

concentrations (Currie and Kalff 1986). Conversely, bacterioplankton

are often carbon-limited and thus are closely linked to exuded carbon

metabolites from phytoplankton (Jones et al. 1983; Sondergaard et al.

1985). The phosphorus remaining after bacteria become carbon-limited

then determines in part phytoplankton growth (Currie and Kalff

1984a). Hamilton and Taylor (1984) suggested that phosphorus

dynamics are largely determined by the interdependence between

bacteria, protozoan grazers, and supply of dissolved organic

compounds.

It has been demonstrated in laboratory microcosms that bacterial

grazing by protozoa enhances phosphorus turnover and mineralization

(Barsdate et al. 1974; Fenchel and Harrison 1976). Increased

bacterial uptake and excretion of phosphorus occurred in systems with

protozoan grazers, and were primarily associated with increased

bacterial growth rates. However, these grazers contributed only

modestly to overall system excretion.

The activities of protozoan grazers increase the fraction of

organic phosphorus (Taylor 1984), and there are indications that

algae rely on this fraction for growth (Currie and Kalff 1984b).

Bacterial uptake of phosphorus is proportional to bacterial densities

but protozoan grazing pressure may enhance luxury phosphorus uptake

(Taylor 1984). Ciliate grazing alleviates nutrient limitation of

bacterial populations by preventing overexploitation of resources and

reducing density-dependent factors inhibiting bacterial metabolism












and growth. The nurturing of bacterial prey when grazed by protozoa

is probably related to the excretion of low molecular weight

compounds by the grazers, which are quickly utilized by the bacteria

(Taylor et al. 1985). Based on the above studies, organic phosphorus

excreted by protozoa may represent a substantial pathway for

phosphorus to be assimilated by phytoplankton (Figure 2-5).

Zooplankton excretion of phosphorus is a significant source of

nutrients for primary productivity (Lehman 1980; Ejsmont-Karabin

1983). Excretion rates in zooplankton are inversely proportional to

body weight. Numerous studies have suggested that the relatively

smaller body weight and higher metabolic rates of ciliated protozoa

should result in disproportionately higher excretion rates of

phosphorus (Johannes 1964, 1965; Buechler and Dillon 1974; Bartell

1981) when compared to larger crustaceans (Lehman 1980). Buechler

and Dillon (1974) estimated that if ciliated protozoa comprised only

1% of zooplankton biomass, then they could potentially process almost

50% of the total phosphorus being regenerated by the zooplankton

community.

Taylor (1984) suggested that if the size structure of

zooplankton communities shifts towards smaller forms during

eutrophication, the role of zooplankton as internal phosphorus sinks

should be reduced and would retard flow of phosphorus to higher

trophic levels. On a proportional basis, he reported that smaller

zooplankton species excrete the same amount of phosphorus as they

assimilate relative to larger zooplankton. Latitudinal differences

in the structuring of zooplankton communities exist such that the






























































Figure 2-5. Major pathways of phosphorus flux through the
planktonic microbial communities of lakes.











proportional contribution of ciliate biomass to total zooplankton

biomass progressively increases with lake productivity in the

subtropics (Bays and Crisman 1983) but does not markedly shift in

temperate lakes (Pace 1987).

Zooplankton communities dominated by larger forms will

accelerate export of epilimnetic phosphorus via several pathways.

Fecal pellets of large zooplankton may not fully decompose in the

epilimnion and thus settle from the photic zone where they remain

unavailable to phytoplankton until thermal overturn (Ferrante and

Ptak 1978). In addition, the diurnal migrations of some crustaceans

will produce a net loss of nutrients to the hypolimnion (Lampert and

Taylor 1985).

Taylor (1984) suggested that plankton communities dominated by

large-bodied zooplankton should have higher biomass compared to

small-bodied communities, and contribute more phosphorus for

phytoplankton utilization. Although zooplankton communities

dominated by small size classes cycle more phosphorus than those

composed of large species (Henry 1969), higher nutrient release rates

by ciliated protozoa may not provide sufficient phosphorus to supply

phytoplankton growth if their overall contribution to zooplankton

biomass is low.

Finally, Bartell (1981) concluded that the level of zooplankton

biomass determines phosphorus flux. The increase in phosphorus

release per unit body mass displayed by small-bodied taxa

consequently may be completely offset by reductions in total

zooplankton standing crops. As plankton community structure varies











with the level of productivity and latitude, so should the

proportional distribution of phosphorus among trophic levels (Taylor

1984).

Ciliate Importance in Nitrogen Regeneration

Comparatively few data are available on the assimilation and

excretion rates of nitrogen compounds by ciliated protozoa. It has

been assumed that the allometry described for phosphorus regeneration

by ciliates is similar for nitrogen excretion (Billen 1984).

Nannoplankton-sized protozoa flagellatess and ciliates) repeatedly

have been demonstrated to be major regenerators of nitrogen in marine

environments (Glibert et al. 1982; Taylor 1982; Goldman and Caron

1985; Sherr et al. 1986), thus providing strong evidence for a

positive predator feedback loop between protozoa and their bacterial

prey.

In freshwater systems, a significant portion of total primary

production flows through planktonic bacteria as dissolved organic

matter (Pedros-Alio and Brock 1982; Riemann 1983). It has been

assumed that variations in diel bacterial production are associated

with increased nutrient concentrations resulting from the feeding

activities of macrozooplankton (Lampert 1978; Copping and Lorenzen

1980). Riemann et al. (1986) reported that crustaceans significantly

increase the amount of dissolved free amino acids in solution, but

comparative data are not available for freshwater ciliated protozoa.

Caron et al. (1988) indicated that marine bactivorous ciliates

may be important in remineralization of nitrogen for phytoplankton

growth. Ciliate grazing activity is significant in alleviating











nutrient limitation of primary producers in circumstances in which

bacteria function as consumers of growth-limiting nutrients. In

situations where bacteria serve as nutrient sinks, the grazing

activities of ciliates remineralize nutrients for phytoplankton

growth. Therefore, the relative capacity of protozoan grazing

activities for nitrogen and phosphorus regeneration is greatest when

the assimilable bacterial substrates have a high C:limiting-nutrient

ratio (Caron et al. 1988).

Ciliate Importance in Carbon and Energy Flow

A substantial portion of the organic carbon fixed by algae

enters the planktonic food web as dissolved materials incorporated

into bacterial biomass (Williams 1981). Although most

macrozooplankton cannot effectively utilize bacterioplankton (e.g

Porter 1984), ciliates actively graze bacterioplankton standing crops

resulting in rapid turnover of prey populations but maintenance of

relatively constant bacterial numbers (105-106 cells/ml) (Azam et

al. 1983). Protozoa may regulate bacterial standing stocks and

influence phytoplankton through grazing activities and release of

nutrients (Sherr and Sherr 1984).

The precise role of protozoa in energy transfer remains

speculative. They may function as a pivotal intermediary to

transform ultrafine organic carbon into larger particles available to

macrozooplankton (Sherr and Sherr 1987; Sherr et al. 1988). It is

significant that bacteria probably utilize refractory carbon

otherwise lost from the food chain and thereby rechannel it into the

food web. As a result, some of the carbon initially fixed by


































































Figure 2-6. Upward movement of DOC/POC in the pelagic food web.
All components contribute DOC/POC to the pool (modified from
Porter 1979).












phytoplankton and lost via exudation must return to the food web by

ciliated protozoan grazing (Figure 2-6).

Conversely, protozoa may divert much of the primary and

secondary productivity from higher trophic levels via CO2 respiration

and lengthened food chains. Smaller organisms have higher

assimilation efficiencies than larger organisms and transfer energy

very efficiently to the next trophic level (Williams 1981).

However, from the previous discussion it is apparent that these

food webs may be longer and more convoluted than classical food

chains, and may actually increase the amount of energy dissipated

despite higher transfer efficiencies. Pomeroy and Wiebe (1988)

presented compelling evidence for the inefficiency of a marine food

web based on bacterial biomass. The trophic link between freshwater

ciliates and crustaceans has not been documented in situ, and further

research is needed to quantify accurately the energetic and carbon

flow through ciliated protozoa to crustacean zooplankton.

















CHAPTER III
COMMUNITY STRUCTURE OF PLANKTONIC CILIATES IN FLORIDA LAKES

Introduction

Microzooplankton abundance and biomass are important

determinants of zooplankton production (Downing 1984) and community

structure (Bays and Crisman 1983). Quantitative predictions of

zooplankton biomass can be made from indices of lake trophy, and

numerous studies indicate that ciliated protozoa constitute a

significant portion of the zooplankton community (Pace and Orcutt

1981; Bays and Crisman 1983; Pace 1986). The smaller size and higher

metabolic rate of ciliates dictate a substantial role in nutrient

regeneration within the water column (Buechler and Dillon 1974;

Taylor and Lean 1981), but only recently have protozoa been

considered as a major link in the limnetic food web (Porter et al.

1979). Unfortunately, the taxonomic shifts within the ciliated

microzooplankton community associated with increasing eutrophication

have been described only generally (Beaver and Crisman 1982), and

their importance in food chain dynamics remains speculative (Porter

et al. 1985).

The purpose of this research was to provide a detailed

understanding of the community structure of pelagic ciliate

populations relative to lake trophic state. I investigated the

abundance and biomass of ciliate taxa using data from 30 Florida












lakes spanning the trophic gradient from acidic oligotrophic to

hypereutrophic.

Methods

Thirty study sites were chosen throughout penisular Florida

representing a wide range of trophic, chemical, and morphometric

conditions (Tables 3-1 and 3-2). Twenty of the lakes were sampled

monthly during 1979 and ranged from nonacidic oligotrophic to

hypereutrophic (Beaver 1980). The remaining ten lakes were sampled

quarterly and were characterized as acidic oligotrophic based on mean

annual pH (Brezonik et al. 1984).

Chlorophyll a and nutrient analyses were performed using

standard techniques (APHA 1982). Samples for chemistry and ciliates

were taken from a composite of the water column.

Water samples were collected at 1 m intervals from the surface

to the bottom (exclusive of the sediments) with a 2 L Kemmerer bottle

and pooled. Subsamples (76 ml) were withdrawn from this composite,

stained with 1 drop 0.1% bromophenol blue, and preserved with 2 ml

saturated HgCl2. Enumeration employed the Utermohl technique (Lund

et al. 1958) and identification followed Kahl (1930-1935), Maeda and

Carey (1985), and Maeda (1986). Biovolumes of individual taxa were

estimated from cell dimensions assuming that ciliate shapes

approximate lengthened spheroids. These estimates were then

converted to dry weights utilizing the 0.279 pg/um3 conversion factor

(Gates et al. 1982).

Data on ciliate abundance and biomass (Pace 1986) and

chlorophyll a (Pace 1984) for a suite of Quebec lakes were used for















Table 3-1. Morphometric characteristics of study lakes used to
assess community structure of ciliated protozoa.a


Number County


Surface Area
(Hectares)


Mean Depth
(Meters)


Anderson-Cue
Annie
Blue Cypress
Brooklyn
Cowpen
E. Tohopekaliga
Eustis
Francis
Galilee
Geneva
Jackson
Johnson
Kerr
Kingsley
Lowery
McCloud
Magnolia
Miona
Newnans
Ocean Pond
Panasoffkee
Placid
Sampson
Santa Fe
Santa Rosa
Scott
Sheeler
Thonotosassa
Washington
Wauberg
Weir


Putnam
Highlands
Indian River
Clay
Putnam
Osceola
Lake
Highlands
Putnam
Clay
Highlands
Clay
Marion
Clay
Clay
Putnam
Clay
Sumter
Alachua
Baker
Sumter
Highlands
Bradford
Bradford
Putnam
Polk
Clay
Hillsborough
Brevard
Alachua
Marion


a modified from Beaver (1980)


Lake


59
35
2653
261
236
4843
3159
218
34
660
1381
194
1145
669
511
6
83
169
3006
718
1805
1344
826
1911
44
115
7
331
1765
100
2301


2.0
8.3
1.6
5.7
3.7
2.8
4.1
2.9
3.5
4.1
2.9

4.6
7.3
4.8
2.0
8.0
-
1.5
2.6
2.1
6.1
1.9
5.5
8.1

5.7
2.5

3.8
6.3
















Table 3-2. Mean values for selected limnological variables for
study lakes used to assess community structure of ciliated
protozoa.a


Lake Number


Chl. a


TP TN Color Secchi Disk


(mg/m3) (mg/m3) (mg/m3)


2.8
2.3
3.3
3.0
1.2
9.8
41.9
12.1
2.9
2.0
4.1
2.5
1.5
3.1
1.1
0.9
1.1
14.8
65.4
3.6
6.1
8.2
6.0
7.8
2.2
71.6
1.0
71.1
5.2
95.1
9.0


40
11
82
11
11
50
78
38
18
25
34
14
25
33
8
16
10
98
115
55
64
41
65
57
14
176
7
582
54
215
52


830
410
1310
200
160
1000
2330
550
250
400
640
260
650
560
240
430
170
1680
1990
550
930
600
790
580
210
2010
190
2160
1730
2500
840


(Pt units)


73
25
247
12
9
61
30
21
19
12
11
31
9
10
12
15
14
35
163
74
57
9
132
56
10
28
5
128
227
45
9


a modified from Beaver (1980)


(meters)


1.0
4.6
0.8
2.8
3.0
1.4
0.5
1.9
2.6
3.2
2.9
1.4
3.5
3.9
3.3
3.8
5.2
0.9
0.6
1.0
1.5
2.2
1.3
2.2
5.9
0.5
7.9
0.5
0.8
0.5
2.0


4.9
5.9
5.8
5.0
4.8
6.3
8.3
6.7
5.0
6.4
6.5
5.2
6.3
6.7
5.2
4.7
5.1
7.3
7.0
5.2
7.9
6.3
6.7
5.8
5.1
8.2
5.1
8.1
7.0
7.4
7.0












comparing the response of ciliate populations to increased

eutrophication in north temperate lakes with my comparable data set

for subtropical lakes. As in Pace (1986), ciliate biomass

was calculated by applying a 0.279 pg/um3 dry weight conversion

factor (Gates et al. 1982). All abundance and biomass values were

based on annual means. Statistical operations were performed using

SAS (1985) and CLUSTAN (Wishart 1979) computer packages.

Results and Discussion

Abundance and Biomass Regression Models

The study lakes were classified to trophic state based on mean

annual chlorophyll a, with the oligotrophic subset subdivided on the

basis of pH (Beaver and Crisman 1981).

Mean annual abundance and biomass of all ciliate components in

Florida lakes displayed highly significant (p <0.01) regressions

against chlorophyll a with a moderate to large amount of the

variation being explained by the models (Table 3-3). Abundance

showed a better relationship (r2= 0.69-0.85) than did biomass (r2=

0.40-0.84). Total ciliate abundance was strongly related to

2
chlorophyll a (r = 0.85) as was the biomass of small (<30 microns)

2
ciliates (r = 0.84). Regressions of the various ciliate components

against total phosphorus produced similar results, but the

relationship was weaker for both biomass (r2= 0.35-0.75) and

abundances (r = 0.35-0.42).

Pace (1986) derived regression equations for a comparable data

set from Quebec lakes. Application of the regression equations just

described for Florida lakes to his data set overpredicted both

















Table 3-3. Summary of regression models for ciliate abundance and
biomass using chlorophyll a and total phosphorus as independent
variables (n=30, p<0.01, x= logl0 chl. a or TP, y= loglO ciliate
component).






ABUNDANCE Chlorophyll a r2 Total Phosphorus r2


Total y= 0.82x + 3.62 0.85 y= 0.74x + 3.11 0.41

Large (>30 um) y= 0.53x + 3.33 0.75 y= 0.52x + 2.94 0.42

Small (<30 um) y= 1.00x + 3.17 0.73 y= 0.94x + 2.49 0.38

Haptorida y= 0.93x + 2.75 0.69 y= 0.89x + 2.09 0.37

Scuticociliatida y= 2.09x + 1.53 0.69 y= 1.52x + 1.49 0.42

Oligotrichida y= 0.55x + 3.42 0.75 y= 0.49x + 3.09 0.35




BIOMASS


Total y= 0.68x + 1.24 0.67 y= 0.80x + 0.49 0.54

Large (>30 um) y= 0.61x + 1.18 0.58 y= 0.62x + 0.70 0.35

Small (<30 um) y= 1.02x + 0.18 0.84 y= 0.98x 0.54 0.46

Haptorida y= 0.86x + 0.07 0.40 y= l.llx 0.97 0.40

Scuticociliatida y= 1.37x 0.80 0.78 y= 1.89x 2.82 0.75

Oligotrichida y= 0.57x + 0.93 0.67 y= 0.65x + 0.38 0.51














abundance (Figure 3-1) and biomass (Figure 3-2). Comparison of the

model slopes for abundance and biomass did not indicate a significant

difference between studies, but the slopes for abundance did approach

significance (p <0.07). The intercepts in both studies were not

significantly different for either biomass or abundance. Confidence

intervals for predicted abundance overlapped in the oligotrophic

range but departed for mesotrophic lakes, thus indicating possible

latitudinal differences in the response of ciliate communities to

increased lake productivity.

Both studies used comparable methodologies, although the

equations derived for Quebec lakes were based on ciliates collected

during the growing season from a limited number of basins (n= 12)

representing a more restricted range of trophic conditions

(chlorophyll a= 1-29 mg m-3). The disparity in the predictive

ability of the equations for abundance may reflect fundamental

ecological differences between northern temperate and subtropical

Florida lakes. These results provide evidence contrary to the

suggestion of Pace (1986) that the size structure of zooplankton

communities does not change with increasing trophic state. These

regression equations and others derived for Florida lakes (Bays and

Crisman 1983) clearly indicate that limnetic ciliated protozoa

decrease in size with eutrophication. Obviously both sets of

equations do not appear to have widespread geographical applicability

unless the relationship between latitude and ciliate communities can

be further elucidated.





















105


104


.0


- ~-


CHLOROPHYLL (mg/m3)

















Figure 3-1. Comparison of regression equations for total ciliate
abundance in Quebec (open) and Florida (solid) lakes. Dashed lines
represent 95% confidence intervals. Quebec: loglOTA= 0.54(loglOChl)
+ 3.55; Florida: loglOTA= 0.82(loglOChl) + 3.62.


1






















* 0*


* 0*


0 000
000*


CHLOROPHYLL


(mg/m3 )


Figure 3-2. Comparison of regression equations for total ciliate
biomass in Quebec (open) and Florida (solid) lakes. Quebec: loglOTB=
0.49(loglOChl) + 1.07; Florida: loglOTB= 0.68(loglOChl)
+ 1.24.


1000 -


100 -


10 -












Species Number and Community Composition

In order to evaluate overall trends in taxonomic composition,

total species richness and Shannon-Weaver diversity indices were

calculated for each lake (Figure 3-3). Species number increased with

trophic state with acidic oligotrophic lakes being significantly

lower (ANOVA, p<0.05) than all other lake groups. This subgroup had

a mean number of species of 10.8 (Extremes 8-13) compared to 18.2

(Extremes 16-21) for nonacidic oligotrophic lakes. At the opposite

end of the trophic spectrum, the hypereutrophic group exhibited a

mean of 24.5 species (Extremes 21-27). Duncan's multiple range

test indicated that the lake groups on the extremes of the trophic

spectrum (acidic oligotrophic and hypereutrophic) contained

significantly different (p <0.05) numbers of species compared to the

remainder of the lakes.

Shannon-Weaver indices followed the same pattern with a general

increase along trophic lines. The mean value for hypereutrophic

lakes (2.82) was significantly higher (ANOVA, p<0.05) than both

oligotrophic classifications (OA= 1.53, ON= 2.22). Ciliate diversity

in the acidic oligotrophic lakes was significant different from all

other trophic categories. A number of factors can influence

diversity indices calculated for ciliated protozoan communities

including sample size and, although undocumented, differential

preservation of taxa. While the sample size utilized in the present

study (150-200/sample) may have missed some of the rarer taxa, this

does not diminish the significance of the diversity trends

established relative to trophic state.
















I

Z
Z



m
00
z







o


10 1.0
w 0
O m

0 0


'rl



cl I w X



OA ON M E H












Figure 3-3. Mean Shannon-Weaver diversity indices and number of
species grouped by trophic classification (OA= acidic
oligotrophic, ON= nonacidic oligotrophic, M= Mesotrophic, E=
eutrophic, H= hypereutrophic).












Brezonik et al. (1984) determined that these same acidic lakes

also displayed reduced phytoplankton abundance, diversity, and number

of species compared to a nonacidic lake group. Unlike ciliated

protozoa, crustaceans and rotifer zooplankton communities in these

acidic lakes showed no significant difference in species diversity

compared to nonacidic lakes. Although they reported reduced

zooplankton abundance with pH, it was concluded that lake

productivity influenced zooplankton abundance, biomass and

composition more than pH per se. It is unlikely that the observed

changes in ciliate composition and size with increasing

eutrophication are due directly to physiochemical exclusion, as most

ciliates are extremely tolerant of the range of conditions found in

freshwater lakes (Bick 1972).

Hierarchical cluster analysis of the mean species abundance data

of each lake produced three lake groups roughly corresponding to

trophic classifications based on chlorophyll a (Figure 3-4). Cluster

I consisted of the ten acidic lakes plus four of the nonacidic

oligotrophic lakes, and contained two smaller clusters, one of which

was exclusively acidic lakes. All of the mesotrophic lakes were

classified into Cluster II along with two of the more productive

oligotrophic lakes (Nos. 11 and 14). Eutrophic and hypereutrophic

systems comprised Cluster III and, as indicated by the coefficient of

similarity, displayed significantly different ciliate assemblages

compared to less productive lakes. Therefore, the hierarchical

cluster analysis based on strictly biological data demonstrates







































3 6


30
28
302--------------------------6


A-


Figure 3-4. Hierarchical cluster analysis of study lakes based

on log-transformed mean abundance of the 23 dominant ciliate

taxa. Coefficient is similarlity type (taken from Beaver 1980).


I _














the relationship between lake trophic state and taxonomic composition

of ciliate communities.

Indicator Taxa

Based on presence-absence data (Tables 3-4, 3-5, 3-6, 3-7), an

ubiquitous ciliate assemblage was detected and consisted of Urotricha

farcta (Protostomatida), Holophyra simplex (Protostomatida),

Mesodinium pulex (Haptorida), Strombidium viride (Oligotrichida), and

Cyclidium glaucoma (Scuticociliatida). These taxa were found in all

survey lakes, were frequently numerically dominant, and with the

exception of the oligotrich were <30 microns in length. Other taxa

widely distributed included Askenasia faurei (Haptorida), Halteria

cirrifera (Oligotrichida), and Cyclidium citrullus

(Scuticociliatida). These taxa were rarely dominant, and their

appearance was usually limited to seasonal occurrences.

Of the 23 dominant taxa, some displayed restricted distribution

along the trophic gradient (Tables 3-4, 3-5, 3-6, 3-7). The taxa

largely restricted to the more productive situations were Plaqiopyla

nasuta (Trichostomatida), Litonotus fasciola (Pleurostomatida),

Dileptus anser (Haptorida), Cvclotrichium limneticum (Haptorida), and

Paramecium trichium (Hymenostomatida). All of the organisms in this

group were among the largest ciliates (ca. 100 microns) encountered

during the survey. Frequently, their occurrence coincided with peaks

in total ciliate abundance and diversity in midsummer and because of

their size contributed heavily to the biomass peaks in productive

systems.











Table 3-4. Distribution of the 23 dominant ciliate taxa in acidic
oligotrophic lakes. X= ciliate taxon found in lake one at least one
occasion.


Lake No. 16

Taxon

Urotricha farcta X

Holophyra simplex X

Mesodinium pulex X

Strobilidium humile X

Strombidium viride X

Cyclidium glaucoma X

Askenasia faurei X

Tintinnidium fluviatile

Halteria cirrifera

Cyclidium citrullus X

Coleps hirtus

Spathidium sp. X

Didinium nasutum X

Strombidium cf oculatum

Cinetochilum margaritaceum X

Vorticella microstoma

Uronema niqracans

Plaqiopyla nasuta

Litonotus fasciola

Dileptus anser

Paramecium trichium

Cyclotrichium limeticum

Stentor niqer


27 17 15 5 1 25 12 9 4


X


X X X X


X X










Table 3-5. Distribution of the 23 dominant ciliate taxa in nonacidic
oligotrophic lakes. X indicates ciliate taxon found in lake on at
least one occasion.

Lake No. 13 10 2 14 3 20


Taxon

Urotricha farcta

Holophyra simplex

Mesodinium pulex

Strobilidium humile

Strombidium viride

Cyclidium glaucoma

Askenasia faurei

Tintinnidium fluviatile

Halteria cirrifera

Cyclidium citrullus

Coleps hirtus

Spathidium sp.

Didinium nasutum

Strombidium cf oculatum

Cinetochilum margaritaceum

Vorticella microstoma

Uronema niqracans

Plaqiopyla nasuta

Litonotus fasciola

Dileptus anser

Paramecium trichium

Cyclotrichium limneticum

Stentor niqer


X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X


X X
x x










Table 3-6. Distribution of the 23 dominant ciliate taxa in mesotrophic
lakes. X indicates ciliate taxon found in lake on at least one
occasion.


Lake No.

Taxon

Urotricha farcta

Holophyra simplex

Mesodinium pulex

Strobilidium humile

Strombidium viride

Cyclidium glaucoma

Askenasia faurei

Tintinnidium fluviatile

Halteria cirrifera

Cyclidium citrullus

Coleps hirtus

Spathidium sp.

Didinium nasutum

Strombidium cf oculatum

Cinetochilum marqaritaceum

Vorticella microstoma

Uronema niqracans

Plaqiopyla nasuta

Litonotus fasciola

Dileptus anser

Paramecium trichium

Cyclotrichium limneticum


11 29 23 22 24 31 6 8


X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

X X

x
X

X X

X


X X


X

X X


Stentor niger







56



Table 3-7. Distribution of the 23 dominant ciliate taxa in
eutrophic/hypereutrophic lakes. X indicates ciliate taxon found
in lake on at least one occasion.


Lake No.

Taxon

Urotricha farcta

Holophyra simplex

Mesodinium pulex

Strobilidium humile

Strombidium viride

Cyclidium glaucoma

Askenasia faurei

Tintinnidium fluviatile

Halteria cirrifera

Cyclidium citrullus

Coleps hirtus

Spathidium sp.

Didinium nasutum

Strombidium cf oculatum

Cinetochilum margaritaceum

Vorticella microstoma

Uronema niqracans

Plaqiopyla nasuta

Litonotus fasciola

Dileptus anser

Paramecium trichium

Cyclotrichium limneticum

Stentor niger


7 19 28 26 30


X

x
X

X X

X












The largest planktonic ciliate (150-200 microns) found in any

abundance was Stentor niger (Heterotrichida), and it was almost

exclusively limited to acidic oligotrophic lakes with little organic

color. Kawakami (1984) reported that this species is positive

phototactic and contains zoochlorellae. All of the specimens of S.

niger I observed were densely packed with algal symbionts.

Additionally, this species is quite delicate and complete

identification requires collection of live specimens. Because of its

immense size, it contributed an average of 64% of total ciliate

biomass in those acidic oligotrophic lakes in which it occurred.

Based on intense monitoring of one of these acidic lakes (Lake

McCloud), it is apparent this myxotrophic ciliate is a major

component of the total zooplankton community and is frequently found

in metalimnetic plates of intense autotrophic and heterotrophic

activity (Bienert et al. 1990). Consequently, S. niger may have a

dramatic effect on food chain dynamics in these nutrient poor

systems.

To determine which of the above common ciliate species were the

best indicators for assessing trophic conditions, the F-statistic was

calculated (the ratio of the among groups to within groups variance

of log abundance). The F-statistic is not a formal test of

significance, but an index of the degree of class definition by each

taxon (see Green 1979 for discussion). The mean abundance of each

species increased with trophic state with the exception of Holophyra

simplex which was more numerous in acidic versus nonacidic












oligotrophic systems and Coleps hirtus which was less numerous in the

eutrophic subset compared to the mesotrophic group (Table 3-8).

Vorticella microstoma and M. pulex are the best ciliate taxa for

assessing trophic state of Florida lakes. They are almost

nonexistent in acidic lakes and steadily increase with

eutrophication, although they only comprise an average of 1.5% and

15% of the total ciliate population for all lakes, respectively.

Stepwise multiple regression using chlorophyll a as the dependent

variable and species abundance as the independent variables produced

similar results with V. microstoma (p <0.01) and M. pulex (p <0.01)

abundances explaining most (r2= 0.92) of the variation in the model.

Lake Panasoffkee (Marion Co.) was excluded from the above

analysis and by Beaver (1980). During 1979 this lake had a large

coverage of submersed macrophytes, primarily Vallisneria sp., and had

a very short water residence time (0.20 years). The 30 lakes used to

determine ciliate community characteristics did not have the extent

of macrophyte coverage nor the short water retention time of Lake

Panasoffkee. Additionally, water clarity was high and Secchi disk

readings were frequently made to the lake bottom. These

characteristics were used to exclude this lake from these analyses,

however, for comparative purposes I will discuss the ciliate

community of Lake Panasoffkee.

Water column conditions in Lake Panasoffkee during 1979

indicated that the phytoplankton community was moderately productive

(chlorophyll a= 6.1 mg m3, TP= 64 mg m-3, TN= 930 mg m-3) and that

the lake was somewhat colored (57 Pt units). Ciliate abundance (39

















Table 3-8. Best ciliate indicator taxa for lake trophic state in
Florida lakes based on F-statistic. Values represent mean numbers
of individuals/L within each trophic classification. Lake key: OA=
Acidic oligotrophic, ON= Nonacidic oligotrophic, M= Mesotrophic, E=
Eutrophic, H= Hypereutrophic.


F (pr.)
Taxa (4,25 dF)


OA ON
(n=10) (n=6)


M E H
(n=8) (n=2) (=4)


Vorticella microstoma 232

Mesodinium pulex 78

Strobilidium humile 52

Holophyra simplex 52


60 420 3100 6800


550 1500 4500 5200 25300

680 2800 5900 14000 26800

190 720 2000 4500 13800


Coleps hirtus


28 <10


10 200


10 3300


20 50 250 860 2300


Spathidium sp. (<30um)













cells ml-1) and biomass (96 mg d.w. m-3) were comparable to other

mesotrophic lakes discussed in this chapter (mean abundance= 28 cells

ml mean biomass= 91 mg d.w. m-3). The annual percentage

composition of the ciliate community in Lake Panasoffkee (71% .pa

oligotrichs, 10% scuticociliates) was clearly different from other

mesotrophic lakes (average oligotrichs= 33%, average scuticociliates=

30%), and was more closely aligned with nonacidic oligotrophic lakes

(mean oligotrichs= 53%, mean scuticociliates= 10%). As will be

discussed in the following chapter, the reduced importance of

scuticociliates in Lake Panasoffkee is likely related, in part, to a

lack of thermal stratification in this shallow lake (mean depth= 2.1

m) with short hydraulic residence time.

Canfield et al. (1984a) have underscored the importance of

considering the nutrient concentrations present in macrophyte biomass

when evaluating lake trophic state. It is likely the nutrient

concentrations present in Lake Panasoffkee would be considerably

greater if the nutrients sequestered by submerged macrophytes were

taken into account. Thus, the planktonic ciliate community of Lake

Panasoffkee must be considered atypical when contrasted with other

Florida lakes with less macrophyte coverage and longer water

retention times.

My results indicate that the various components of planktonic

ciliate populations in Florida lakes are strongly related to lake

trophic state. Abundance and biomass of the total ciliate community,

dominant taxonomic orders, and the two size classes all increased

predictably along trophic lines. However, a marked latitudinal














difference existed in annual mean ciliate abundance per unit

chlorophyll. Subtropical lakes (Florida) had considerably higher

ciliate abundance at a given level of trophy than comparable

temperate lakes (Quebec) in the mesotrophic and eutrophic range.

In addition, there were also compositional shifts as the

Oligotrichida dominance in oligotrophic systems shifted to

Scuticociliatida dominance at higher trophic states. This coincided

with small (<30 microns) ciliates constituting a large percentage of

the community at higher trophic states (Beaver and Crisman 1982).

The species-assemblage group of very large ciliates detected in the

most productive lakes is likely evidence of higher quantity and

variety of food sources. The number of species was significantly

reduced in acidic lakes, but this is probably a response to food

limitation rather than physiological exclusion (Beaver and Crisman

1981). This trend is also reflected in the Shannon-Weaver indices as

there may be fewer niches in the oligotrophic systems and more food

niches in the species rich hypereutrophic lakes.
















CHAPTER IV
SEASONALITY OF PLANKTONIC CILIATES IN FLORIDA LAKES

Introduction


Recent investigations have demonstrated a highly significant

relationship between the abundance and biomass of planktonic ciliated

protozoa and lake trophic state, as measured by chlorophyll a and

total phosphorus (Beaver and Crisman 1982; Pace 1986). However, the

seasonal dynamics of planktonic ciliates remain poorly understood.

Most studies have been confined to the temperate zone (Pace 1982;

Hunt and Chen 1983; Gates 1984; Gates and Lewg 1984), and detailed

data for a trophic gradient of lakes within the same geographical

regions are clearly lacking. Several investigators in the temperate

region have suggested that temporal changes in ciliate populations

are due to availability of food resources. These resources can be

spatially enhanced by intense microbial activity in the hypolimnion

associated with thermal stratification (Pace and Orcutt 1981; Pace

1982; Psenner and Schlott-Idl 1985).

Florida lakes deeper than five to six meters are clearly warm

monomictic and stratify during the warmest part of the year (March-

September), with shallower lakes normally being holomictic throughout

the year (Beaver et al. 1981). In this study, the average maximum

depths of the oligotrophic and mesotrophic subsets were greater than

seven meters and less than five meters in the more productive lakes.

Deeper, less productive, systems were usually stratified during the












spring-summer period. In contrast, shallower productive lakes

periodically experienced holomictic events during the normal time of

stratification due to changes in meteorological conditions.

This research examined the seasonal distribution of planktonic

ciliate abundance, biomass and composition in 20 subtropical Florida

lakes constituting a broad trophic gradient. The influences of

trophic state and thermal regimes on the seasonal dynamics of

planktonic ciliate components are discussed.

Methods

The names and locations of the study lakes are provided in

Beaver (1980). Biological and chemical samples were collected

monthly from 20 Florida lakes between January and December 1979.

Enumeration and biomass estimation of ciliates was described in

Chapter III. Trophic state assessment of the study lakes was based

on Carlson's (1977) trophic state index using chlorophyll a and

produced 4 trophic categories--oligotrophic (n= 6), mesotrophic

(n= 8), eutrophic (n= 2), and hypereutrophic (n= 4).

Temperature profiles were taken at 1-meter intervals, and the average

for the water column was used as the monthly value for statistical

calculations.

All statistical analyses utilized the SAS (1985) computer

package. Prior to analyses, plankton counts were normalized by a log

10(n + 1) transformation. Temporal relationships between plankton

components and environmental variables were evaluated in two ways.

First, simple correlations were computed between the variables.

Second, the variability associated with pooling data spanning one to












two orders of magnitude was reduced by regressing residuals for the

dependent variables against the independent variables. Independent

variables were evaluated for collinearity (SAS 1985). Multiple

linear regression models were selected based on the C statistic

(Freund and Minton 1979). The C statistic is a function of the

total number of variables, total number of points and the error mean

square. It is a scaleless quantity, and is particularly useful in

determining overfitted (redundancy) and underfitted (too few

variables). Multiple linear regression was performed on select

models after the above evaluation.

The two approaches outlined above were used in assessing

temporal dynamics of ciliates in this chapter and also applied in

Chapter V (colored lake ciliates), Chapter VI (bacterioplankton) and

Chapter VII (primary productivity). Given that plankton

characteristics are dynamic, the selection of these statistical

procedures was predicated on the assumption that each sampling event

represented an experimental unit.

Results

Abundance and Biomass of Total Ciliate Populations

Oligotrophic lakes generally displayed pronounced abundance

(Figure 4-1) and biomass (Figure 4-2) peaks of total ciliates at the

onset of fall mixis. Several of these systems also experienced

ciliate pulses either near the end of winter or during summer. The

highest ciliate concentration (45 ciliates ml-1) and biomass (174

-3
mg d.w. m ) in the oligotrophic subset occurred in Lakes Kingsley

and Jackson, respectively.
















OLIGOTROPHIC


F A J A 0 D


EUTROPHIC


200



100


F A J A O D


F A J A 0 D


HYPEREUTROPHIC


F A J


A 0 D


Figure 4-1. Seasonality of total ciliate abundance in Florida lakes.
Values represent monthly means (cells/ml) within trophic
classifications.


MESOTROPHIC

















OLIGOTROPHIC


F A J A 0 D


EUTROPHIC


I- A J


1500


1000


500


A 0 D


MESOTROPHIC


I- A J A 0 D


HYPEREUTROPHIC


F A J


A 0 D


Figure 4-2. Seasonality of total ciliate biomass in Florida lakes.
Values represent monthly means (mg d.w./cubic meter) within trophic
classifications.


150


100


50












Typically, mesotrophic lakes displayed a bimodal seasonality in

abundance and/or biomass with ciliate peaks occurring in the spring

and fall, corresponding to the development of stable thermal

stratification and destratification, respectively. Exceptions to

this trend included Lakes Washington and Santa Fe which did not

display spring peaks. The greatest abundance and biomass values for

mesotrophic waters were noted in the most productive mesotrophic lake

(86 cells ml-1, 410 mg d.w. m-3)--East Lake Tohopekaliga.

A similar bimodality in ciliate abundance and biomass was

detected for eutrophic and hypereutrophic systems, but the maxima

occurred during the winter and summer. The main biomass pulse

consistently occurred during the summer months with the exception of

Lake Miona, the shallowest lake (maximum depth= 2.0 m). Scott Lake

had the highest concentration of total ciliates (356 cells ml-1) and

biomass value of any survey lake (4410 mg d.w. m 3) which was

attributable to a bloom of Paramecium trichium (Hymenostomatida) and

Plaqiopyla nasuta (Trichostomatida). Since these protozoa were

relatively large-sized, they also contributed greatly to the

midsummer biomass peaks in other hypereutrophic systems and were

usually associated with periods of highest abundance of total

ciliates and scuticociliates (Figure 4-3). The mass occurrence of

these ciliate species was limited to hypereutrophic lakes (annual

mean chlorophyll a >65 mg m-3) and they were only rarely encountered

in lakes of lower trophic state.



















NEWNANS


400



200


F A J A 0 0


4000



2000


A J
FAJ


THONOTOSASSA


2000



1000


WAUBERG


400



200


F A J A O D


Figure 4-3. Contribution of the combined biomass of Plaqiopyla
nasuta and Paramecium trichium (filled area) to total ciliate biomass
(solid line) in the hypereutrophic lakes. Biomass expressed in
mg d.w./cubic meter.


SCOTT


A O D












Seasonality of Dominant Ciliate Orders

Oligotrophic systems characteristically exhibited population

pulses dominated by the Oligotrichida (Figure 4-4). The highest

value recorded was 22 oligotrichs ml-1 in Lake Kerr during September.

Generally oligotrich populations peaked during the fall coincident

with thermal overturn, but several lakes recorded increased

representation of this ciliate order during other seasons. Members

of the Haptorida and Scuticociliatida, although poorly represented in

oligotrophic waters, peaked simultaneously with oligotrich

populations (Figure 4-5).

Abundance maxima in mesotrophic lakes were almost exclusively

dominated by scuticociliates. Population levels of this order were

usually depressed throughout the winter months, but rose during the

late spring and early summer (>20 scuticociliates ml-1) after the

development of stable thermal stratification. Following the initial

spring rise, populations declined during summer months but remained

at levels above those of winter. A final maxima of short duration

occurred during overturn.

The seasonality of the Oligotrichida in mesotrophic lakes was

not as distinct as that of the Scuticociliatida, but there are

indications that oligotrichs increased moderately during the spring

prior to or concurrent with the scuticociliate blooms. Like the

scuticociliates, oligotrichs tended to be at their lowest levels

during the winter season. Haptorid populations generally peaked

during autumn, but individual lakes recorded peaks throughout the

year.



















OLIGOTROPHIC










F A J A 0 D




EUTROPHIC











F A J A 0 D


MESOTROPHIC


F A J A 0 D


HYPEREUTROPHIC


F A J A 0 D


Figure 4-4. Seasonality of the Oligotrichida (open cirlces) and
Scuticociliatida (closed circles) in Florida lakes. Values represent
means (cells/ml) within trophic classifications.



















OLIGOTROPHIC


FA JA D

F A J A 0 0




EUTROPHIC










F A J A


MESOTROPHIC


F A J A 0 D




HYPEREUTROPHIC










F J A 0


Figure 4-5. Seasonality of the Haptorida in Florida lakes.
represent means (cells/ml) within trophic classifications.


Values












Ciliate pulses in the most productive lakes were usually

dominated by the scuticociliates with population levels of this order

reaching >100 ml-1 in several instances (Figure 4-4). In many cases

the scuticociliate blooms occurred exclusively during midsummer, but

very shallow unstratified lakes had blooms during other seasons.

Distinctive patterns for the Oligotrichida and Haptorida in

eutrophic-hypereutrophic lakes were not readily discernible, but

there was a slight tendency for oligotrich populations to decrease

somewhat during both spring and late summer and for the Haptorida to

increase during the spring and fall.

Relationship between Environmental Variables and Ciliate Populations

Major ciliate components were positively correlated with periods

of higher productivity as measured by chlorophyll a, total nitrogen,

and total phosphorus (Table 4-1). The abundance and biomass of total

ciliates and small ciliate abundance were the most strongly

correlated components with chlorophyll a (Table 4-1). All components

displayed a weak positive correlation with temperature with the

exception of Haptorida. The relationship between temperature and

ciliate groups was considerably improved if the oligotrophic and

mesotrophic subsets were removed from the analysis, suggesting

temperature may have a stronger effect on shallow productive lakes.

An analysis of collinearity indicated that total phosphorus,

total nitrogen, and chlorophyll a were all collinear in this data

set. The best univariate regression models were based on chlorophyll

a for total ciliate biomass (r2= 0.48), oligotrich biomass (r2=

0.21), haptorid biomass (r 2= 0.07), and scuticociliate biomass (r =





















Table 4-1. Significant correlations (p <0.01) between limnological
variables and major ciliate components. Correlation coefficients are
Pearson product-moment type.




Chl. a TP TN Temperature


Ciliate Component


Total ciliate abundance 0.84 0.55 0.55 0.26

Total ciliate biomass 0.71 0.53 0.42 0.20

Haptorid abundance 0.59 0.40 0.27 NS

Haptorid biomass 0.28 0.21 NS -0.13

Oligotrich abundance 0.70 0.52 0.44 0.30

Oligotrich biomass 0.47 0.46 0.22 0.23

Scuticociliate abundance 0.74 0.50 0.54 0.30

Scuticociliate biomass 0.72 0.56 0.54 0.29

Small ciliate abundance 0.82 0.54 0.57 0.29

Small ciliate biomass 0.84 0.58 0.60 0.28

Large ciliate abundance 0.65 0.46 0.38 0.18

Large ciliate biomass 0.57 0.45 0.29 0.15












0.53). Little additional variance was accounted for by including

terms for either TP or TN.

Discussion

Seasonal cycles for planktonic ciliate abundance and composition

previously have been described quantitatively for only a few lakes

(Nauwerck 1963; Mamaeva 1976; Hecky et al. 1978; Pace and Orcutt

1981). The seasonality of planktonic ciliates in oligotrophic

Florida lakes is consistent with patterns noted for comparable

tropical and temperate systems. Mamaeva (1976) and Hunt and Chen

(1984) both recorded oligotrich peaks during the fall months at the

time of overturn. Gates (1984) reported a ciliate biomass maximum

during the early spring and late summer in a temperate oligotrophic

lake and noted a significant but weak correlation of ciliate biomass

with nutrient concentrations. In deep oligotrophic tropical lakes,

Lewis (1985) and Hecky et al. (1978) both recorded primary pulses in

ciliate abundance and biomass in the fall with a secondary peak

during late winter. The seasonality of Oligotrichida and

Scuticociliatida in Lake Tanganyika (Hecky et al. 1978) is similar to

that of comparable Florida systems--oligotrichs reaching a maximum

during late winter and fall with the appearance of scuticociliates

being limited to the fall ciliate maximum.

The bimodal seasonality in mesotrophic Florida lakes also

resembles that found in temperate waters. Sorokin (1972) noted a

bimodal trend in protozoan biomass in a Russian reservoir, and

Godeanu (1978) recorded the most oligotrichs during spring.













Detailed seasonality data on planktonic ciliates in

eutrophic-hypereutrophic lakes are sparse. There is a tendency

for very large-bodied (ca. 100um) ciliate communities to reach

population maxima in the benthos and the water column during

midsummer (Goulder 1974; Finlay 1978; Finlay et al. 1979), and this

has been related to anoxia at the sediment-water interface (Finlay

1980). In an eutrophic Georgia reservoir, midsummer blooms of

scuticociliates occur in metalimnetic and hypolimnetic zones of

intense microbial activity (Pace and Orcutt 1981; Pace 1982). The

blooms of Paramecium and Plaqiopyla in Florida lakes coincided with

depressed hypolimnetic oxygen concentrations, providing further

evidence of the relationship between ciliate biomass surges and

stable thermal stratification in highly productive lakes.

The factors regulating planktonic ciliate populations include

the quality and quantity of available food, temperature, and

predation. Food resources probably most strongly influence seasonal

and spatial dynamics of planktonic ciliates and have been used to

explain ciliate temporal and spatial distribution (Pace 1982; Psenner

and Schlott-Idl 1985). Small-bodied ciliates (e.g. scuticociliates)

are principally bactivorous and display maximum grazing efficiency on

particles between 0.3 micron and 1.0 micron (Fenchel 1980a). As s

result, they are largely excluded from lakes having <5 x 106

bacteria ml-1, a concentration normally found only in more productive

systems (Fenchel 1980b).

Population changes in phytoplankton communities also may

directly influence ciliate populations. Typically, oligotrophic and












mesotrophic lakes contain large proportions of nannoplanktonic

chlorophytes (Paerl and MacKenzie 1977), and the seasonal dynamics of

these algae could affect ciliate populations through temporal

modification of food sources. Ample evidence suggests that potential

algal-grazing ciliates (large-bodied oligotrichs) and their algal

prey often coincide within the water column. Nauwerck (1963)

recorded oligotrich peaks simultaneously with peaks in three small

chlorophytes--Chlamvdomonas, Stichococcus, and Chlorella. Hecky et

al. (1978) found that oligotrich peaks corresponded to chlorophyte

maxima, and Sorokin (1972) noted a rise in protozoan biomass

associated with elevated bacterial densities during a senescing

spring algal bloom. In addition, Bienert (personal communication)

has noted the occurrence of metalimnetic plates of Strombidium viride

(>30 microns) feeding on nannoplanktonic chlorophytes in a softwater

oligotrophic Florida lake.

Direct evidence of the nannoplankton grazing potential of

oligotrichs in marine systems indicates that members of this order

may crop as much as 20% of the phytoplankton standing stock daily

(Heinbokel and Beers 1979). Fenchel (1980b) has shown that ciliates

which feed on larger (>lum) particles compare favorably with metazoan

suspension feeders with respect to the ability to concentrate

particles from dilute suspension. Consequently, size partioning of

food resources by pelagic ciliates likely contributes to the

compositional shift in protozoan populations. Large-bodied

oligotrichs dominate in oligotrophic lakes, but are progressively













replaced by small-bodied taxa in more productive systems (Beaver and

Crisman 1982).

Another factor likely to substantially influence planktonic

ciliate succession is temperature. The growth and reproduction of

freshwater ciliates are strongly correlated with temperature (Finlay

1977). Finlay (1980) has demonstrated in field studies that

temperature has a highly significant effect on benthic communities in

hypereutrophic situations with total ciliate biomass and abundance

peaks coinciding with the warmest water temperatures. Thus, the

results of the present study are in good agreement with Finlay

(1980), at least for the most productive lakes, where ciliate

population pulses occurred during midsummer. Finally, Zaret (1980)

has proposed that invertebrate predation pressures should be more

intense on microzooplankton populations than macrozooplankton

populations. Sorokin and Paveljeva (1972) documented that the

predaceous rotifer Asplanchna reduced ciliate concentrations within

metalimnetic plates of a Russian reservoir. Crustaceans are also

capable of greatly reducing ciliate populations as both cladocerans

(Porter et al. 1979) and copepods (Archbold and Berger 1985) may

subsist on protozoa. Predation pressure is likely to be a function

of trophic state, as the elevated densities of both predator and prey

should increase encounter probabilities.

Ciliate seasonality often has been determined in isolation from

other plankton components, and few studies exist specifically

relating protozoan seasonality to other zooplankton groups.

Fortunately, concurrent measurements of rotifer and crustacean












populations are available (Bays 1983) which underscore the necessity

of evaluating protozoa in zooplankton studies. Eutrophic/hyper-

eutrophic systems were dominated by macrozooplankton during spring

and fall, while microzooplankton biomass rotiferss, nauplii,

ciliates) dominated the summer communities. Ciliates accounted for

34% and 62% of the total zooplankton biomass during June, July, and

August in eutrophic and hypereutrophic lakes, respectively. This is

in agreement with Pace and Orcutt (1981) for a eutrophic Georgia

reservoir. Mesotrophic lakes exhibited a spring-fall pattern in

macrozooplankton biomass and a fall peak in microzooplankton biomass

with 34% of total zooplankton biomass being accounted for by ciliates

in autumn. Oligotrophic systems were characterized by

macrozooplankton peaks in late winter-early spring, but dominance was

shared with microzooplankton during fall. Ciliates contributed an

average of 24% to the total zooplankton biomass in the late winter-

early spring period and 27% during the fall months.

It is apparent from this data that seasonal trends of major

ciliate orders are a function of trophic state for Florida lakes, and

it is likely that subtropical thermal regimes and lake depth largely

determine suitability of food resources. Departures from these

generalized schemes usually occurred in the shallowest lakes of each

subset and were coincident with destratification during the normal

period of stratification. Although temperature shows a weak but

significant relationship with major ciliate components, I feel

temperature has a direct influence on ciliate seasonal dynamics only

in the most productive Florida systems that are often holomictic.















CHAPTER V
CILIATE POPULATIONS OF HIGHLY COLORED FLORIDA LAKES

Introduction

The clear relationship between abundance and biomass of

planktonic ciliated protozoa and lake trophic state, as measured by

chlorophyll a and total phosphorus, is well documented for clear

water lakes (Beaver and Crisman 1982; Pace 1986). Taxonomic

replacements in ciliate communities occur along gradients of both

increasing productivity (Beaver and Crisman 1982) and increasing

acidity in softwater lakes (Beaver and Crisman 1981). Typically,

ciliate communities in oligotrophic systems are dominated by large-

bodied oligotrichs which are progressively replaced by small-bodied

scuticociliates in more eutrophic situations. The primary factor

controlling the temporal and spatial distributions of planktonic

ciliates is believed to be the quality and quantity of available food

resources (Pace 1982; Fenchel 1987). Unfortunately, most knowledge

on ciliate distribution comes from clear water lakes, and comparison

with ciliate communities in organically colored lakes of differing

fertility is missing.

Several lake classification schemes have recognized that dark-

water lakes have "atypical" chemical and biological properties that

differentiate them from clear lakes (Hansen 1962). For example,

Shannon and Brezonik (1972) noted that colored lakes in Florida













possess higher nitrogen and phosphorus concentrations than would be

predicted from their chlorophyll a concentrations.

Most research on biological responses to organic color in lakes

has concentrated on phytoplankton growth and dynamics. Primary

effects include regulation of micronutrient availability (Giesy 1976)

and attenuation of light quality and intensity (Wetzel 1980), both of

which may strongly influence phytoplankton community structure (Kirk

1976). The effect of organic color on zooplankton populations is not

well studied, and data are almost totally absent for pelagic

ciliates.

The purpose of this research was to determine if ciliate

populations in organically colored lakes, representing a broad range

of trophic conditions, differ with respect to their abundance,

biomass, taxonomic composition and seasonality when contrasted with a

comparable trophic gradient of clear water lakes

within the same geographic region.

Methods

Ciliate samples were collected monthly (January-December

1979) from five Florida lakes (Beaver 1980) and approximately monthly

(September 1979-August 1980) from six other Florida lakes (Bienert

1982). All samples were collected from a single midlake station.

The minimum criterion for inclusion in the study was mean annual

color concentrations of >75 Pt units. Ciliates observed to contain

symbiotic zoochlorellae were tabulated separately in the latter six

lakes and were assumed to have 75% of their biomass devoted to

autotrophic production (Hecky and Kling 1981).












Bacteria, phytoplankton and zooplankton abundances were

determined also for these six lakes. Total bacteria were counted by

the epifluorescence technique and were reported by Crisman et al.

(1984). Phytoplankton subsamples from the composite sample were

preserved with Lugol's solution and analysed according to the

Utermohl technique (Lund et al. 1958). Phytoplankton biomass was

calculated from chlorophyll a concentrations assuming 1 mg

chlorophyll a= 67 mg dry weight (APHA 1982). Non-ciliate zooplankton

were collected from the entire water column by vertical tows with a

number 20 Wisconsin-style plankton net (mesh size= 76-80 microns)

and preserved with buffered formalin. Detailed information on

collection and quantification of phytoplankton and zooplankton are

described in Bienert (1982).

Secchi disk transparency, color, conductivity, total phosphorus,

pH and chlorophyll a were determined monthly. Chemical analyses were

performed on subsamples taken from the composite sample and evaluated

according to accepted techniques (APHA 1982).

The six lakes with bacteria, phytoplankton, zooplankton and

chemistry data were selected for correlation analysis. All

statistical operations utilized the SAS (1985) computer package.

Prior to analyses, biological and chemical values were normalized by

a log (n + 1) transformation.

Study Sites

The study sites consisted of relatively shallow lakes of low

transparency and total phosphorus (Tables 5-1 and 5-2). Mean annual

color ranged from 120 to 437 color units. Most of the color probably


















Table 5-1. Morphometric characteristics of lakes used to
determine ciliate community structure in colored lakes.


Surface Area
(hectares)


Mean Depth
(meters)


Blue Cypress

Norris

Dorr

Ida

Jefford

Washington

Eaton

Sampson

Holden

Newnans

Thonotosassa


Indian River

Lake

Lake

Putnam

Alachua

Brevard

Marion

Bradford

Alachua

Alachua

Hillsborough


Lake


County


2653

458

621

49

66

1765

124

826

32

3006

331


3.0


1.5

2.5
















Table 5-2. Mean values of selected limnological variables of
lakes used to determine ciliate community structure in colored
lakes.





Lake Chlorophyll Bacteria Color Secchi disk Total P pH

(mg/m3) (x 106) (Pt units) (meters) (mg/m3)



Blue Cypress 3.3 247 0.81 82 5.8

Norris 3.6 7.3 437 0.70 140 7.0

Dorr 3.7 2.8 120 1.30 20 6.6

Ida 3.9 4.5 152 1.10 100 5.3

Jefford 4.7 5.1 121 0.80 140 5.3

Washington 5.2 227 0.78 54 7.0

Eaton 5.8 10.5 123 1.20 60 6.9

Sampson 6.0 132 1.30 65 6.7

Holden 43.2 10.2 153 0.90 120 6.2

Newnans 65.4 163 0.60 115 7.0

Thonotosassa 71.1 128 0.50 582 8.1











originated from catchments dominated by cypress (Taxodium) and/or

pine (Pinus). Based on average chlorophyll a values, the lakes were

assigned to trophic classifications using the equations of Carlson's

(1977) Trophic State Index. This produced the following subsets--

oligotrophic (Blue Cypress, Norris, Dorr, Ida, Jefford), mesotrophic

(Washington, Eaton, Sampson), and eutrophic/hypereutrophic (Holden,

Newnans, Thonotosassa).

Results

Mean Abundance, Biomass, and Taxonomic Composition of
Ciliate Communities

There was a highly significant correlation (p<0.01) between both

annual ciliate abundance and biomass and chlorophyll a

(Figure 5-1). The regression equations were then compared with those

derived for 25 clear water Florida lakes (Beaver and Crisman 1981,

1982) representing an equivalent trophic gradient. The regression

coefficients (+ 95% C.I.) for abundance in colored (0.82 + 0.16) and

clear water (0.89 + 0.08) lakes were not significantly different, and

confidence intervals of the intercept estimates overlapped (colored,

1.64 + 0.40; clear water, 1.20 + 0.17). Similarly, the regression

coefficients for biomass in colored (0.79 +0.18) and clear water

(0.75 + 0.12) lakes, as well as the intercepts (colored, 2.80 + 0.47;

clear water, 2.54 + 0.25), were not significantly different. Thus,

there is no evidence to indicate that the abundance and biomass of

total ciliates in colored lakes are significantly different from

clear water lakes for a given trophic state.

The proportional abundance of the Oligotrichida in colored lakes

generally decreased with increased productivity (Table 5-3). The






























5 10 45


CHLOROPHYLL


5 10 45


CHLOROPHYLL





Figure 5-1. Relationship between planktonic ciliate abundance (A)
and biomass (B) and mean annual chlorophyll a concentration in 11
highly colored Florida lakes.

















Table 5-3. Mean annual percentage composition (+ SD) of dominant
ciliate orders in 11 colored Florida lakes grouped by trophic
state. Denotes means significantly different (t-test, p <0.05).


Oligotrichida


Haptorida


Scuticociliatida


Oligotrophic


Blue Cypress
Norris
Dorr
Ida
Jefford


Mean

Clear lakes(n=15)


Mesotrophic


Washington
Eaton
Sampson


Mean

Clear lakes(n=6)



Eutrophic/Hypereutrophic


Holden
Newnans
Thonotosassa



Mean


52+15

30+ 5


32+15


* 12+ 4 *

* 28+ 7 *


21+ 4


23+ 6 16+ 7


57+13

57+20


18+8

17+12


15+12

6+ 7


20+11

30+ 7


29+11

35+ 5


Clear lakes(n=4)










contribution of the Haptorida did not appear to change between

trophic states, but the Scuticociliatida increased with

eutrophication. Although the rank ordering of the three ciliate

orders was not significantly different between clear and colored

lakes in the eutrophic/hypereutrophic range, colored lakes displayed

greater representation of scuticociliates in the oligotrophic range

and significantly greater and lower importance of oligotrichs and

haptorids, respectively, in the mesotrophic range.

Seasonality of Ciliate Communities

Oligotrophic colored lakes consistently displayed a strong pulse

of ciliate abundance and biomass during the summer (Figure 5-2). The

highest ciliate density (83 ciliates ml-1) and biomass (317 mg d.w.

-3
m ) in the oligotrophic subset occurred during June in Lake Norris,

the most colored lake.

Mesotrophic Lake Eaton had total abundances maxima during

October (49 ciliates ml-1) and August (42 ciliates ml-1), with

populations remaining low during the winter and gradually increasing

throughout the spring and summer months. Total ciliate biomass

generally tracked total abundance, but a biomass surge was noted

during February that was due to the large oligotrich Tintinnidium

fluviatile (Kahl). The remaining colored mesotrophic lakes, Sampson

and Washington, recorded abundance/biomass peaks during June and

September, and in June, respectively.

Eutrophic Holden Pond recorded two distinct peaks of total

ciliate abundance (A) and biomass (B) in October (A= 301 ciliates ml

1, B= 1740 mg d.w. m-3) and June (A= 360 ciliates ml-1, B= 1510


















NORRIS DORR
300 80 100 -- 80

200 40 50o -40
S 100-, -


D M J D M J
m
IDA JEFFORD

200 50 400
100 -
S 100 20 5 0
I 1--0 -
0 5z

Om
D M J D M J
ET N HOLDEN
EATON 4
100 40 1500 -
2 1000 200
50 0 20 0200


D M J D M J










Figure 5-2. Seasonality of total ciliate biomass (closed circles)
and total ciliate abundance (open circles) in six highly colored
Florida lakes.











mg d.w. m-3). Populations tended to be depressed at other times of

the year. This pattern was also noted in the other productive colored

lakes (Thonotosassa and Newnans) which showed peaks in total abundance

and biomass during the summer and winter.

In oligotrophic lakes pulses in ciliate densities occurred

during midsummer and were consistently dominated by the Oligotrichida

(Figure 5-3). The highest densities of oligotrichs in the

oligotrophic lake set occurred in Lake Norris during May (49 ml-).

The dominant ciliate species found during these events were

Strombidium cf oculatum (Kahl), Strombidium viride (Kahl), and

Strobilidium humile (Kahl). Strombidium cf oculatum contributed

heavily to the total biomass of these systems because of its relative

large size (ca. 20000 microns3) and high abundance. Although mostly

of secondary importance, populations of haptorids and scuticociliates

frequently increased in early spring.

In mesotrophic Lake Eaton, oligotrichs exhibited maximum

densities in November 1979, following the October peak in total

ciliate abundance, and again in August 1980 coincident with the peak

in total ciliates recorded during that year. Scuticociliate

densities were greatest in October and January. The seasonality of

oligotrichs in eutrophic Holden Pond paralleled that of total ciliate

abundance and biomass with peaks occurring in October and June.

Scuticociliate densities were highest during November and January,

and again in July, following the June peak in total ciliate

abundance. In both mesotrophic and eutrophic/hypereutrophic lakes,

the dominant oligotrich was Strombidium cf oculatum. Although recent






















NORRIS


D M J


D M J


JEFFORD


D M J


D M J


EATON


HOLDEN


300

200
100


D M J


D M J


Figure 5-3. Seasonality of Oligotrichida (closed circles) and
Scuticociliatida (open circles) in six highly colored Florida lakes.


DORR











taxonomic reorganizations within the Oligotrichida (Maeda and Carey

1985; Maeda 1986) did not discuss a freshwater distribution of

Strombidium oculatum, Kahl (1930-1935) acknowledged that this species

is also encountered in freshwater.

Importance of Myxotrophic Ciliates

Partitioning the biomass of ciliate populations into

heterotrophic and autotrophic components produced a distinct

seasonality irrespective of trophic state (Figure 5-4). Myxotrophic

ciliates were abundant and had high biomass during midsummer in all

six lakes. Autotrophic taxa were usually poorly represented in the

autumn and winter plankton but increased in spring. The dominant

myxotrophic ciliate in terms of both abundance and biomass was

Strombidium cf oculatum.

The highest autotrophic ciliate biomass for the oligotrophic

subset of lakes was recorded in Lake Norris during June (>175

mg d.w. m-3). Among the eutrophic lakes, the highest biomass was

found in Holden Pond during October (>1200 mg d.w. m-3). The average

standing crop of autotrophic ciliate biomass accounted for over 50%

of the annual total ciliate biomass in four of the study lakes (Table

5-4).

The seasonality of heterotrophic biomass generally paralleled

that of the autotrophic portion of the ciliate community. With one

exception the autotrophic biomass peak exceeded the heterotrophic

maximum for each lake. The biomasses of both autotrophs (r= 0.75)

and heterotrophs (r= 0.57) were strongly correlated with chlorophyll

a, but were not related to bacterial densities.



















DORR


NORRIS


D M J


D M J


JEFFORD


D M J


EATON


D M J


HOLDEN


1000

500


D M J


D M J


Figure 5-4. Seasonality of autotrophic ciliate biomass (closed
circles) and heterotrophic ciliate biomass (open circles) in six
highly colored Florida lakes.


200

100


0%












0

U-

















Table 5-4. Annual means for heterotrophic and autotrophic ciliate
biomass, and percentage contribution of autotrophic ciliate biomass
to total autotrophic biomass. Myxotrophic ciliates were assumed to
have 75% of their biomass devoted to autotrophic production and 25%
to heterotrophic production.


Heterotrophic Biomass


Autotrophic Biomass


% Contribution to
Total Autotrophic
Biomass


(mg d.w. m-3)


44.5

28.4

28.6

32.6

40.7


Holden 274.1


(mg d.w. m-3)


52.4

22.8

36.8

47.0

15.0

386.6


Lake


Norris


Dorr


Ida


Jefford


Eaton




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