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This is to certify that the
thesis entitled

PARASITES OF JUVENILE BLUEGILL, LEPOMIS
MACROCHIRUS AND YOUNG-OF-THE-YEAR
LARGEMOUTH BASS, MICROPTERUS SALMOIDES IN
THREE LAKES II AND GULL LAKE, MICHIGAN

presented by

BRENDA MAY PRACHEIL

has been accepted towards fulfillment
of the requirements for the

M. S. degree in Zoology

 

altr'lc)‘ m. (“u .

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2/05 p:/ClRC/DaleDue.indd-p.1

PARASITES OF JUVENILE BLUEGILL, LEPOMIS MACROCHIR US AND YOUNG-
OF—THE-YEAR LARGEMOUTH BASS, MICROPT ER US SALMOIDES IN THREE
LAKES II AND GULL LAKE, MICHIGAN

By

Brenda May Pracheil

A THESIS

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

MASTER OF SCIENCE

Department of Zoology
Ecology, Evolutionary Biology and Behavior Program

2006

ABSTRACT
PARASITES OF JUVENILE BLUEGILL, LEPOMIS MACROCHIRUS AND YOUNG-
OF-THE-YEAR LARGEMOUTH BASS, MICROPTERUS SALMOIDES FROM
THREE LAKES [I AND GULL LAKE, MICHIGAN
By
Brenda May Pracheil
A total of 622 fish, 393 juvenile bluegill and 26 young-of-the-year (Y OY)

largemouth bass from Three Lakes II, Michigan (TL) and 117 juvenile bluegill and 86
YOY largemouth bass from Gull Lake, Michigan (GL) were examined for parasites.
Monogene, trematode, cestode, acanthocephalan, nematode and protozoan parasites
infected juvenile bluegill and YOY Iargemouth bass. Larval trematodes, particularly
Coptogonimus sp., were the most prevalent and abundant parasites in juvenile bluegill
and YOY largemouth bass in both lakes. For bluegill in both lakes, the intestinal parasite
component community diversity values (Shannon diversity) were not representative of
total parasite component community diversity. Shannon diversity values for the total,
enteric and parenteric component communities for TL largemouth bass were similar.
Total parasite component community diversity of GL largemouth bass was higher than
enteric or parenteric communities. Larval trematodes and parasites using small
invertebrate intermediate hosts were the first parasites to colonize juvenile bluegill and
YOY Iargemouth from both lakes. The percentage of the parasite species consisting of
adult parasites generally increased with bluegill length in both lakes, but generally did not
increase for YOY largemouth bass. Largemouth bass had higher parasite component

community diversities than bluegill of the same age in both lakes.

ACKNOWLEDGMENTS

I would first like to thank my advisor Dr. Patrick Muzzall for all his guidance
throughout my education at Michigan State University. His door was always open when
I had questions or needed someone to debate the finer points of parasite ecology. He
truly made my educational experience here a fruitful one. I also thank my committee
members, Drs. Mary Bremigan and Don Hall for their input on this project.

There have been several other people who have been instrumental to this project.
I thank Merritt Gillilland for his help with statistics, snails and many great conversations
about parasite communities. Thanks are also due to Josh Nixon for saving my computer
fi'om crashing and Nate Coady, Laura Duclos and Matt Bolek for several engaging
discussions about parasites which helped me to form ideas which were key in the
completion of this work. Additionally, since pulling a seine solo is not an easy prospect,
I thank Chris and Simon Pracheil, Nate and Kate Coady, Merritt Gillilland, Karl Strause,
Andrea Winkle, Angelina Flores and Ai Shimizaki for field assistance. I finally thank my
husband Chris and son Simon and my parents Martin and Becky Ferris for providing me

with loving encouragement and emotional support while I completed my thesis work.

iii

TABLE OF CONTENTS

LIST OF TABLES .................................................................................. vi
LISTOF FIGURES ............................................................................ ' .............................. v iii

CHAPTER ONE: PARASITE INFRAPOPULATIONS AND COMMUNITIES
OF JUVENILE BLUEGILL, LEPOMIS [MACROCHIRUS AND LARGEMOUTH

BASS, MCROPIERUS SAIMOIDES IN THREE LAKES II, MICHIGAN ............... 1
INTRODUCTION ............................................................................ 2
MATERIALS AND METHODS .......................................................... 6
RESULTS ................................................................................... 14
DISCUSSION ................................................................................... 24

CHAPTER TWO: PARASITE INFRAPOPULATIONS AND COMMUNITIES
OF JUVENILE BLUEGILL, LEPOMIS WCROCHIRUS AND LARGEMOUTH
BASS, MCROPIIERUS SAWOIDES IN GULL LAKE, MICHIGAN AND

A COMPARISON OF PARASITE COMMUNITIES IN THREE LAKES II AND

GULL LAKE, MICHIGAN ......................................................................................... 40
INTRODUCTION. ............................................................................................... 41
MATERIALS AND METHODS ......................................................... 45
RESULTS ................................................................................... 49
DISCUSSION ............................................................................... 55

CHAPTER THREE: ACQUISITION AND DYNAMICS OF THE PARASITE
COMMUNITY OF JUVENILE BLUEGILL, LEPOMIS NIACROCHIRUS AND
YOUNG-OF-THE-YEAR LARGEMOUTH BASS, MICROPTERUS SALMOIDES

IN THREE LAKES H AND GULL LAKE, MICHIGAN .................................... 68
INTRODUCTION .......................................................................... 69
MATERIALS AND METHODS ......................................................... 72
RESULTS .................................................................................... 73
DISCUSSION .............................................................................. 75

iv

CONCLUSION ...................................................................................... 8 1

APPENDIX 1 ....................................................................................... 130
APPENDIX 11 ...................................................................................... 134
APPENDIX [11 ..................................................................................... 135
APPENDIX IV ..................................................................................... 136
APPENDIX v ...................................................................................... 137
LITERATURE CITED ........................................................................... 138

LIST OF TABLES

Table 1. Prevalence, mean abundance : SD (maximum) and site of infection
of parasites of 393 juvenile Lepomis macrochirus in 2003 and 2004 from Three
Lakes II, Michigan .................................................................................. 83

Table 2. Prevalence (%), mean abundance 3: SD (maximum) and site of infection
of parasites of 26 young-of-the—year Microptems salmoides fi'om Three Lakes II,
Michigan ............................................................................................. 86

Table 3. Mean abundance : SD (maximum) of parasites of juvenile Lepomis
macrochirus with greater than 30% overall prevalence by cohort fi'om Three
Lakes II, Michigan ................................................................................... 89

Table 4. Monthly prevalence, mean abundance : SD of parasites with greater
than 30% overall prevalence fiom the 2001 cohort of Lepomis macrochirus
from Three Lakes II, Michigan .......................................................................................... 90

Table 5. Monthly prevalence, mean abundance: SD of parasites with greater
than 30% overall prevalence from the 2002 cohort of Lepomis macrochirus
from Three Lakes H, Michigan .................................................................... 91

Table 6. Monthly prevalence, mean abundance: SD of parasites with greater
than 30% overall prevalence fiom the 2003 cohort of Lepomis macrochims
from Three Lakes H, Michigan .................................................................... 94

Table 7. Variance to mean abundance ratio for the most common parasites
(parasites with >30°/o prevalence overall) for the 2002 cohort of Lepomis
macrochirus from Three Lakes [1, Michigan by month ........................................ 95

Table 8. Variance to mean abundance ratio for the most common parasites
(parasites with >30% prevalence overall) for the 2003 cohort of Lepomis
macrochirus from Three Lakes [1, Michigan by month ....................................... 96

Table 9. Mean 3: SD (range) of Brillouin’s diversity and evenness and species
richness and adjusted species richness for parasite infracommunities of Lepomis
macrochirus from Three Lakes II, Michigan ..................................................... 97

Table 10. Mean 1 SD (range) of Brillouin’s diversity and evenness and species
richness and adjusted species richness for parasite infracommunities of juvenile
Lepomis macrochirus from Three Lakes [1, Michigan by cohort .............................. 98

Table 11. Mean : SD of Brillouin’s diversity and evenness and species richness

and adjusted species richness for parasite infracommunities of for the 2001
cohort of juvenile Lepomis macrochirus from Three Lakes II, Michigan by month ...... 99

vi

Table 12. Mean 1 SD of Brillouin’s diversity and evenness and species richness
and adjusted species richness for parasite infiacommunities of for the 2002

cohort of juvenile Lepomis macrochirus from Three Lakes [1, Michigan by month ..... 100

Table 13. Mean 1: SD of Bn'llouin’s diversity and evenness and species richness
and adjusted species richness for parasite infiacommunities of for the 2003

cohort of juvenile Lepomis macrochirus from. Three Lakes H, Michigan by month ...... 101

Table 14. Prevalence, mean abundance : SD (maximum) and site of infection of

parasites of 117 juvenile Lepomis macrochirus from Gull Lake, Michigan by year. . . ..

Table 15. Prevalence, mean abundance : SD (maximum) and site of infection of
parasites of 86 juvenile Micropterus salmoides from Gull Lake, Michigan by year

Table 16. Mean : SD (range) of Brillouin’s diversity and evenness and species
richness and adjusted species richness for parasite infiacommunities of juvenile
Lepomis macrochirus from Gull Lake, Michigan from the 2003 and 2004

102

..... 105

sampling years ..................................................................................... 108

vii

LIST OF FIGURES

Figure 1. Map of Three Lakes H, Michigan with collection site ............................ 109

Figure 2. Mean lengths of Lepomis macrochims by cohort from Three lakes H,
Michigan by month. Standard error bars are included on mean length bars .............. 110

Figure 3. Water temperature of Three Lakes H (TL) and Gull Lake (GL),
Michigan by month ................................................................................ 111

Figure 4. Monthly abundance of mollusks by taxonomic group fi'om Three Lakes
H, Michigan ......................................................................................... 112

Figure 5. Monthly mean larval trematodes per Lepomis macrochirus irrespective
of cohort and total mollusks collected per month from Three Lakes H, Michigan ....... 113

Figure 6. Map of Gull Lake, Michigan with collection site ................................. 114

Figure 7. Monthly abundance of mollusks by taxonomic group from Gull Lake,
Michigan ............................................................................................ 1 15

Figure 8. Monthly mean trematodes per Lepomis macrochirus and total mollusks
collected per month from Gull Lake, Michigan ................................................ 116

Figure 9. Shannon diversity values for total, enteric and parenteric parasite
component communities for Lepomis macrochirus (BG) and Micropterus
salmoides (LMB) from Three Lakes H and Gull Lake, Michigan ........................... 117

Figure 10. Jaccard’s coefficient of community similarity for parasite component
communities of juvenile Lepomis macrochirus and young-of-the-year Micropterus
salmoides from Three Lakes H and Gull Lake, Michigan .................................... 118

Figure 11. Length of fish at first occurrence of parasite species from 392 juvenile
Lepomis macrochirus from Three Lakes H, Michigan. Numbers above vertical

lines represent the first occurrence of a parasite species and represent parasite

species as follows: l—Cryptogom'mus sp. metacercaria; 2—Proteocephalus

ambloplitis, 3—Trichodina sp., 4—Posthodiplostomum minimum, S—Neascus sp.,
6—Azygia sp. , 7—Cwnallanus sp., 8——Spiroxys, 9—Neoechinorhynchus

cylindratus, IO—Haplobothrium globuliforme, ll—Anchoradiscus sp., 12—

Monogene sp., lB—Diplostomum sp., l4—Spinitectus sp., IS—Myxobolus sp. .,

l6—A ctinocleidus sp.,17—Pomphorhynchus bulbocolli, 18—Clinostomum sp. .,
19—Crepidostomum sp. Height of lines arbitrarily determined” .. . .. 1 19

viii

Figure 12. Length of fish at first occurrence of parasite species from 117 juvenile
Lepomis macrochirus from Gull Lake, Michigan. Numbers above vertical lines

represent the first occurrence of a parasite species and represent parasite species as
follows: l—Cryptogonimus sp. metacercaria; 2— Posthodiplostomum minimum,
3—Diplosromum sp., 4—Pomphorhynclrus bulbocolli, S—Monogene sp., 6—
Proieocephalus ambloplitis, 7—Neascus sp., 8—Anchoradiscus sp., 9—
Neoechinorhynchus cylindratus, IO—Haplobothrium globuliforme, 11—
Leptorlnmchoides thecaius, 12——Spinitectus sp., l3—Azygia sp., 14——

Actinocleidus sp., IS—Trichodina sp., 16—Myxobolus sp. Height of lines

arbitrarily determined .............................................................................. 121

Figure 13. Length of fish at first occurrence of parasite species from 26 young-
of-the-year Micropterus salmoides from Three lakes H, Michigan Numbers above
vertical lines represent the first occurrence of a parasite species and represent

parasite species as follows: l—Cryptogonimus sp. metacercaria; 2— Monogene

sp., 3—Cryptogonimus sp. adult, 4—Proteocephalus ambloplitis, S—Trichodina

sp., 6—Monogene sp. A, 7—Azygia sp., 8—Posrhodiplosromum minimum, 9—

Neascus sp., IO—DI'pIostomum sp., ll—Neoechinorlrwclms cylindratus, 12—
Pomphorhynchus bulbocolli, l3—Spiroxys sp., 14— Cmnallanus sp. Height of

lines arbitrarily determined ....................................................................... 123

Figure 14. Length of fish at first occurrence of parasite species fiom 86 young-
of—the-year Micropterus salmoides from Gull Lake, Michigan. Numbers above

vertical lines represent the first occurrence of a parasite species and represent

parasite species as follows: l—Coptogonimus sp. metacercaria; 2— Trichodina

sp., 3—Camallanus sp., 4—Posthodiplostomum minimum, 5—DI'pIostomum sp.,
6—Pr0te0cephalus ambloplitis, 7—Leptorlwnchoides thecatus, 8—

Pomphorhynchus bulbocolli., 9—Monogene sp., 10—Azyg1'a sp., ll—Spinitectus

sp., 12—Monogene sp. A, l3—Myxobolus sp., 14— Neoechinorhynchus

cylindratus, 15—Clinostomum sp. Height of lines arbitrarily determined ................. 125

Figure 15. Percentage of adult parasite species of 392 juvenile Lepomis
macrochirus from Three Lakes H, Michigan in five mm length classes. .................. 127

Figure 16. Percentage of adult parasite species of 117 juvenile Lepomis
macrochirus from Gull Lake, Michigan by five mm length classes ......................... 128

Figure 17. Percentage of adult parasite species of 86 young-of-the-year
Micropterus salmoides from Gull Lake, Michigan by five mm length classes ............ 129

ix

CHAPTER ONE

PARASITE INFRAPOPULATIONS AND COMMUNITIES OF JUVENILE
BLUEGILL, LEPOMS WCROCHIRUS AND LARGEMOUTH BASS,

MCROPIERUS SAWOIDES IN THREE LAKES II, MICHIGAN

INTRODUCTION

Fish habitat (Esch, 1971; Wilson et al., 1996), diet and age (McDaniel and Bailey,
1974; Cone and Anderson, 1977; Hanek and Fernando, 1978a, 1978b; Bailey, 1984) are
determining factors in the composition and structure of parasite communities in
centrarchid fishes. The habitat in which a fish resides largely determines which parasites
it may host. Habitat attributes such as substrate type, vegetation type and quantity play a
major role in parasite intermediate hosts found in an area. Mollusks serving as
intermediate hosts for trematode parasites, for instance, shed larval trematodes that may
infect a fish by direct penetration. By sharing habitat with these mollusks, fish may
become infected with these parasites. Habitat, in turn, influences diet by determining
what prey items (which may be serving as intermediate hosts) are available to a fish. For
example, copepods serve as intermediate hosts for several species of parasites that are
acquired by fish through ingestion.

As a fish ages, it increases in size and surface area. With increased surface area, a
fish increases its chances of becoming infected with parasites via direct penetration (Spall
and Summerfelt, 1970). Also, some larval parasites, such as Posthodiplosromum
minimum, are long-lived and accumulate in a fish over several years (Spall and
Summerfelt, 1970; Hoffman, 1999). In bluegill, Lepomis macrochirus and largemouth
bass, Micropterus salmoides, age may influence parasite communities because juveniles
and adults have been shown to have different diets and habitats (Mittelbach, 1984;

Werner and Hall, 1988; Olson, 1996; Post, 2003; Sammons and Maceina, 2005).

The life history traits of juvenile bluegill and young-of-the-year (YOY)
largemouth bass should contribute to the development of a parasite fauna unique to their
life stage. Adult bluegill spawn in vegetated littoral areas in May or June in Michigan
when water temperature reaches approximately 20° C (Breder, 193 6; Werner, 1967;
Werner and Hall, 1988). After hatching approximately two weeks post-spawn (Breder,
1936), bluegill fry undergo a migration to the limnetic zone of a lake and remain there for
approximately six to eight weeks (Werner, 1967; Werner and Hall, 1988). Juvenile fish
then return to the vegetated littoral zone for the next two to three years (Werner and Hall,
1988) until they move to the limnetic zone of the lake for the duration of their life
(Werner and Hall, 1988). The shift to the limnetic habitat gradually takes place in
bluegill between 45 and 75 mm SL (Osenberg et al., 1992). At approximately 75 mm SL,
bluegill switch to feeding almost exclusively in the limnetic zone of a lake (Werner and
Hall, 1988), which is approximately commensurate with maturity (Osenberg et al., 1992).

Throughout life, bluegill prey on aquatic invertebrates that serve as intermediate
hosts for many types of parasites (Zischke and Vaughn, 1962; Werner, 1969; McDaniel
and Bailey, 1974; Sadzikowsi and Wallace, 1976; Cone and Anderson, 1977; Werner and
Hall, 1988; Fisher and Kelso, 1990). However, the invertebrate prey available in the
limnetic zone where bluegill spend their adult life differs from that available in the
vegetated littoral zone where they live as juveniles (Mittelbach, 1984; Werner and Hall,
1988). This shifi in diet and habitat may cause the parasite fauna to concurrently shift
(Wilson et al., 1996). Additionally, the vegetated habitat of juvenile bluegill is habitat for
many mollusks that serve as intermediate hosts for trematodes that shed larval parasites

that directly penetrate bluegill (Wilson et al., 1996).

Largemouth bass spawn in April or May in Michigan in vegetated littoral areas
(Breder, 1936) when the water temperature reaches approximately 15-18° C (Mittelbach
and Persson, 1998). The YOY largemouth bass remain in the littoral zone for the first
few weeks to months of life feeding on invertebrates (Gilliam, 1982; Olson, 1996; Post,
2003). When largemouth bass become large enough to eat fish, they switch to a
piscivorous diet, primarily preying on juvenile bluegill (Gilliam, 1982; Olson, 1996; Post,
2003) and continue to prey on fishes throughout their life. Since largemouth bass eat
aquatic invertebrates such as copepods, arnphipods and mayflies for the first few weeks
to months of life (Sale, 1981; Gilliam, 1982; Fischer and Kelso, 1990; Olson, 1996;
Dibble and Harrel, 1997; Post, 2003), they may acquire parasites that use these
invertebrates as intermediate hosts. As is the case with juvenile bluegill, while living in
the vegetated littoral zone, largemouth bass are vulnerable to colonization by larval
trematodes shed by mollusks. Since largemouth has become piscivorous early in life,
primarily eating juvenile bluegill, they may acquire parasites that use bluegill as
intermediate or paratenic hosts.

Because juvenile and adult bluegill (Werner and Hall, 1988) and juvenile and
adult largemouth bass (Werner and Hall, 1988; Sammons and Maceina, 2005) have
different habitats and diets, parasite faunas should differ between juvenile (pre-
reproductive) and adult (reproductively mature) fish. Most studies on the parasites of
bluegill and largemouth bass are restricted to the examination of adult fish or fish of
unknown age (see Hoffman, 1999 for a list of studies of bluegill parasites). Few studies

report on changes in bluegill parasite communities with host age (McDaniel and Bailey,

1974; Cloutman, 1975) and only one study examines parasite community dynamics of
largemouth bass with host age (Cloutman, 1975).

Studies on the parasite communities of juvenile bluegill and YOY largemouth
bass are limited to Fischer and Kelso (1987, 1988, 1990), Landry and Kelso (1999) and
Steinauer and Font (2003). All these studies were conducted in Louisiana which may not
be indicative of the parasite communities of these fish in Michigan. Effects of fish age
on parasite community composition and structure in juvenile bluegill and YOY
largemouth bass were also not examined in the above studies. Fisher and Kelso (1987,
1988, 1990), Landry and Kelso (1999) and Steinauer and Font (2003) reported that
parasite communities of juvenile bluegill and YOY largemouth bass were dominated by
larval trematodes. However, not all larval trematodes in these studies were counted so
the numeric role and the effect these parasites have on parasite community diversity of
juvenile bluegill and YOY largemouth bass is not known.

The objectives of this study were to determine patterns of parasite infrapopulation
abundance and prevalence for the most common parasites of three cohorts of juvenile
bluegill (C optogonimus sp., Posthodiplostomum minimum, Neascus sp. and
Proteocephalus ambloplitis) and YOY largemouth bass (Coptogonimus sp.
metacercariae, Neascus sp., P. minimum, Diplosromum sp., Neoechinorhynchus
cylindratus and Proteocephalus ambloplitis) from Three Lakes H, Michigan; to
determine patterns of parasite infracommunity diversity in three cohorts of juvenile
bluegill; and finally, to describe parasite component community diversities in juvenile

bluegill and YOY largemouth bass.

MATERIALS AND METHODS

Description of Study Site

Three Lakes H (Figure 1) (hereafter referred to as TL) is in Kalamazoo County,
Michigan and is connected to two other lakes, Three Lakes 1 and Three Lakes III, by
short (<1 km) channels (Mittelbach, 1984). Three lakes H is a eutrophic lake with a
surface area of 22 hectares and exhibits thermal stratification (Mittelbach, 1984). This
lake has a broad littoral zone that extends up to 60 m fi'om shore with a bottom that
gradually slopes to a maximum depth of approximately 10 m (Mittelbach, 1984).

Fish Collection and Examination

Collection of fish took place in a shallow (<15 m) area on the southeast side of
the lake where the yellow pond lily, Nuphar Iutea was the dominant vegetation. A total
of 393 juvenile bluegill (209 from 2003 and 184 from 2004) were collected by seine in
June through November, 2003 and April through July, 2004. Twenty-six YOY
largemouth bass were also collected by seine in July and September, 2003. Upon
collection, fish were placed in aerated coolers and transported to the laboratory at
Michigan State University.

Fish were killed within 48 hours of collection by an overdose of the anesthetic
MS-222. The standard length (SL), distance from the tip of the snout to the end of the
caudal peduncle, was measured in millimeters for each fish before being preserved in a
vial of 70% ethyl alcohol. Five scales from each fish were removed from under the lefi
pectoral fin below the lateral line for aging. Scales were mounted on glass slides and

scale annuli were counted using dissecting and compound microscopes. Some fish were

examined immediately after euthanization so live parasites could be properly fixed for
identification purposes.

The head of the fish was removed and the remainder of the fish was out along the
ventral surface to the vent. The stomach, pyloric ceca, intestine, gall bladder, liver,
spleen, kidneys, heart, eyes, brain, gonads, nares, skin, fins, muscles, and gills were
placed in Petri dishes containing tap water and examined for parasites. The location of
all parasites and the number of all countable parasites (parasites except monogenes and
protonans) were recorded. Only prevalence of monogenes and protozoans was recorded
because MS-222 may have caused some of these parasites to fall off the fish, so accurate
‘ counts of these parasites could not be made. Parasites were preserved in 70% ethyl
alcohol.

Parasite Preparation and Identification

Protozoan parasites were identified on wet mount slides. Trematodes,
monogenes, cestodes and acanthocephalans were rehydrated in a graded ethyl alcohol
series and were left in each solution for approximately one hour. The rehydration series
concentrations were as follows: 70% ethyl alcohol; 40% ethyl alcohol; 20% ethyl
alcohol; and 100 % distilled water. Parasites were then placed in a Stentor dish of
Grenacher’s borax carmine stain overnight and then removed to another Stentor dish of
distilled water for one hour. The parasites were then dehydrated in a graded ethyl alcohol
series and were left in each solution for approximately one hour. The dehydration series
concentrations were as follows: 20% ethyl alcohol; 40% ethyl alcohol; 70% ethyl
alcohol; 80% ethyl alcohol; 95% ethyl alcohol; and two repetitions of 100% ethyl

alcohol. Parasites were moved to a Stentor dish of xylene to clear for approximately one

hour and mounted on glass slides using Canada balsam diluted with xylene and covered
with a glass coverslip. Nematodes were cleared by adding five drops of 100% glycerine
daily until all ethyl alcohol evaporated and stored in vials of 100% glycerine.
Parasitological Terminology

A host is an animal which is infected with a parasite (Roberts and Janovy, 2004).
A definitive host is one in which the parasite becomes sexually mature and produces
some type of offspring (Roberts and Janovy, 2004). An intermediate host is one in which
the parasite does not reach sexual maturity but undergoes growth and development
necessary to infect the next host in its life cycle (Roberts and Janovy, 2004). A paratenic
host is one in which the parasite does not reach sexual maturity and does not undergo
growth and development necessary to infect the next host in the life cycle, yet still
remains alive and infective (Roberts and Janovy, 2004). Parasite paratenic hosts bridge
trophic gaps between intermediate and definitive hosts. For instance, adult largemouth
bass infrequently eat copepods, the intermediate host for a cestode parasite of these fish.
Bluegill can become infected with a larval stage of this cestode when eating an infected
copepod (Hunter, 1928). The largemouth bass can become infected with this cestode
parasite by eating an infected bluegill. A direct life cycle does not require an
intermediate host for sexual reproduction (Roberts and Janovy, 2004). An indirect life
cycle requires development in one or more intermediate hosts prior to sexual
reproduction (Roberts and Janovy, 2004).

A parasite infracommunity is the community of all species of parasites in one host
individual (Bush et al., 1997). A parasite component community is the community of all

species of parasites infecting one host species in a geographic area (Bush et al., 1997).

Enteric parasites occur within the gastrointestinal tract and parenteric parasites live in
sites outside of the gastrointestinal tract (Roberts and Janovy, 2004). Life cycles and life
stage terminology of parasites found in the present study are in Appendix I.

The most common parasite species were defined as those with greater than 30%
prevalence (arbitrarily detemrined) in examined fish for each host species. The term
prevalence is the percentage of individuals in a sample infected with a parasite species
(Bush et al., 1997). Abundance is the number of parasites of a species in a fish and mean
abundance is the mean number of parasites of a species per examined fish in a sample
(Bush et al., 1997). Species richness is the number of parasite species per host and mean
species richness is the mean number of parasite species per fish in a sample. Adjusted
species richness is the number of countable parasite species per host and mean adjusted
species richness is the mean number of countable parasites per fish in a sample. Adjusted
species richness was calculated in order for comparisons to be made between species
richness and Brillouin’s diversity and evenness values, which only include countable
parasites.

Data Analysis

Names of fish cohorts correspond to the year those fish hatched. For example,
fish that hatched in 2003 are referred to as the 2003 cohort of fish. The 2001 cohort of
bluegill consisted of age 2 fish collected in June-October, 2003; the 2002 cohort of
bluegill consisted of age 1 fish collected in June-October, 2003 and age 2 fish collected in
April-July, 2004; and the 2003 cohort of bluegill consisted of age 0 fish collected in June-

October, 2003 and age 1 fish collected in April-July, 2004. No fish with mature gonads

.were examined in the present study. Mean fish lengths are expressed as mean 1 standard
deviation (SD) (range).
Prevalence and Mean Abundance of the Most Common Parasites

Mean parasite abundances are expressed as mean 1 SD (maximum). Parasite
abundance values were natural log transformed for nomrality. All statistical comparisons
were considered significant at the a=0.05 level. Because multiple chi-square analyses
were needed to detect significant differences in prevalence among cohorts of fish,
Bonferroni corrections were used to compute a lower a—value to minimize
experimentwise error. The new a—value for these tests was 0.02. Chi-square analyses
were used to detect significant differences in prevalence of the most common parasite
species by comparing numbers of infected and uninfected bluegill between sampling
years irrespective of fish cohort and between fish cohorts irrespective of sampling year.
An unpaired t-test was used to detect significant differences in mean abundances of the
most common parasite species of juvenile bluegill between the 2003 and 2004 sampling
years. In cases where variance was not equal between samples, a t-test assuming unequal
variance was used. Analysis of variance (PROC MIXED, SAS 9.1) was used to test for
significant differences in mean abundances of most common parasite species among
cohorts of TL bluegill. Tukey’s HSD was used for all pairwise comparisons between
cohorts. Analysis of variance (PROC MIXED, SAS 9.1) was used to test for significant
differences in mean abundances of most common parasite species among months of
collection for TL bluegill. Tukey’s HSD was used for all pairwise comparisons between
months. Variance to mean abundance ratios were calculated for the most common

parasites of the 2002 and 2003 cohorts of bluegill in order to infer that decreases in

10

prevalence and mean abundance were due to parasite-induced mortality of bluegill.
Monthly patterns of infracommunities of the most common parasites of YOY largemouth
bass were not examined due to low numbers of bass examined.

A Spearman’s rank correlation was used to detect relationships between
untransformed abundances of the most common parasite species and fish length for
bluegill and largemouth bass irrespective of cohort and sampling year and for each cohort
of bluegill. A Spearman’s rank correlation was also used to detect relationships between
untransformed abundances of the most common parasite species, Brillouin’s diversity,
evenness, species richness and adjusted species richness and fish length for juvenile
bluegill in each cohort irrespective of sampling year.

Parasite Infracommunities

Mean Brillouin’s diversity and evenness values, species richness and adjusted
species richness values for parasite infracommunities are expressed as mean 1 standard
deviation (SD) (range). Parasite infiacommunity diversity, evenness, species richness
and adjusted species richness values were natural log transformed for normality. Values
for Brillouin’s index for use in diversity and evenness (Pielou, 1975; Magurran, 1988)
were calculated for each fish examined using common logarithms for all countable
parasites irrespective of their site of infection to measure diversity and evenness for the
parasite infiacommunity. Values for the Shannon diversity index were calculated for
each host species in each lake using common logarithms for all countable parasites
irrespective of their site of infection to measure diversity of the total parasite component

community. Separate Shannon diversity values for each host species for total, enteric and

II

parenteric parasites were calculated to determine whether diversities of these parasite
component communities were comparable.

All statistical comparisons were considered significant at the a=0.05 level. An
unpaired t-test was used to detect significant differences in mean parasite infracommunity
diversity, evenness, species richness and adjusted species richness of juvenile bluegill
between the 2003 and 2004 sampling years. In cases where variance was not equal
between samples, a t-test assuming unequal variance was used. Analysis of variance
(PROC MIXED, SAS 9.1) was used to test for significant differences in mean parasite
infiacommunity diversity, evenness, species richness and adjusted species richness
among cohorts of TL bluegill. Tukey’s HSD was used for all pairwise comparisons
between cohorts. Analysis of variance (PROC MIXED, SAS 9.1) was used to test for
significant differences in parasite infracommunity diversity, evenness, species richness
and adjusted species richness among months of collection for TL bluegill. Tukey’s HSD
was used for all pairwise comparisons between months.

Spearman’s rank correlation was used to detect relationships between
untransformed parasite infiacommunity diversity, evenness, species richness, adjusted
species richness and bluegill and largemouth bass length irrespective of cohort and
sampling year and for each cohort of bluegill.

A t-test for two Shannon diversity values was used to compare enteric and
parenteric component community diversity values to total component community
diversity values in juvenile bluegill and YOY largemouth bass. This t-test was also used

to compare total component community diversity between age-0 bluegill and YOY

12

largemouth bass. The variance of the parasite component community diversities for

bluegill and largemouth bass was approximated by:

.2 = )3,- logzfi — (afi- log/.32 n'1

H

where fl: number of individuals of each species, and n= number of individuals of all

species (Brower et al., 1993), for the test statistic:

r= H1’ —H2’
(312+322)m

(Brower et al., 1993) which is compared to the Student’s t-distribution with a = 0.05 and

degrees of fi'eedom approximated by:

DF= QSZH1'+ s2H2L2
ISZHl’lz'I‘ (3211212

n1 n2

(Brower et al., 1993).
Mollusk Collection

Mollusks were collected three meters from shore starting at the midpoint of the
fish collection area each month fish were sampled. Five one minute side-by-side
transects were sampled by sweeping an aquatic D-fiame dip net through the water
column from the top layer of substrate, through the submergent vegetation up to the
water’s surface (Hairston et al., 1958; Brown, 1979). All contents of the nets were
emptied into a container and preserved in 10% formalin or 70% ethyl alcohol in the field.
Mollusks were identified to family with a key to aquatic snails of the United States

(Burch, 1982, 1988; Burch and Tottenham, 1980) and counted.

13

RESULTS

Host Demographics

A total of 393 juvenile bluegill (209 from 2003 and 184 from 2004) and 26 YOY
largemouth bass were examined from TL. Irrespective of cohort, bluegill collected in
2003 and 2004 had mean lengths of31.8 : 8.7 (16-54) mm and 28.1 i 5.0 (20—42) mm,
respectively. Bluegill collected in 2003 were significantly larger than those collected in
2004 (t=4.61, p<0.01, 345 d.f.). The 2001 cohort consisted of 66 age 2 bluegill collected
in 2003; the 2002 cohort consisted of 63 age 1 bluegill collected in 2003 and 28 age 2
bluegill collected in 2004; and the 2003 cohort consisted of 80 age 0 bluegill collected in
2003 and 156 age 1 bluegill collected in 2004. Monthly mean lengths of fish by cohort
are in Figure 2. Monthly water temperatures from TL are in Figure 3.

The YOY largemouth bass were collected in July and September, 2003 and
consisted of 26 age 0 fish with a mean length of 38.4 i 15.0 (19—69) mm. Largemouth
bass fiom TL were significantly longer than age 0 bluegill (t=-5.38, p<0.01, 25 d.f.).
Parasites of Juvenile Bluegill and Young-of-the—Year Largemouth Bass

Prevalence and mean abundance : SD (maximum) for all parasite species of
juvenile bluegill by sampling year are in Table 1. Juvenile bluegill were infected with
71,400 parasites from fourteen countable parasite species: seven trematodes, Azygia sp.,
Crepidostomum sp., Clinostomum sp., Coprogonimus sp., Diplostomum sp., Neascus sp.
and Posthadiplostomum minimum; two cestodes, Proteocephalus ambloplitis and
Haplobothrium globuliforme, two acanthocephalans, Neoechinorlnmchus cylindratus and

Pomphorhynchus bulbocolli; three nematodes, CamaIIwrus sp., Spinitectus sp. and

14

Spiroxys sp. Bluegill were also infected with five non-countable parasite species: three
monogenes, Actinocleidus sp., Anchoradiscus sp. and Monogene sp.; and two protozoans,
Myxobolus sp. and T richodina sp. Some individuals of Crepidostomum sp., Spinitecrus
sp., Anchoradiscus sp. and Actinocleidus sp. were gravid adults- Parenteric larval
parasites, Clinostomum sp., Cryptogonimus sp., Diplostomum sp., Neascus sp., P.
minimum, P. ambloplitis, H. globuliforme, N. cylinrb'anw and Spiroxys sp. comprised
996% of all parasites counted. The larval trematode Coptogonimus sp. accounted for
93.2% of all parasites.

Prevalence and mean abundance : SD (maximum) for all parasites of YOY
largemouth bass are in Table 2. Young-of-the-year largemouth bass were infected with
1,157 parasites fiom 10 countable parasite species: five trematodes, Azygia sp.,
Coptogonimus sp., Diplostomum sp., Neascus sp. and P. minimum; one cestode, P.
ambloplitis; two acanthocephalans, N. cylincb'arus and P. bulbocolli; two nematodes,
CamaIlanus sp. and Spiroxys sp. Largemouth bass were also infected with three species
of non-countable parasites: two monogenes, Monogene sp. and Monogene sp. A; and one
protozoan, T richodina sp. Some individuals of Monogene sp. A, Coptogonimus sp. and
CamaIIanus sp. were gravid adults. Parenteric larval parasites, Coptogonimus sp.
metacercariae, Diplostomum sp., Neascus sp., P. minimum, P. ambloplitis and Spiroxys
sp. accounted for 95.8% of all parasites counted. Both adults and metacercariae of
Coptogonimus sp. were found. Cryptogonimus sp. metacercariae, which had the highest
prevalence and mean abundance, accounted for 76.9% of all parasites. Many parasite

species were common to both juvenile bluegill and YOY largemouth bass in TL, but a

15

larger percentage of the parasites of juvenile bluegill consisted of larval trematodes,
particularly Coptogonimus sp.
Prevalence and Mean Abundance of the Most Common Parasite Species

The most common parasite species of juvenile bluegill were Coptogonimus sp.,
Neascus sp., Posthodiplostomum minimum and Proteocephalus ambloplitis. The most
common parasite species of YOY largemouth bass were Coptogonimus sp., Neascus sp.,
Posthodrplostomum minimum, Diplosromum sp., Neoechinorhynchus cylindratus and
Proteocephalus ambloplitis. Abundance of the most common parasites was not

consistently higher in one year than in another. Bluegill from 2003 had significantly
higher prevalences of Neascus sp. (X2=11.37, p<0.01) and P. ambloplitis (X2=15.63,
p<0.01) than bluegill from 2004. Bluegill from 2004 had significantly higher
prevalences of P. minimum (X2=23.07, p<0.01) than bluegill from 2003. There was no

significant difference in prevalence of Coprogonimus sp. between sampling years.
Bluegill had significantly higher mean abundances of Coprogonimus sp. (t=6.89, p<0.01,
393 d.f), Posthodiplosromum minimum (t=8.71, p<0.01, 393 d.f.) and Neascus sp.
(t=4.53, p<0.01, 393 d.f.) in 2003 than 2004 and significantly higher mean abundances of
Proteocephalus ambloplitis (t=2.97, p<0.01, 393 d.f.) in 2004 than in 2003.

Prevalence and mean abundance : SD (maximum) for the most common parasite
species of juvenile bluegill by cohort irrespective of collection year in Table 3.
Coptogonimus sp. and P. minimum were the most prevalent and abundant parasite
species for all cohorts of juvenile bluegill. In general, the older cohorts of bluegill had

higher prevalences of the most common parasites. The 2001 cohort of bluegill had

significantly higher prevalences of P. minimum (X2=14.41, p<0.01), Neascus sp.

l6

(x2=45.34. o<o.on and P. ambloplitis (X2=46.06, p<0.01) than the 2003 cohort of
bluegill in TL. The 2002 cohort of bluegill had significantly higher prevalences of P.

minimum (X2=21.77, p<0.01), Neascus sp. (X2=58.08, p<0.01) and P. ambloplitis
(X2=32.22, p<0.01) than the 2003 cohort of bluegill.

After the first year of life, abundance of the most common parasites did not
significantly increase between the two oldest cohorts of bluegill. The 2002 and 2001

cohorts of bluegill had significantly higher mean abundances of Coptogonimus sp.

(ANOVA, F2, 390:1396, p<0.01), Neascus sp. (ANOVA, F2, 390=44.59, p<0.01), P.

minimum (ANOVA, F2, 390=84.l7, p<0.01) and P. ambloplitis (ANOVA, F2, 390:3558,

p<0.01) than the 2003 cohort. There were no significant differences in mean abundances
of any of the most common parasites between the 2001 and 2002 cohorts.

Prevalence and mean abundance : SD for the most common parasites of juvenile
bluegill by month and cohort are in Tables 4-6. With the exception of P. ambloplr'ris, the
2001 cohort had the highest mean abundances of the other most common parasites and
the highest prevalence of Neascus sp. each month this cohort was collected. In the 2002
cohort of bluegill, mean abundances of Cryptogonimus sp., Neascus sp. and P. minimum
decreased from May to June, 2004. In the 2003 cohort, mean abundances of
Coptogonimus sp. and P. minimum were significantly lower in May, 2004 than in
October, 2003 and abundances of Neascus sp. and P. ambloplitis were lower (although
not significant) in May, 2004 than in October, 2003. For the 2001 cohort of bluegill,

there were significant differences among months for abundances of thogonimus sp.

(ANOVA, F4, 61:4.61, p<0.01), Neascus Sp. (ANOVA, F4, 61: 12.77, p<0.01), P.

17

minimum (ANOVA, F4, 51:11.68, p<0.01). There were significant differences among
months for mean abundances of Coprogonimus sp. (ANOVA, F3, 32=3.57, p<0.01),

Neascus sp. (ANOVA, F3, 32=3.22, p<0.01) and P. minimum (ANOVA, F3, 32=3.87,
p<0.01) for the 2002 cohort of bluegill. The 2003 cohort of bluegill had significant

differences among months for mean abundances of Coptogonimus sp. (ANOVA, F7,
3323:4206, p<0.01), Neascus sp. (ANOVA, F7, 223=16.02, p<0.01) and P. minimum

(ANOVA, F7, 223:8.04, p<0.01).

Variance to mean abundance ratios of the most common parasite species by
cohort and month for juvenile bluegill are in Tables 7 and 8. In the 2002 cohort of
bluegill, variance to mean abundance ratios of Cryptogonimus sp. and Neascus sp. had
the largest decreases between May and June, 2004. For the 2003 cohort of bluegill, the
largest decreases in variance to mean abundance ratios occurred between October, 2003
and April, 2004 for Coptogonimus sp. and Neascus sp. and rose for of P. minimum and
P. ambloplitis between October, 2003 and April, 2004.

Significant Spearman’s rank correlations irrespective of bluegill cohort were

detected between abundances of Coptogonimus sp. (rs=0.71, p<0.01), Neascus sp.

(rs=0.52, p<0.01), P. minimum (rs=0.56, p<0.01) and P. ambloplitis (rs=0.31, p<0.01) and
fish length. The 2001 cohort of bluegill had significant correlations between abundances

of Coptogonimus sp. (rs=0.40, p<0.01), P. minimum (rs=0.70, p<0.01), Neascus sp.

(rs=0.59, p<0.01), P. ambloplitis (rs: -0.28, p=0.02) and bluegill length. The 2002 cohort

18

of bluegill had significant correlations between abundance of Coptogonimus sp.

(rs=0.35, p<0.01), P. minimum (rs=0.64, p<0.01), Neascus sp. (rs=0.34, p<0.01) and fish

length and a non-significant correlation between abundance of P. ambloplitis (rs=-0.04,

p=0.74) and fish length. The 2003 cohort of bluegill had significant correlations between

abundance of Coptogonimus sp. (rs=0.30, p<0.01), Neascus sp. (rs=0.25, p<0.01) and

fish length and a non-significant correlation between abundance of P. amblopliris

(rs=0.09; p=0. 15) and length. In YOY largemouth bass, abundances of Coprogonimus
sp. metacercariae (rs= ~0.54, p<0.01), Neascus sp. (rs=0.73, p<0.01), N. cylindratus

(rs=0.71, p<0.01) were significantly correlated with fish length.

Parasite Infracommunity Comparisons
Bluegill

Mean Brillouin’s diversity, evenness, species richness and adjusted species
richness for parasite infracommunities of juvenile bluegill by sampling year irrespective
of cohort are in Table 9. For bluegill irrespective of cohort, the 2003 sampling year had
significantly higher infracommunity diversity (t=3.44, p<0.01, 391 d.f.), species richness
(t=5.66, p<0.01, 354 d.f.) and adjusted species richness (t=5.64, p<0.01, 359 d.f.).

Mean parasite infracommunity diversity, evenness, species richness and adjusted
species richness for juvenile bluegill by cohort irrespective of sampling year are given in

Table 10. The 2002 and 2001 cohorts of bluegill had significantly higher species

richness (ANOVA, F2, 290=85.23, p<0.01) and adjusted species richness (ANOVA, F2?

290:76. 13, p<0.01) than the 2003 cohort. Mean infracommunity diversity was

19

significantly higher in the 2002 cohort than in the 2003 cohort (ANOVA, F2_ 290:5.47,

p<0.01), but mean infracommunity diversity in the 2001 cohort did not significantly
differ from either the 2002 or 2003 cohorts.

Monthly mean parasite infracommunity diversity, evenness values, species
richness and adjusted species richness for each cohort of bluegill are in Tables 11-13. In
all cohorts of bluegill, infracommunity diversity and evenness generally increased from
June through October, 2003. In the 2001 (Table 11) and 2002 (Table 12) cohorts of
juvenile bluegill, species richness and adjusted species richness peaked in August. In the
2003 cohort (Table 13), species richness and adjusted species richness increased fi'om
August through April, 2004. In the 2002 cohort, there was a significant decrease in
species richness and adjusted species richness and a decrease (although not significant) in
diversity and evenness between May and June, 2004. In the 2003 cohort, there was a
significant decrease in infracommunity diversity and evenness and no change in species
richness and adjusted species richness between May and June, 2004. For the 2001 cohort

of bluegill, there were significant differences among months for infiacommunity

diversity (ANOVA, F4, 61:5-44, p<0.01), evenness (ANOVA, F4, 61: 7.37, p<0.01),
species richness (ANOVA, F4? 61:7.28, p<0.01) and adjusted species richness (ANOVA,
F4, 61:5.47, p<0.01). There were significant differences among months for
infracommunity diversity (ANOVA, F3, 32:2.72, p=0.01), evenness (ANOVA, F3,
32=2.91, p<0.01), species richness (ANOVA, F3, 32:3.87, p<0.01) and adjusted species

richness (ANOVA, F3, 32:3.10, p<0.01) for the 2002 cohort of bluegill. The 2003 cohort

20

of bluegill had significant differences among months for infracommunity diversity

(ANOVA, F7. 223:5.89, p<0.01), evenness (ANOVA, F7. 223=7.59, p<0.01), species
richness (ANOVA, F7, 223=7.84, p<0.01) and adjusted species richness (ANOVA, F7,

223:7.24, p<0.01).
There were significant correlations between parasite infiacommunity diversity

(rs=0.13, p=0.01), species richness (rs=0.61, p<0.01) and adjusted species richness

(rs=0.58, p<0.01) of parasite infracommunities of bluegill and bluegill length,

irrespective of cohort and collection year. Although there were significant positive
correlations between all diversity metrics except evenness and bluegill length irrespective
of cohort, this was not always the case within each cohort. For the 2001 cohort of
bluegill, there were no significant correlations between parasite infracommunity diversity
and evenness and species richness and adjusted species richness and fish length. For the

2002 cohort of bluegill, there was a significant correlation between adjusted species

richness (rs=0.25, p=0.02) and fish length. The 2003 cohort of bluegill had significant
correlations between species richness (rs=0.30, p<0.01) and adjusted species richness

(rs=0.26, p<0.01) and fish length.

Largemouth Bass

Mean parasite infracommunity diversity, evenness, species richness and adjusted
species richness for YOY largemouth bass were 0.28 i 1.4 (0.03-0.50), 0.54 i 0.22
(0.10-0.83), 4.3 i 1.4 (2-7) and 3.7 i 1.3 (2-6) respectively. With the exception of

species richness, all values of all diversity metrics significantly increased with age.

21

There were significant correlations between infracommunity diversity (rs=0.55, p<0.01)

and evenness (rs=0.52, p=0.01) and adjusted species richness (rs=0.40, p=0.04) and

largemouth bass length.
Parasite Component Communities

Shannon diversity values (approximated variance) for the totaL enteric and
parenteric parasite component communities of bluegill irrespective of cohort were 0.14,
0.34 and 0.13, respectively. Age 0 bluegill had higher Shannon diversity values for the
total and parenteric parasite component community. The Shannon diversity values for the
total, enteric and parenteric parasite component communities of age 0 bluegill were 0.21,
0.09 and 0.21, respectively. Shannon diversity values for the totaL enteric and parenteric
component communities of largemouth bass were 0.40, 0.37 and 0.41 respectively, all of
which were higher than Shannon diversity values found in either juvenile or age 0
bluegill. There were no significant differences in Shannon diversity values between the
total and enteric or total and parenteric parasite component communities of juvenile
bluegill irrespective of cohort or YOY largemouth bass. There were no significant
differences between total parasite component communities of age 0 bluegill and YOY
largemouth bass from TL. The Jaccard’s coefficient for community similarity between
parasite component communities of age 0 bluegill and YOY largemouth bass was 0.53.
Mollusk Abundances

Individuals of the snail families Lymnaeidae, Planorbidae, Physidae, the genus
Viviparus sp. and the clam family Sphaeriadae were collected in TL. Abundances of
mollusks by taxonomic group and month are in Figure 4. Mollusk abundances generally

increased throughout July and August, declined through September and October and

22

declined between October and April. Mean number of trematodes per bluegill by month
and number of mollusks collected per month are in Figure 5. In general, abundances of

larval trematodes rose and fell in concert with mollusk abundances over the study period.

23

DISCUSSION

Parasites of Juvenile Bluegill and Young-of-the-year Largemouth Bass

Many of the parasite species found in the juvenile bluegill and YOY largemouth
bass from TL have been found in previous studies of parasites of bluegill and largemouth
bass in Michigan. Parasites of Michigan bluegill were summarized by Muzzall and
Peebles (1998). The present study of TL bluegill is the first report of Azygia sp.,
Coptogonimus sp., H. globulifonne, Actinocleidus sp. and Anchoradiscus sp. fi'om
Michigan bluegill. Reports on parasites of Michigan largemouth bass include Esch
(1971), Hudson et a1. (1994); Muzzall et a1. (1995); Hudson and Bowen (2002); Gillilland
and Muzzall (2004) and Muzzall and Gillilland (2004). The present study is the first
report of Azygia sp., Clinostomum sp., Cryptogonimus sp. metacercaria and adults,
Diplosromum sp., Neascus sp., P. minimum, Camallanus sp., monogene sp. A,
Trichodina sp. and Myxobolus sp. from Michigan largemouth bass.

The present study notwithstanding, 22 parasite species have been reported from
adult bluegill or bluegill of unknown age in Michigan (Muzzall and Peebles, 1998). Of
those 22 species, seven (31%) are represented by larval or immature stages; five of which
(23% of total parasite species) were larval trematodes. Prior studies of Michigan bluegill
parasites have primarily surveyed adults which have a lower percentage of larval parasite
species than juvenile bluegill in the present study. Parasites of juvenile bluegill in the
present study hosted 19 parasite species—nine species (47%) were represented by larval

or immature forms; five of which (26% of total parasite species) were larval trematodes.

24

Juvenile bluegill are an important intermediate host for many parasite species because
they are a prey item for many vertebrate species (Muzzall and Peebles, 1998).

Although adult bluegill fiom Michigan have a larger percentage of adult parasite
species (Muzzall and Peebles, 1998) than juvenile bluegill from the present study; 69%
adult parasite species in adult bluegill compared with 53% adult parasite species in
juvenile bluegill, similar percentages of the parasite species of adult and juvenile bluegill
fi'om TL are comprised of larval trematodes. Since larval trematodes are long-lived
(Spall and Summerfelt, 1970), it may be that many of the larval trematodes of adult
bluegill infect juveniles while they are living in the littoral zone. However, because mean
abundances of larval trematodes are sometimes not reported in studies of parasites of
Michigan adult bluegill (Esch, 1971), it is not known whether abundances of these
parasites continue to increase as fish age.

The present study is the first in Michigan to report on the entire parasite
community of largemouth bass, albeit largemouth bass were age 0. Esch (1971) did not
include monogenes or copepods; Hudson et al. (1994), Muzzall et al. (1995), and Hudson
and Bowen (2002) worked only with copepods; Gillilland and Muzzall (2004) reported
on P. amblopliris; and Muzzall and Gillilland (2004) worked only with acanthocephalan
parasites of largemouth bass.

Esch (1971) reported that the parasite communities of adult largemouth bass in
Michigan consisted of 83% adult parasite species and 17% larval or immature parasite
species. In TL, of the 13 parasite species infecting YOY largemouth bass, 62% were
adult parasite species and 46% of parasite species were represented by larval or immature

forms. Percentages of adult and larval or immature parasite species do not add up to

25

100% because Cryptogonimus sp. was represented by both adult and larval forms. A
greater percentage of the parasites of adult largemouth bass were adult species compared
to YOY largemouth bass. Due to their size, adult largemouth bass are much less
vulnerable to predation than YOY individuals; hence, parasite species using adult
largemouth bass as an intermediate host may not be able to complete their life cycle.
Additionally, since YOY largemouth bass spend more time in the littoral zone with snails
shedding cercariae than adults (Gilliam, 1982; Sammons and Maceina, 2005), YOY
largemouth bass should harbor more larval trematode parasite species than adults.

Neascus sp., P. minimum, Camallcmus sp., P. amblopliris, Spinitecrus sp. and N.
cylindrarus, have been reported from juvenile bluegill and YOY largemouth bass in
previous studies (Lernly and Esch, 1984; Fischer and Kelso, 1987, 1988, 1990; Camp,
1988; Landry and Kelso, 1999; Steinauer and Font, 2003). The mean abundances of
Cryptogonimus sp. found in the present study are the highest metacercarial mean
abundances reported in juvenile bluegill in the United States. In all previous studies of
parasite communities of juvenile bluegill, as well as in the present study, larval
trematodes had higher species richness and abundances than any other taxonomic group
of parasites (Fischer and Kelso, 1987, 1988, 1990; Landry and Kelso, 1999; Steinauer
and Font, 2003).
Prevalence and Mean Abundance of Most Common Parasites

Bluegill collected in 2003 had significantly higher mean abundances of
Coptogonimus sp., P. minimum, and Neascus sp. than bluegill in 2004. This is likely
because bluegill collected in 2003 were significantly larger than bluegill in 2004. The

oldest and longest cohort of bluegill, the 2001 cohort, was only collected in 2003.

26

Because bluegill from 2003, on average, were both older and larger than the bluegill from
2004, they had more time to acquire parasites and are more vulnerable to penetration by
trematode cercariae by having more exposed surface area (Spall and Summerfelt, 1970),
which led to higher mean abundances of Coptogonimus sp. metacercaria, P. minimum
and Neascus sp. Additionally, there were significant positive correlations between
abundance of the four most common parasites and length of bluegill irrespective of
cohort. Since parasite mean abundance and length of fish irrespective of cohort are
highly correlated, it follows that mean abundances of parasites were significantly higher
in 2003 than 2004.

In many cases, abundances of the most common parasites increased with
increased fish length and also varied monthly. As previously discussed, length plays a
role in mean abundance of larval trematode parasites because as a fish increases in
length, surface area that can be penetrated by a parasite increases. Length also plays a
role in larval trematode abundance because length and age in bluegill have a strong
positive correlation and as fish age, they have had more time to accumulate larval
trematodes. Month influences trematode abundances because water temperature, which
varies by month, influences whether a snail sheds cercariae and also whether cercariae
are sufficiently active to penetrate fish (Spall and Summerfelt, 1970). Cercariae of P.
minimum, for instance, are not produced at temperatures below 15° C and are not active
enough to penetrate fish at temperatures less than 18° C (Hoffman, 1958). During the
study period, water temperatures in TL were not above 18° C until May (Figure 3). Since
it takes approximately three weeks for the metacercariae of this species to be large

enough to be detected in the fish (Spall and Summerfelt, 1970), prevalence and mean

27

abundance of this parasite would not be expected to increase until June, 2004. Since
temperatures at TL were only recorded once a month during fish collection, it is not
known if the water temperature was consistently above 18° C through May, 2004.
Because the increase in prevalence and mean abundance was not observed until July
(Tables 5 and 6), it seems likely that water temperatures were not consistwa above 18°
C until June.

Parasites altering the behavior of their fish intermediate hosts, which may lead to
decreased fish survivorship, are well-documented (Barber et al., 2000, review;
Marcogliese et al., 2001; Shirakashi and Goater, 2002; Barber et al., 2004; Seppala et al.,
2004). In some cases, fish infected with parasites do not swim as well as uninfected fish
or seek cover from predators as do uninfected fish (Barber et al., 2000). Iffish with high
parasite burdens have reduced swimming ability or do not seek cover when a predator is
nearby, the fish with the highest abundances of parasites could be selectively preyed
upon. Likewise, by interfering with the vision of a fish (Crowden and Broom, 1980;
Brassard et al., 1982; Marcogliese et al., 2001; Shirakashi and Goater, 2002; Seppala et
al., 2004), a parasite may inhibit the ability of a fish to escape predation because the
predator cannot be as easily seen. If a bluegill intermediate host has a reduced ability to
escape a predator definitive host, the probability of parasite transmission increases.

Bluegill with the highest abundances of P. amblopliris may be experiencing some
type of indirect parasite-induced mortality. The 2001 and 2002 cohorts of bluegill from
TL had significantly higher prevalences of P. mnbloplitis than the 2003 cohort of
bluegill. When examining the relationship between abundance of this parasite and length

by cohort, there was a significant positive correlation for the 2003 cohort, a non-

28

significant negative correlation in the 2002 cohort and a significant negative correlation
between abundance and length of P. ambloplitis in the 2001 cohort of bluegill. This
suggests that as fish age, the direction and the strength of the relationship between P.
ambloplitis abundance and length becomes increasingly more negative. Because the
relationship between abundance of this parasite and length becomes more negative, it
may be that as fish age, the fish with the heaviest infections of P. ambloplitis are removed
fi'om the population in some way. There are many reports of parasite-induced host
mortality in fishes (Barber et al., 2000, review; Coyner et al., 2001; Marcogliese et al.,
2001; Shirakashi and Goater, 2002; Barber et al., 2004; Seppala et al., 2004).
Proreocephalus ambloplitis, which causes significant damage to the liver and viscera of
infected fish (Mitchell et al., 1983), was found in bluegill examined in the present study.
Livers of juvenile bluegill infected with this parasite were filled with necrotic tissue and
fibrous adhesions (B. Pracheil, personal observation) which likely led to poor health, and
perhaps, increased vulnerability to predation.

Another possible explanation for the decline of P. ambloplitis with age is that
juvenile bluegill may be eating fewer of the c0pepod intermediate hosts of this parasite.
Osenberg et al. (1992) reported that bluegill between 45 and 75 mm SL spend some time
foraging in limnetic areas of the lake. In the limnetic habitat, bluegill may not be
ingesting the copepod intermediate hosts for P. amblopliris as frequently as they did by
strictly foraging in the littoral zone of the lake as they did when they were younger.
However, this does not seem to be a likely explanation for decreases in prevalence and

mean abundance of P. ambloplitis because Wilson et al. (1996) found limnetic adult

29

bluegill from another Michigan lake had higher prevalence and mean abundance of P.
ambloplitis than fish of similar length in the littoral zone.

erogonimus sp. and Neascus sp. had the largest decreases in prevalence and
mean abundance accompanied by decreases in variance to mean abundance ratio between
October, 2003 and May, 2004 (Tables 5-8). Parasite populations are typically
overdispersed meaning many hosts have a few number of parasites and a few hosts have
a large number of parasites. A decrease in variance to mean abundance ratio implies that
after the decrease in mean abundance of these two parasite species from October through
April and from May through June in the 2002 cohort and fiom October through May in
the 2003 cohort, the overdispersion of these parasite species decreases. The decrease in
degree of overdispersion of larval trematode populations suggests that these decreases
may be due to mortality of the most heavily infected hosts (Kennedy, 1987). However,
other factors which cannot be measured in a field study such as immigration of less
heavily infected bluegill into the'population or mortality of parasites in the most heavily
infected bluegill could also produce a similar effect.

Heavy metacercaria] burdens have been reported to decrease survivorship of
juvenile bluegill. Lemly and Esch (1984), for instance, have experimentally shown that
heavy infections of the larval trematode Uvulifer ambloplitis (a Neascus-type species) to
be a causative agent for direct mortality of juvenile bluegill. Although the type of
parasite-induced host mortality was not speculated, Fischer and Kelso (1988) attributed
similar decreases in prevalence, mean abundance and variance to mean abundance ratio
of Allocanthochasmus sp., to death of the most heavily infected juvenile bluegill.

Indirect parasite-induced mortality of juvenile bluegill in TL caused by Cryptogonimus

3O

sp. and Neascus sp. may be responsible for the concurrent decreases in prevalence, mean
abundance and variance to mean abundance ratios of these parasites. Coptogonimus sp.,
the most prevalent and abundant species reported in the present study and Neascus sp.
were found largely in the muscle of the bluegill (Table 1) which could negatively impact
swimming ability. Cryptogonimus sp. was also found in the brain which may affect
cognition, on the gills which may influence gas exchange and waste removal and on the
posterior exterior surface of the eyes, which may affect vision.

Indirect parasite-induced mortality of YOY largemouth bass caused by selective
predation of the fish with the highest Coptogonimus sp. metacercariae abundances may
explain the significant negative correlation between abundance of Cryptogonimus sp.
metacercariae and fish length. Most YOY largemouth bass do not survive to age 1 and
mortality of many of them is due to predation by other juvenile and adult largemouth bass
(Post et al., 1998). For instance, Post et al. (1998) estimated that by August, between 91
and 99% of YOY largemouth bass have been eaten by older largemouth bass when YOY
populations ranged fi'om 24,000 — 94,000 individuals. As in juvenile bluegill,
Coptogonimus sp. metacercariae encyst largely in the muscle, but also in the brain and
on the gills, posterior exterior surface of the eye and on the gills. Metacercarial
encystment in these areas of the fish may lead to decreased swimming ability, vision
and/or gas exchange. In TL, if the YOY largemouth bass most heavily infected with
Coptogonimus sp. metacercariae are more vulnerable to predation, then the individuals
with the lowest metacercarial abundances survive leading to the negative correlation
between abundance of this parasite and length. Cryptogonimus sp. metacercariae

stunting the grth of the YOY largemouth bass could also explain the significant

31

negative correlation between Coptogonimus sp. abundance and fish length. In this case,
the YOY largemouth bass with the highest abundances of Coptogonimus sp.
metacercariae would have a slower growth rate than fish with lower abundances. The
larval trematode Neascus sp. has been shown to stunt the growth of juvenile bluegill
(Lemly and Esch, 1984) and a similar phenomenon could be occurring with
thogonimus sp. in TL largemouth bass.

In YOY largemouth bass, metacercarial abundances of Neascus sp. increased
significantly with increased length. These opposed relationships of metacercarial
abundances to length for erogonimus sp. and Neascus sp. may be due to habitat
partitioning by the snail hosts of these parasites. Physa sp., one reported snail host of
Neascus sp. (see Hoffman, 1999), is present in TL and is known to have variable habitat
use in response to predation pressure (Turner, 1996; Bemot and Whittinghill, 2003) and
parasite presence (Bemot, 2003 ). In response to these stimuli, snails may change their
position in the water column (Turner, 1996; Bernot and Whittinghill, 2003). In TL, YOY
largemouth bass were found in deeper areas of the littoral zone with less vegetation than
juvenile bluegill (B. Pracheil, personal observation), an observation that was also noted
by Fischer and Kelso (1990) in Louisiana. Ifsnails infected with Neascus sp. are sharing
this deeper, less vegetated habitat with YOY largemouth bass, these fish would be
vulnerable to penetration by Neascus sp. and may have an increase in abundance of this
parasite with length. However, since the snail host of Cryptogonimus sp. is not known, it
is not possible to say whether the behavior of the snail host of this parasite can also be

altered.

32

Parasite Infracommunities

In bluegill irrespective of cohort, parasite infracommunity diversity, species
richness and adjusted species richness have significant positive correlations with fish
length. This indicates that as a fish becomes older and longer, its parasite community
becomes more diverse. This is similar to the findings of Cloutrnan (1975) and Fellis and
Esch (2004) who reported increased parasite community diversity with increased adult
bluegill length. This suggests that overall, parasite infracommunity diversity
significantly increases with length, but length is not as important to diversity when
looking at a smaller time scale, such as within a cohort. As fish become older and longer,
they are able to eat a wider variety of parasite intermediate hosts, but they also increase
their probability of being penetrated by cercariae due to increased surface area. The
increase in larval trematode abundances, particularly Coptogonimus sp., may be
negating the positive effects on diversity caused by acquisition of more parasites through
ingestion. It may also be that parasite infracommunities of the 2001 and 2002 cohorts of
bluegill in TL have achieved maximum diversity and diversity measures will not increase
until these fish primarily inhabit limnetic areas and are exposed to different parasite
species from new intermediate hosts.

In the 2002 cohort, adjusted parasite species richness was significantly correlated
with bluegill length but species richness was not. This suggests that length of fish may
continue to be an important determinant of internal parasite communities, but not for
external parasite communities. In the 2003 cohort of bluegill, species richness was the
only diversity metric shown to be significantly influenced by length. It can be inferred

that the factors structuring the internal parasite infiacommunity and the entire parasite

33

infiacommunity may vary in juvenile bluegill with age, such as diet and habitat, or that
the factors structuring these communities may vary from year-to-year, such as
temperature.

In addition to a decrease in mean abundance of Captogonimus sp., Neascus sp.,
P. minimum and P. mnbloplitis in each cohort of juvenile bluegill in the spring, there are
also simultaneous decreases in infracommunity diversity and evenness values in the 2002
and 2003 cohorts between April and June, 2004. Cloutrnan (1975) also found bluegill
parasite community diversity values to decrease between April and May. In the present
study, the magnitude of the decreases in diversity and evenness is not equal; diversity has
a larger magnitude decrease than evenness. These decreases in infracommunity diversity
and evenness values are concurrent with the decrease in abundances of the most common
parasites. Based on data from the present study, the decrease in parasite mean abundance
in April through June, 2004 may have led to a restructuring of the parasite community.
This restructuring can be inferred fiom the decrease in the diversity to evenness ratio for
Cryptogonimus sp. between May and June in the 2002 cohort and between April and May
in the 2003 cohort. Because the drop in evenness is of a lower magnitude than the
decrease in diversity, parasite individuals are more evenly distributed among species after
the decrease in diversity and evenness. Increased evenness with respect to diversity
between April and June, 2004 is likely a result of the decreased mean abundance of
Cryptogonimus sp. and could also be brought about by increased mortality of heavily
parasitized juvenile bluegill.

Parasite infracommunity diversity, evenness, species richness and adjusted

species richness showed significant positive correlations with largemouth bass length.

34

This agrees with Cloutman (1975) who found that parasite community diversity of
largemouth bass older than 12 months increased with age. As largemouth bass become
older and longer, their gape size increases and allows them to eat a wider variety of prey,
especially when they attain a size at which they can eat fish. As largemouth bass
increase in size and become piscivorous, they eat juvenile bluegill serving as intermediate
hosts for parasites such as Coptogonimus sp. and P. ambloplitis. Parasite communities
of largemouth bass in TL are not dominated by larval trematodes to the degree that
parasite communities of juvenile bluegill are. Therefore, largemouth bass parasite
infracommunity diversity values are higher than those of bluegill because individuals of
the parasite species they harbor are more evenly distributed among species. Cloutman
(197 5) also found that parasite communities of largemouth bass older than 12 months
were more diverse and had fewer larval trematodes than bluegill older than 12 months.
Parasite Component Communities

The Shannon diversity values for the total, enteric and parenteric parasite
component communities of YOY largemouth bass are more similar to each other than
those of juvenile bluegill. There is also a difference (although not significant) between
Shannon diversity values for the total parasite component communities of age 0 bluegill
and YOY largemouth bass. The variance values for the Shannon diversity t-test are
approximated from the relative abundances of each species in a community. Since
parasite individuals in this community are not evenly distributed among species in
bluegill, a high variance value was generated. Variance values are a component of the
approximation for degrees of freedom and also serve as the denominator in the t-test.

High variance values lowers the degrees of fieedom and the t-value which influence test

35

significance. The differences in the diversities of the total, enteric and parenteric parasite
component communities of juvenile bluegill and total parasite component communities of
age 0 bluegill and YOY largemouth bass were non-significant. However, it may be that
this t-test may not be a robust method for detecting significant differences between
parasite component communities in TL because enteric diversity of juvenile bluegill was
(more than two times higher than either total or parenteric diversity and total diversity of
largemouth bass parasites was nearly twice that of age 0 bluegill. Because Shannon
diversity values for the parasite component community only generate one diversity value
per host species per site, as performed by Marcogliese and Cone (2001), other forms of
statistical tests are not applicable.

Some surveys of fish parasite communities only census parts of the fish or do not
include metacercarial abundances (Esch, 1971; Steinauer and Font, 2003). Results of the
present study indicate that parasite community diversity values obtained fiom
examination of certain parts of the fish may not be representative of the entire parasite
community. Juvenile bluegill from TL had similar total and parenteric component
community diversities, but the diversity of the enteric parasite component community is
more than twice that of either the parenteric or total parasite component communities.
The enteric parasite component communities of age 0 bluegill were much lower than the
total or parenteric parasite component communities. In TL largemouth bass, the total,
enteric and parenteric parasite component community diversities are similar. The present
study shows that depending on the host species and age and study area, the diversity of
the enteric component community may not be representative of total component

community. Total and parenteric parasite component communities of juvenile bluegill

36

from the present study were dominated by larval Coprogonimus sp. with very high mean
abundances relative to other parasite species in the community. Conversely, one parasite
species did not dominate the enteric parasite community; therefore, diversity values
derived only from enteric parasites are not an adequate descriptor of the total parasite
component community. In the case of juvenile bluegill from TL, the enteric parasite
component community diversity is an overestimate of total component community
diversity.

In the present study system, host life history can explain why age 0 bluegill have
very different total, enteric and parenteric parasite component community diversities and
YOY largemouth bass have similar totaL enteric and parenteric parasite component
community diversities. The parasite component communities of juvenile bluegill are
dominated by larval trematodes. Juvenile bluegill live in vegetated areas containing
mollusks that shed larval parasites that directly penetrate the fish (Wilson et al., 1996).
These juvenile bluegill acquire these parasites passively by sharing habitat with mollusks
that shed larval parasites.

Although the parasite communities of YOY largemouth bass are numerically
dominated by larval trematodes, their larger gape size allows them to prey on a wider
variety of intermediate hosts. Since largemouth bass are able to eat a wider variety of
intermediate hosts, the diet of YOY largemouth bass is a more influential parasite
community determinant than the diet of juvenile bluegill. Additionally, YOY largemouth
bass in TL were found in deeper, less vegetated water than juvenile bluegill (B. Pracheil,
personal observation). This deeper, less vegetated water may have less mollusks

shedding larval trematodes; hence, YOY largemouth bass do not acquire as many larval

37

trematodes as do juvenile bluegill. Furthermore, the distribution of parasite individuals
among species becomes more even due to the numerically lessened role of larval
trematodes in the parasite component community, leading to similar total, enteric and
parenteric parasite component community diversity in YOY largemouth bass.

Mollusk Abundances

Since larval trematodes, which are shed by mollusks and directly penetrate
bluegill, numerically dominated the parasite community of juvenile bluegill in TL,
mollusk abundance may have a large influence on parasite community structure. In
general, an increase in numbers of mollusks found in the sampling area in concert with
water temperature increasing above 18° (Hoffman, 1958) corresponded with an increase
in the number of trematodes found per fish (Figure 4 and 5).

In the present study, decreases in the mean number of larval trematodes per fish
cannot be directly attributed to decreases in mollusk numbers. Since metacercarial
parasites are thought to be long-lived and accumulate in a fish over time (Spall and
Summerfelt, 1970), a decrease in the mollusk abundances only has an effect on
recruitment of new parasite individuals (depending on water temperature). Fewer
mollusks may mean there are fewer larval parasites shed to penetrate fish. Decreases in
numbers of trematodes per fish may be attributed to a larger proportion of younger,
smaller fish examined in a month since younger fish have lower mean abundances of
larval trematodes. Mortality of the most heavily infected bluegill also could explain the
decline of the larval trematode community in concert with mollusk numbers in some
months.

Summary

38

Several prior studies in other areas of the United States have shown larval
trematodes to dominate the parasite fauna of juvenile bluegill (Fisher and Kelso, 1987,
1988, 1990; Landry and Kelso, 1999; Steinauer and Font, 2003). In some of these
studies, including the present study in TL, larval parasites, particularly larval trematodes,
have been implicated as potential causes of parasite-induced host mortality (Lemly and
Esch, 1984; Fischer and Kelso, 1988). This suggests that larval trematodes may be a
major selective pressure influencing the survivorship of juvenile bluegill.

In general, fish habitat and diet are the major determinants of parasite
communities. Because parasite communities are structured as functions of these
components, a better understanding of the diet and habitat of juvenile bluegill and YOY
largemouth bass can be gained through surveying their parasite fauna. Juvenile bluegill
in TL had an increase in parasite species richness with increased length and hence, with
increased age. As juvenile bluegill in TL age, the decreasing importance of fish length
on measures of parasite community diversity coupled with the recruitment of new
parasite species suggests diet and habitat variability among juvenile age classes in TL.
Finally, because fish parasite communities are firnctions of the diet and habitat of fish, the
differences in parasite community composition and total community diversity between
YOY bluegill and YOY largemouth bass in TL reinforces our knowledge of the diets and

habitats of these fishes.

39

CHAPTER TWO

PARASITE INFRAPOPULATIONS AND COMMUNITIES OF JUVENILE
BLUEGILL, LEPOMS AJACROCHIR US AND LARGEMOUTH BASS,
MICROPTERUS SALMOIDES IN GULL LAKE, MICHIGAN AND A COMPARISON
OF PARASITE COMMUNITIES BETWEEN GULL LAKE AND THREE LAKES H,

MICHIGAN

4o

INTRODUCTION

Fish habitat (Esch, 1971; Wilson et al., 1996), diet and age (McDaniel and Bailey,
1974; Cone and Anderson, 1977; Hanek and Fernando, 1978a, 1978b; Bailey, 1984) are
determining factors in the composition and structure of parasite communities in
centrarchid fishes. The habitat in which a fish resides largely determines which parasites
it may host. Habitat attributes such as substrate type, vegetation type and quantity play a
major role in parasite intermediate hosts found in an area. Mollusks serving as
intermediate hosts for trematode parasites, for instance, shed larval trematodes that may
infect a fish by direct penetration. By sharing habitat with these mollusks, fish may
become infected with these parasites. Habitat, in turn, influences diet by determining
what prey items (which may be serving as intermediate hosts) are available to a fish. For
example, copepods serve as intermediate hosts for several species of parasites that are
acquired by fish through ingestion.

As a fish ages, it increases in size and surface area. “fith increased surface area, a
fish increases its chances of becoming infected with parasites via direct penetration (Spall
and Summerfelt, 1970). Also, some larval parasites, such as Posrhodrplosromum
minimum, are long-lived and accumulate in a fish over several years (Spall and
Summerfelt, 1970; Hoffman, 1999). In bluegill, Lepomis macrochirus and largemouth
bass, Micropterus salmoides, age may influence parasite communities because juveniles
and adults have been shown to have different diets and habitats (Mittelbach, 1984;

Werner and Hall, 1988; Olson, 1996; Post, 2003; Sammons and Maceina, 2005).

41

The life history traits of juvenile bluegill and young-of-the-year (Y OY)
largemouth bass should contribute to the development of a parasite fauna unique to their
life stage. Adult bluegill spawn in vegetated littoral areas in May or June in Michigan
when water temperature reaches approximately 20° C (Breder, 1936; Werner, 1967;
Werner and Hall, 1988). After hatching approximately two weeks post-spawn (Breder,
1936), bluegill fry undergo a migration to the limnetic zone of a lake and remain there for
approximately six to eight weeks (Werner, 1967; Werner and Hall, 1988). Juvenile fish
then return to the vegetated littoral zone for the next two to three years (Werner and Hall,
1988) until they move to the limnetic zone of the lake for the duration of their life
(Werner and HalL 1988). The shift to the limnetic habitat gradually takes place in
bluegill between 45 and 75 mm SL (Osenberg et al., 1992). At approximately 75 mm SL,
bluegill switch to feeding almost exclusively in the limnetic zone of a lake (Werner and
Hall, 1988), which is approximately commensurate with maturity (Osenberg et al., 1992).

Throughout life, bluegill prey on aquatic invertebrates that serve as intermediate
hosts for many types of parasites (Zischke and Vaughn; 1962; Werner, 1969; McDaniel
and Bailey, 1974; Sadzikowsi and Wallace, 1976; Cone and Anderson, 1977; Werner and
Hall, 1988; Fisher and Kelso, 1990). However, the invertebrate prey available in the
limnetic zone where bluegill spend their adult life differs fiom that available in the
vegetated littoral zone where they live as juveniles (Mittelbach, 1984; Werner and Hall,
1988). This shift in diet and habitat may cause the parasite fauna to concurrently shift
(Wilson et al., 1996). Additionally, the vegetated habitat of juvenile bluegill is habitat for
many mollusks that serve as intermediate hosts for trematodes that shed larval parasites

that directly penetrate bluegill (Wilson et al., 1996).

42

Largemouth bass spawn in April or May in Michigan in vegetated littoral areas
(Breder, 1936) when the water temperature reaches approximately 15-18° C (Mittelbach
and Persson, 1998). The YOY largemouth bass remain in the littoral zone for the first
few weeks to months of life feeding on invertebrates (Gilliam, 1982; Olson, 1996; Post,
2003). When largemouth bass become large enough to eat fish, they switch to a
piscivorous diet, primarily preying on juvenile bluegill (Gilliam, 1982; Olson, 1996; Post,
2003) and continue to prey on fishes throughout their life. Since largemouth bass eat
aquatic invertebrates such as copepods, arnphipods and mayflies for the first few weeks
to months of life (Sule, 1981; Gilliam, 1982; Fischer and Kelso, 1990; Olson, 1996;
Dibble and HarreL 1997; Post, 2003), they may acquire parasites that use these
invertebrates as intermediate hosts. As is the case with juvenile bluegill, while living in
the vegetated littoral zone, largemouth bass are vulnerable to colonization by larval
trematodes shed by mollusks. Since largemouth bass become piscivorous early in life,
primarily eating juvenile bluegill, they may acquire parasites that use bluegill as
intermediate or paratenic hosts.

Because juvenile and adult bluegill and juvenile and adult largemouth bass have
different habitats and diets, parasite faunas should differ between juvenile (pre-
reproductive) and adult (reproductively mature) fish. Most studies on the parasites of
bluegill and largemouth bass are restricted to the examination of adult fish or fish of
unknown age (see Hoffman, 1999 for a list of studies of bluegill parasites). Few studies
report on changes in bluegill parasite communities with host age (McDaniel and Bailey,
1974; Cloutman, 1975) and only one study examines parasite community dynamics of

largemouth bass with host age (Cloutman, 1975).

43

Studies on the parasite communities of juvenile bluegill and YOY largemouth
bass are limited to Fischer and Kelso (1987, 1988, 1990), Landry and Kelso (1999) and
Steinauer and Font (2003). All these studies were conducted in Louisiana which may not
be indicative of the parasite communities of these fish in Michigan. Effects of fish age
on parasite community composition and structure in juvenile bluegill and YOY
largemouth bass were also not examined in the above studies. Fisher and Kelso (1987,
1988, 1990), Landry and Kelso (1999) and Steinauer and Font (2003) reported that
parasite communities of juvenile bluegill and YOY largemouth bass were dominated by
larval trematodes. However, not all larval trematodes in these studies were counted so
the numeric role and the effect these parasites have on parasite community diversity of
juvenile bluegill and YOY largemouth bass is not known.

The objectives of this study were to determine patterns of parasite infrapopulation
abundance and prevalence for the most common parasites of three cohorts of the most
common parasites of juvenile bluegill (Coptogonimus sp., Posthodrplostomum minimum,
Neascus sp. and Diplosromum sp.) and YOY largemouth bass (Coptogonimus sp. adults,
Coptogonimus sp. metacercariae, Pomphorhynclurs bulbocolli and Cwnallcmus sp.); to
determine patterns of parasite infracommunity diversity in juvenile bluegill; to describe
parasite component community diversities in juvenile bluegill and YOY largemouth bass;
and finally, to compare parasite communities of juvenile bluegill and YOY largemouth

bass from Three Lakes H and Gull Lake, Michigan.

44

MATERIALS AND METHODS

Description of Study Site

Gull Lake (Figure 6) (referred to as GL from hereafter) is a mesotnophic lake of
glacial origin located within Kalamazoo and Barry Counties in southwestern Michigan
(Dexter, 1996). This surface area of the lake is 2,030 acres and it has a maximum depth
of 110 feet (Dexter, 1996). Several springs along the lakeshore feed GL in addition to
five inlets; Prairieville Creek at the north side, Long Lake, Miller Lake and Grass Lake at
the west side and Wintergreen Lake on the east side. Gull Creek serves as the lake’s only
'outlet (Dexter, 1996).
Fish Collection and Examination

Collection of fish took place in Miller’s Marsh, a shallow area (<2 m) on the west
side of the lake where the yellow pond lily, Nuphar Iutea was the dominant vegetation.
Bluegill were collected by seine in August through September, 2003 and May through
June, 2004. Largemouth bass were collected in July through October, 2003. Upon
collection, fish were placed in aerated coolers and transported to the laboratory at
Michigan State University. Fish fiom GL were examined as described in Chapter One.
Parasite Preparation and Identification

Parasites were prepared and identified as described in Chapter One.
Parasitological Terminology

Ecological terms as used in the present study are defined in Chapter One. The
most common parasite species were defined as countable parasite species with greater

than 30% prevalence (arbitrarily determined) in each host species.

45

Data Analysis

Names of fish cohorts correspond to the year those fish hatched. For example,
fish that hatched in 2003 are referred to as the 2003 cohort of fish. The 2002 cohort of
bluegill consisted of age 1 fish collected in August and September, 2003; and the 2003
cohort of bluegill consisted of age 0 fish collected in August and September, 2003 and
age 1 fish collected in May- July, 2004. No fish with mature gonads were examined in
the present study. However, since no fish from the 2002 cohort were collected in the
2004 sampling year, by-cohort analyses were not conducted. Calculation and use of
diversity values in the present study are presented in Chapter One.

Mean parasite abundance values are expressed as mean 1 standard deviation (SD)
(maximum). Mean fish length values and mean parasite infracommunity diversity,
evenness, species richness and adjusted species richness values are expressed as mean i
SD (range). Parasite abundance, Brillouin’s diversity and evenness values, species
richness and adjusted species richness data were natural log transformed.

All statistical comparisons were considered significant at the c=0.05 level. Due
to small sample sizes, all analyses for juvenile bluegill parasites are conducted
irrespective of fish cohort. All analyses comparing bluegill and YOY largemouth bass
use age 0 bluegill. Chi-square analyses were used to infer Significant differences in
prevalence by using numbers of fish infected and uninfected with the most common
parasites of bluegill irrespective of fish cohort between sampling years. An unpaired t-
test was used to detect significant differences in mean abundances of the most common
parasites, mean Brillouin’s diversity and evenness, parasite species richness and adjusted

parasite species richness for juvenile bluegill irrespective of fish cohort between

46

sampling years. An unpaired t-test was also used to detect significant differences in
Brillouin’s diversity and evenness and species richness and adjusted species richness of
parasite infracommunities of juvenile bluegill between GL and TL.

A Spearman’s rank correlation was used to detect relationships between
untransformed abundance of the most common parasite species, untransformed
Brillouin’s diversity and evenness and untransformed species richness and adjusted
species richness and fish length for juvenile bluegill and YOY largemouth bass
irrespective of cohort and sampling year.

A t-test for Shannon diversity values was used to compare enteric and parenteric
component community diversity values to total component community diversity values
and also to compare total component community diversity between juvenile bluegill and
YOY largemouth bass. This t-test was also used to detect significant differences in
parasite component communities of juvenile bluegill and YOY largemouth bass between
GL and TL. Variance of parasite component community diversity for bluegill and

largemouth bass was approximated by:

s2 = Zfi logzfi — (2‘51? 102 filz n‘1
n

where fl: number of individuals of each species, and n= number of individuals of all

species (Brower et al., 1993), for the test statistic:

1: H1’ —H2’
(S12+S22)1/2

 

(Brower et al., 1993) which is compared to the Student’s t-distribution with a = 0.05 and

degrees of fi'eedom approximated by:

47

DF = ( S2H1’ + $211202
LS‘HI’)‘ + LS-HZ’)’
n1 n2

(Brower et al., 1993).

Fish of the same age and cohort were used when comparing Shannon diversity values
and Jaccard’s coefficients between lakes and fish species.

Mollusk Collection

Snails were collected, identified and counted as described in Chapter One.

48

RESULTS

Host Demographics

A total of 117 juvenile bluegill (52 fiom 2003 and 65 from 2004) and 86 young-
of—the-year largemouth bass were examined. The mean length of juvenile bluegill
irrespective of cohort for the 2003 and 2004 sampling years were 41.0 i 13.0 mm (19-55
mm) and 35.2 i 4.8 mm (26-48 mm), respectively. There was no significant difference
in length of bluegill between years in this lake. The 2002 cohort of juvenile bluegill
consisted of 33 age 1 fish from the 2003 sampling year with a mean length of 48.8 i 3.4
mm (43-55 mm). The 2003 cohort of juvenile bluegill consisted of 19 age 0 fish from the
2003 sampling year with a mean length of 25.2 i 4.7 mm (19-37 mm) and 65 age 1 fish
fiom the 2004 sampling year with a mean length of 35.2 _+_: 4.8 mm (26—48 mm). Eighty-
six age 0 YOY largemouth bass were collected in July- October, 2003 with a mean length
of 37.0 i 9.4 mm (21—61 mm). Water temperatures by month from GL are found in
Figure 3.
Parasites of Juvenile Bluegill and Young-of-the-Year Largemouth Bass

Prevalence and mean abundance 33 SD (maximum) for all parasite species of
juvenile bluegill by sampling year are in Table 14. Juvenile bluegill were infected with
6634 countable parasites from 11 species: five trematodes, Azygia sp., Coptogonimus
sp., Diplostomum sp., Neascus sp. and P. minimum; two cestodes, Proreocephalus
ambloplitis and Haploborhrium globuliforme, three acanthocephalans, Leptorhynchoides
thecatus, Neoechinorhynchus cylindmrus and Pomphorhynchus bulbocolli; and one

nematode, Spinitectus sp. Five species of non-countable parasites also infected juvenile

49

bluegill: three monogenes, Actinocleidus sp., Anchoradrscus sp. and Monogenea sp.; and
two protozoans: Myxobolus sp. and Trichodina sp. Some individuals of
Pomphorhynchus bulbocolli, Spinirectus sp., Actimcleidus sp. and Anchoradiscus sp.
were gravid adults. Parenteric larval parasites, Cryptogonimus sp., Diplostomum sp.,
Neascus sp., P. minimum, P. wnbloplitis, H. globuliforme and N. cylindratus comprised
99.0% of all parasite individuals counted. Coprogonimus sp. metacercariae accounted
for 88.9% of all parasite individuals counted.

Prevalence and mean abundance : SD (maximum) for parasites of YOY
largemouth bass are in Table 15. Young-of-the-year largemouth bass were infected with
3297 countable parasites from 12 species: six trematodes, Azygia sp., Clinosromum sp.,
Cryptogonimus sp., Diplosromum sp., Neascus sp. and P. minimum; one cestode, P.
ambloplitis; three acanthocephalans, L. thecarus, N. qylindratus and P. bulbocolli; and
two nematodes, CamaIlanus sp. and Spinitectus sp. Four species of non-countable
parasites: two monogenes, Monogenea sp. and Monogene sp. A; and two protozoans,
Myxobolus sp. and T richodina sp. also infected YOY largemouth bass. Both adults and
metacercariae of Coptogonimus sp. were found as well as enteric and parenteric L.
thecatus. Some individuals of Monogene sp. A, Coptogonimus sp. and Camallanus sp.
were gravid adults. Parenteric larval parasites, Clinosromum sp., Coptogonimus sp.
metacercariae, Diplosromum sp., Neascus sp., P. minimum, P. ambloplitis and L. thecatus
accounted for 44.4% of all parasites counted. Coptogonimus sp. metacercaria, which
had the highest prevalence and mean abundance, accounted for 41.6% of all parasites

counted. Although juvenile bluegill and YOY largemouth bass had several parasite

50

species in common, larval trematodes comprised a much larger part of the parasite
community in juvenilebluegill than in YOY largemouth bass.

Parasite species common to TL and GL bluegill were the monogenes,
Actinocleidus sp. and Anchoradiscus sp.; the trematodes, Azygia sp., Coptogonimus sp.,
Diplosromum sp., Neascus sp. and P. minimum; the cestodes, P. amblopliris and H.
globuliforme, the acanthocephalans, N. cylindratus and P. bulbocolli; the nematode,
Spinitectus sp.; and the protozoans, Myxobolus sp. and T richodina sp.

Prevalence and Mean Abundance of Most Common Parasites

The most common parasite species by host species were as follows: bluegill;
Cryptogonimus sp., Posthodiplosromum minimum, Diplostomum sp., and
Pomphorhynchus bulbocoIIi; largemouth bass: Cryptogonimus sp. adults, Coptogonimus
sp. metacercaria; Pomphorhynchus bulbocolli and Cwnallanus sp. Gull Lake bluegill
had significantly higher prevalences of Coptogonimus sp. (X2=10.05, p<0.01), P.

minimum (X2=34.65, p<0.01), Diplostomum sp., (X2= 18.20, p<0.01) and P. bulbocolli

(X2=24.67, p<0.01) in the 2004 sampling year than in 2003. In 2004, bluegill fiom GL

had significantly higher mean abundances of P. minimum (t=-5.85, p<0.01, 83 d.f.) and
Diplostomum sp. (t=-10.47, p<0.01, 68 d.f.) than in the 2003 sampling year. There was
no significant difference in mean abundance between years for the other most common
parasite species.

In GL bluegill, significant correlations were detected between abundance of

Coptogonimus sp. (rs=0.63, p<0.01), P. bulbocolli (rs=0.38, p<0.01) and bluegill length

(irrespective of cohort). In largemouth bass, there were significant correlations between

51

abundance of Cryptogonimus sp. metacercariae (rs= -0.52, p<0.01), P. bulbocolli

(rs=0.61, p<0.01), CamaIlanus sp. (rs= -0.37, p<0.01) and fish length.

Parasite Infracommunities

Brillouin’s diversity, evenness, species richness and adjusted species richness of
parasite infracommunities of juvenile bluegill by sampling year are in Table 16. Bluegill
collected in 2004 from GL had significantly higher Brillouin’s diversity (t= -5.55,
p<0.01, 117 d.f.) and evenness (t= -4.28, p<0.01, 92 d.f.), species richness (t= -4.42,
p<0.01, 85 d.f.) and adjusted species richness (t= -4.65, p<0.01, 82 d.f.) than bluegill
collected in 2003.

There were significant correlations between parasite infracommunity diversity
(rs=0.13, p=0.01), species richness (rs=0.61, p<0.01), adjusted species richness (rs=0.58,

p<0.01) and bluegill length. Mean diversity, evenness, species richness and adjusted
species richness of parasite infracommunities of GL largemouth bass were 0.27 i 0.14
(0-0.59), 0.57 i 0.25 (0-1), 3.8 i 1.8 (1.9) and 3.5 i 1.6 (1-8), respectively. In

largemouth bass, there were significant correlations between infracommunity diversity

(rs=0.55, p<0.01), evenness (rs=0.52, p=0.01) and adjusted species richness (rs=0.40,

p=0.04) and fish length.
Parasite Component Communities

The Shannon diversity values of the total, enteric and parenteric parasite
component communities of bluegill were 0.22, 0.38 and 0.21, respectively. The Shannon
diversity values of the total, enteric and parenteric parasite component communities of

age 0 bluegill were 0.24, 0.25 and 0.12, respectively. The Shannon diversity values for

52

the total, enteric and parenteric component communities of largemouth bass were 0.65,
0.53 and 0.13 respectively. There were no significant differences between total, enteric
or parenteric parasite component communities of bluegill or YOY largemouth bass or in
total parasite component communities between age 0 bluegill and YOY largemouth bass.
The Jaccard’s coefficient of community similarity for the parasite component
communities of age 0 bluegill and YOY largemouth bass from GL was 0.47.
Mollusk Abundances

Abundances of mollusks by taxonomic group and month in GL are in Figure 8.
Five taxonomic groups of mollusks were collected in GL; the snail families Planorbidae,
Physidae and the snail genus Viviparus sp.; the clam family Sphaeriadae and the zebra
musseL Dreissena sp. Mollusk abundances generally declined between July and
September and increased between June and July, 2004. Mean number of larval
trematodes per bluegill by month and number of mollusks (excluding zebra mussels,
which are not known to host any trematodes found in GL bluegill) collected per month
are in Figure 8. Abundances of larval trematodes per bluegill decreased between August
and September, 2003 and increased between June and July, 2004. Similarly, mollusk
abundances decreased between August, 2003 and June, 2004 and increased between June
and July, 2004.
Parasite Community Comparisons Between Three Lakes H and Gull Lake

Irrespective of cohort, bluegill from GL had significantly higher mean Brillouin’s
diversity (t = -4. 18, p<0.01, 259 d.f.) and evenness (t = -2.43, p=0.02, 68 d.f.) than
bluegill from TL. Irrespective of cohort, bluegill from TL had significantly higher mean

species richness (t = -4.86, p<0.01, 65 d.f.) and adjusted species richness (t = -4.63,

53

p<0.01, 64 d.f.) than bluegill from GL. There were no significant differences in
Brillouin’s diversity, evenness, species richness or adjusted species richness of parasite
infracommunities of YOY largemouth bass between GL and TL.

Total, enteric and parenteric parasite component community diversity values by
lake and host species are in Figure 9. There were no significant differences in parasite
component communities of bluegill between GL and TL or in largemouth bass between
GL and TL although total component community diversity for each host species was
highest in GL. J accard’s coefficient for community similarity for parasite component
communities of bluegill fi'om TL and GL was 0.74 (Figure 10). Largemouth bass from
GL and TL had a Jaccard’s coefficient of parasite component community similarity of

0.93.

54

DISCUSSION

Parasites of Juvenile Bluegill and Young-of-the-Year Largemouth Bass

Many of the parasites found in the juvenile bluegill and YOY largemouth bass
from GL in the present study have been found in previous studies of parasites of these
fish in GL (Esch, 1971; Muzzall et al., 1995; Gillilland and Muzzall, 2004; and Muzzall
and Gillilland, 2004). The present study is the first report of Azygia sp., Coptogonimus
sp., Diplosromum sp., Neascus sp., P. minimum, Haploborhrium globuliforme,
Neoechinorhynchus cylindrarus, Actinocleidus sp., Anchoradisacs sp., Myxobolus sp. and
Trichodina sp. from GL bluegill; and Clinostomum sp., Cnptogonimus sp. metacercaria
and adults, Diplostomum sp., Neascus sp., P. minimum, CamaIlwrus sp., monogene sp. A,
Trichodina sp. and Myxobolus sp. from GL largemouth bass.

The present study notwithstanding, 22 parasite species have been reported from
adult bluegill or bluegill of unknown age in Michigan (Muzzall and Peebles, 1998
review). Of those 22 species, seven (31%) were represented by larval or immature
stages; five of which (23% of total parasite species) were larval trematodes. Prior studies
of Michigan bluegill parasites have largely surveyed adults which have a much lower
percentage of larval parasite species than juvenile bluegill in the present study. Juvenile
bluegill in GL hosted 15 parasite species; eight species (53%) were represented by larval
or immature forms; four of which (27% of total parasite species) were larval trematodes.
Juvenile bluegill are an important intermediate host for many parasite species because

they are a prey item for many vertebrate species (Muzzall and Peebles, 1998).

55

Although adult bluegill fi'om Michigan have a larger percentage of adult parasite
species (Muzzall and Peebles, 1998) than juvenile bluegill from the present study, similar
percentages of the parasite species of adult and juvenile bluegill fiom GL are comprised
of larval trematodes. Since larval trematodes, are long-lived (Spall and Summerfelt,
1970), it may be that many larval trematodes of adult bluegill infect bluegill while they
are juveniles living in the littoral zone. However, because mean abundances of larval
trematodes are sometimes not reported in studies of parasites of Michigan adult bluegill
(Esch, 1971), it is not possible to know whether abundances of these parasites continue to
increase as fish age.

The present study is the first in Michigan to report on the entire parasite
community of largemouth bass, albeit largemouth bass in the present study are age 0.
Esch (1971) did not include monogenes or copepods; Hudson et al. (1994), Muzzall et al.
(1995), and Hudson and Bowen (2002) worked only with copepods; Gillilland and
Muzzall (2004) reported on P. ambloplitis", and Muzzall and Gillilland (2004) worked
only with acanthocephalan parasites of largemouth bass.

Esch (1971) reported parasite communities of adult largemouth bass in Michigan
to consist of 83% adult parasite species and 17% larval or immature parasite species. In
the present study in GL, of the 14 non-protozoan parasite species reported from YOY
largemouth bass, 57% consisted of adult parasite species and 57% of parasite species
were represented by larval or immature forms. Percentages of adult and larval or
immature parasite species do not add up to 100% because Coptogonimus sp. and L.
thecatus were represented by both adult and larval or immature forms. A greater

percentage of the parasites of adult largemouth bass consist of adult species than in YOY

56

largemouth bass. Due to their size, adult largemouth bass are much less vulnerable to
predation than YOY largemouth bass; hence, parasite species using adult largemouth bass
as an intermediate host may not be able to complete their life cycle.

Posrhodiplosromum minimum, Camallanus sp., P. ambloplitis and N. cylindratus,
have been reported from juvenile bluegill and largemouth bass in previous studies
(Fischer and Kelso, 1987, 1988, 1990; Camp, 1988; Landry and Kelso, 1999; Steinauer
and Font, 2003). The mean abundances of Coptogonimus sp. reported in the present
study are the highest metacercarial mean abundances reported in juvenile bluegill in the
United States. In all previous studies of parasite communities of juvenile bluegilL as well
as in the present study, larval trematodes had higher species richness and abundances
than any other group of parasites (Fischer and Kelso, 1987, 1988, 1990; Landry and
Kelso, 1999; Steinauer and Font, 2003).

Prevalence and Mean Abundance of Most Common Parasites

Posthodiplostomum minimum had significantly higher mean abundance in 2004
than in 2003. Fish accumulate P. minimum metacercariae as they age (Hoffman, 1958;
Spall and Summerfelt, 1970). Bluegill collected in 2004 should have higher mean
abundances of this parasite because they were, on average, older than fish in 2003.

Indirect parasite induced mortality caused by selective predation on the YOY
largemouth bass with the highest Captogonimus sp. metacercariae abundances may
explain the significant negative correlation between abundance of Coprogonimus sp.
metacercariae and fish length. Most YOY largemouth bass do not survive to age 1 and
mortality of many of them is due to predation by other juvenile and adult largemouth bass

(Post et al., 1998). For instance, Post et al. (1998) estimated that by August, between 91

57

and 99% of YOY largemouth bass have been eaten by older largemouth bass when YOY
populations ranged from 24,000 - 94,000 individuals. As in juvenile bluegill,
Coptogonimus sp. metacercariae encyst largely in the muscle, but also in the brain and
on the gills, posterior exterior surface of the eye and on the gills. Metacercarial
encystment in these areas of the fish may lead to decreased swimming ability, vision
and/or gas exchange. In GL, if the YOY largemouth bass most heavily infected with
Coptogonimus sp. metacercariae are more vulnerable to predation, then the individuals
with the lowest metacercarial abundances survive leading to the negative correlation
between abundance of this parasite and length.

This significant negative correlation between Cryptogonimus sp. metacercariae
abundance and YOY largemouth bass length could also be explained by Coprogonimus
sp. stunting the grth of the YOY largemouth bass. In this case, the YOY largemouth
bass with the highest abundances of Coptogonimus sp. metacercariae would have a
slower growth rate than fish with lower abundances. The larval trematode Neascus sp.
has been shown to stunt the growth of juvenile bluegill (Lemly and Esch, 1984) and a
similar phenomenon could be occurring with Cryptogonimus sp. in GL largemouth bass.

Abundance of Cmnallanus sp., which uses a copepod intermediate host, also had
a significant negative correlation with fish length. As largemouth bass become older and
attain a gape size large enough to eat fish, they transition from a diet of zooplankton and
benthic invertebrates to piscivory (Olsen, 1996; Post, 2003). Since larger fish that have
switched to piscivory may be eating copepods less fiequently than they are eating smaller
fish (Gilliam, 1982), abundance of Camallanus sp. might be expected to drop as

largemouth bass become longer. Alternatively, Camallanus sp. has been reported in

58

centrarchid fishes as having seasonal fluctuations in prevalence and abundance, with both
having their peak in the summer and declining throughout the fall months (Spall and
Summerfelt, 1969; Stromberg and Crites, 1975; Steinauer and Font, 2003). As the
largemouth bass in the present study became older and longer, it may be that the
abundance of this parasite declined due to parasite senescence.

Two acanthocephalan species, P. bulbocolli and L. thecatus use amphipod
intermediate hosts and had significant increases in abundances with bluegill length.
Leptorhynchoides thecatus can use juvenile bluegill, a major prey-item for YOY
largemouth bass, as a paratenic host (see Hoffman, 1999). Largemouth bass become
infected with L. thecatus when they eat juvenile bluegill. Bluegill can also serve as
definitive hosts for P. bulbocolli (see Hoffinan, 1999). It has been shown that adults of
Pomphorhynchus laevis, a congener of P. bulbocolli, can be transmitted post-cyclically,
from the intestine of one fish to another (Kennedy, 1999). Instead of eating the
amphipod intermediate host in this case, the largemouth bass may be acquiring this
parasite by preying upon juvenile bluegill hosting this worm, which cannot occur until
largemouth bass reach sufficient size. Since P. bulbocolli has a large bulb that becomes
imbedded in the intestinal wall and grows larger as worms become older, it does not seem
likely that large adult worms could be transmitted in this way. It may be that younger,
smaller P. bulbocolli that have not fully imbedded themselves in the intestinal wall could
be transmitted post-cyclically.

Parasite Infracommunities
Bluegill collected in 2004 had significantly higher mean Brillouin’s diversity and

evenness, species richness and adjusted species richness for the parasite infiacommunity

59

than bluegill from 2003. This is caused by a decrease in the abundance of
Coptogonimus sp. and an increase in the abundances of several other parasite species in
2004 (Table 16).

There were significant positive correlations between parasite infracommunity
diversity, species richness, adjusted species richness and length of juvenile bluegill. Fish
length is an important determinant of parasite community richness. Parasite communities
of adult bluegill have been shown to become more diverse with age (Cloutman, 1975).
As bluegill increase in length and age in GL, they eat a larger variety of prey due to
increased gape size and also eat more which increases the probability of acquiring a
parasite via ingestion of an intermediate host. At 45-75 mm in SL, juvenile bluegill
begin to forage in open water habitat (Osenberg et al., 1992). As fish begin to forage in
this open water habitat, they eat intermediate hosts of new parasites and spend less time
in the littoral zone where they are exposed to large numbers of Coprogonimus sp. I
cercariae. Both the decreased exposure to cercariae and exposure to new parasites by
ingestion of intermediate hosts leads to increased parasite community diversity in
juvenile bluegill.

Infracommunity diversity and adjusted species richness have significant positive
correlations with largemouth bass length. Because adjusted species richness has a
significant positive correlation with length and species richness does not, this suggests
that monogene and protozoan communities are not as heavily influenced by fish length as
the internal parasite community. Species richness of monogenes and protozoans may be
independent of length whereas species richness of countable parasite species are not.

Monogenes and T richodina sp. have direct life cycles and are acquired passively by the

60

fish which, in this system, may not be as dependent on fish length and acquisition of
these parasites may be more heavily influenced by factors such as proximity to another
fish host. Ifa fish is closer to a fish infected with a monogene or Trichodina sp., these
parasites may have an easier time finding another fish host. Myxobolus sp., which was
not a countable species, may be influenced by proximity to the tubificid worm
intermediate host. Since life cycles of centrarchid species of Myxobolus sp. are not
known, it is unclear whether length is a factor in presence of this parasite. In salmonid
fishes, Myxobolus cerebralis recruitment by the fish may be someth length dependent
in small fish because the infective stage to the fish host, the triactinomyxon spore, is
released from the tubificid worm and penetrates the skin of the fish (Gilbert and Granath,
2003). Ifcentrarchid fishes are infected with Myxobolus sp. in the same way, length may
play a role in recruitment of this parasite because as a fish increases in length, they have
more surface area to potentially be penetrated by the triactinomyxon spore. The
countable parasites in this system are acquired both passively by fish, through cercarial
penetration, and actively, through ingestion of an intermediate host. For countable
parasites the actively acquired parasites are still a function of length because as fish
increase in length, they have a larger gape size which allows them to eat a wider variety
of prey that may be serving as intermediate hosts. Also, as fish become longer, they have
greater surface area thus increasing the probability of being penetrated by cercariae.
Parasite Component Communities

The Shannon diversity values for the total, enteric and parenteric parasite
component communities of YOY largemouth bass are less different than those of juvenile

bluegill. There is also a difference (although not significant) between Shannon diversity

61

values for the total parasite component communities of age 0 bluegill and YOY
largemouth bass. The variance values for the Shannon diversity t-test are approximated
from the relative abundances of each species in a community. Since parasite individuals
in this community are not evenly distributed among species in bluegill, a high variance
value was generated. Variance values are a component of the approximation for degrees
of freedom and the denominator in the t-test. High variance values lower the degrees of
freedom and the t-value, both of which influence test significance. The difi‘erences in the
diversities of the totaL enteric and parenteric parasite component communities of juvenile
bluegill and total parasite component communities of age 0 bluegill and YOY largemouth
bass were non-significant. However, it may be that this t-test may not be a robust method
for detecting significant differences between parasite component communities in TL
because enteric diversity of juvenile bluegill was nearly two times higher than either total
or parenteric diversity and total diversity of largemouth bass parasites was nearly three
times higher than that of age 0 bluegill. Because Shannon diversity values for the
parasite component community only generate one diversity value per host species per
site, as performed by Marcogliese and Cone (2001), other forms of statistical tests are not
applicable.

Some surveys of fish parasite communities only census parts of the fish or do not
include metacercarial abundances (Esch, 1971; Steinauer and Font, 2003). Results of the
present study indicate that parasite community diversity values obtained from
examination of certain parts of the fish may not be representative of the entire parasite
community. In the case of juvenile bluegill from GL, the total diversity of the component

community was similar to the diversity of the parenteric component community, but the

62

diversity of the enteric parasite component community is more than twice that of either
the parenteric or total parasite component communities. Total and parenteric parasite
component communities of juvenile bluegill fi‘om the present study weredominated by
larval Cryptogonimus sp. with very high mean abundances relative to other parasite
species in the community. Conversely, one parasite species did not dominate the enteric
parasite community; therefore, diversity values derived only fi'om enteric parasites are '
not an adequate descriptor of the total parasite component community. Enteric parasite
component community diversity is an overestimate of total component community
diversity for GL juvenile bluegill. In GL largemouth bass, the total component
community diversity is similar to enteric component community diversity, but much
larger than parenteric component community diversity. In GL YOY largemouth bass,
parenteric component community diversity is an underestimate of total diversity. The
present study suggests that depending on the host species and study area, the diversity of
the enteric component community may not be representative of total component
community.

In the present study system, host life history can explain why age 0 bluegill have
very different total, enteric and parenteric parasite component community diversities and
YOY largemouth bass have similar total, enteric and parenteric parasite component
community diversities. The parasite component communities of juvenile bluegill are
dominated by larval trematodes. Juvenile bluegill live in vegetated areas containing
mollusks that shed larval parasites that directly penetrate the fish (Wilson et al., 1996).
These juvenile bluegill acquire these parasites passively by sharing habitat with mollusks

that shed larval parasites.

63

When YOY largemouth bass begin eating bluegill, diet becomes a more important
factor in the acquisition of parasites. Through their diet of juvenile bluegill, largemouth
bass acquire parasites that use bluegill as intermediate and paratenic hosts such as
Cryptogonimus sp., P. ambloplitis and N. cylindrarus. There is a more even distribution
of parasite individuals among parasite species due to the numerically lessened role in the
parasite component community of directly penetrating larval trematodes due to the
acquisition of new parasites, leading to similar total, enteric and parenteric parasite
component community diversity in YOY largemouth bass.

Mollusk Abundances

In general, an increase in numbers of mollusks found in the sampling area in
concert with water temperature increasing above 18° (Hoffman, 1958) was parallel with
an increase in the number of trematodes found per fish (Figure 7 and 8). Because larval
trematodes, which are shed by mollusks and directly penetrate bluegill, numerically
dominated the parasite community of juvenile bluegill in GL, mollusk abundance had a
large influence on parasite community structure.

In the present study, the decrease in the mean number of larval trematodes per
fish in September cannot be directly attributed to concurrent decreases in mollusk
abundances. Since metacercarial parasites are thought to be long-lived and accumulate in
a fish over time (Spall and Summerfelt, 1970), a decrease in the mollusk abundances only
has an effect on recruitment of new parasite individuals (depending on water
temperature). Less mollusks may mean there are less larval parasites shed to penetrate

fish. Decreases in numbers of trematodes per fish may be attributed to a larger

64

proportion of younger fish examined in a month since younger fish have lower mean
abundances of larval trematodes.
Parasite Community Comparisons Between Gull Lake and Three Lakes H

There were no significant differences in Brillouin’s diversity, evenness, species
richness or adjusted species richness of parasite infracommunities of juvenile bluegill
between GL and TL or of YOY largemouth bass between GL and TL. Additionally,
there were no significant differences in total parasite component community diversity of
juvenile bluegill or vov largemouth bass between or. and TL. Esch (1971) suggested
that the trophic status of a lake plays a role in the types of parasites harbored by
centrarchids. Eutrophic lakes have better quality habitat for piscivorous birds, mammals
and reptiles that can serve as definitive hosts for larval parasites hosted by fish (Esch,
1971). Due to the diversity of vertebrates associated with eutrophic lakes, Esch and
Fernandez (1993) hypothesized that fish in these lakes should have more allogenic
parasite species (parasite species using a terrestrial organism as a definitive host) and
lakes with less available nutrients should have more autogenic parasite species (parasite
species that use an aquatic organism as a definitive host). Esch (1971) found that adult
bluegill and largemouth bass in GL contained 71% and 78% autogenic parasite species,
respectively and 29% and 22% allogenic parasite species, respectively, compared to 67%
autogenic and 33% allogenic parasite species in largemouth bass fiom eutrophic
Wintergreen Lake. The parasite communities of juvenile bluegill from eutrophic TL
contained 64% autogenic parasite species and 36% allogenic species whereas the parasite
communities of juvenile bluegill in mesotrophic GL contained 72% autogenic species

and 28% allogenic species. Young-of-theyear largemouth bass contained 60% autogenic

65

and 40% allogenic parasite species in TL and 64% autogenic and 36% allogenic parasite
species in GL. Data from the present study agree with the percentages of autogenic and
allogenic parasites in GL found by Esch (1971).

Data fiom the present study support the hypothesis proposed by Wisniewski
(1958) and furthered by Esch (1971) that trophic level of the host is an important parasite
community determinant. Juvenile bluegill in both lakes hosted similar parasite species
and had similar percentages of their community comprised of adult parasites. Since
juvenile bluegill are prey items of YOY largemouth bass, largemouth bass are on a higher
trophic level than juvenile bluegill. Iflake trophic status were more important than host
trophic level, parasites of juvenile bluegill and YOY largemouth bass within a lake would
be more similar to each other than parasites of the same host species between lakes.
Young-of-the-year largemouth bass in both lakes had similar parasite species and had
higher percentages of adult parasites in their community than juvenile bluegill fi'om either
lake. Additionally, juvenile bluegill are intermediate or paratenic hosts for
Coptogonimus sp., P. ambloplitis, and L. thecatus, all which use largemouth bass as
definitive hosts.

The coefiicient of community similarity for bluegill and largemouth bass fi'om
GL was approximately equal to the coefficient of community similarity for bluegill and
largemouth bass from TL. The coefficients of community similarity show that parasite
component communities of bluegill from TL, and GL and YOY largemouth bass fiom TL
and GL were more similar to each other than parasite component communities of GL
bluegill and largemouth bass and TL bluegill and largemouth bass. The present study

suggests that trophic status of a fish host is a more important parasite community

66

determinant than lake trophic status because the coefficients of community similarity are
more similar for the same host species in different lakes than for different host species in
the same lake. Iflake trophic status were more important than fish trophic status, the
total parasite component communities of bluegill and largemouth bass within a lake
would have higher coefficients of community similarity than parasite component
communities of bluegill between lakes or largemouth bass between lakes.
Summary

Differences in parasite community composition between juvenile and adult
bluegill and juvenile and adult largemouth bass in Michigan are a reflection of their diet
and habitat. Adult bluegill occupy open water habitats (Werner and Hall, 1988) where
they are less vulnerable to penetration by larval trematodes and, via exposure to different
intermediate hosts, are also exposed to different parasites than littoral juvenile fish. A
greater percentage of the parasites of juvenile bluegill in GL and TL are comprised of
larval parasites than in adult bluegill previously studied in Michigan. These findings
support the hypothesis that trophic level of the host is the most important determinant of
the parasite community in fishes (Wisniewski, 1958; Esch, 1971). Because of their
trophic level differences, juvenile bluegill and YOY largemouth bass occupy a different
habitat and consume a different diet than adults of these species leading to a parasite

fauna unique to their life stage.

67

CHAPTER THREE

ACQUISITION AND DYNAMICS OF THE PARASITE COMMUNITY IN
JUVENEE BLUEGHJ. LEPOMS MCROCHIRUS, AND YOUNG-OF-THE-
YEAR LARGEMOUTH BASS, MICROPTERUS SALMOIDES IN THREE LAKES

H AND GULL LAKE, MICHIGAN

68

INTRODUCTION

The parasite communities of fish are a reflection of the diet and habitat of the fish
host (Esch and Fernandez, 1993; Marcogliese, 2004). Habitat attributes such as
vegetation type and quantity, and substrate type, play a major role in the parasite
intermediate hosts found in an area. Mollusks serving as intermediate hosts for trematode
parasites, for example, shed larval parasites that may infect a fish by direct penetration.
Habitat also influences diet by determining what prey items (which may be serving as
intermediate hosts) are available to a fish. Because parasite communities of fish are
largely determined by fish diet and habitat, insights into the ecology and life history of a
fish can be gained through examining its parasite fauna (Marcogliese, 2004).

The diet and habitat of bluegill change with age. Afler hatching approximately
two weeks post-spawn (Breder, 1936), bluegill fry undergo a migration to the limnetic
zone of a lake and remain there for approximately six to eight weeks (Werner, 1967;
Werner and Hall, 1988). These fish then return to the vegetated littoral zone for the next
two to three years (W emer and Hall, 1988) until they move to the limnetic zone of the
lake for the duration of their life (Werner and Hall, 1988). The shift to the limnetic
habitat gradually takes place in bluegill between 45 and 75 mm standard length (SL)
(Osenberg et al., 1992). The switch to the limnetic zone of a lake as their primary habitat
occurs at approximately 75 mm SL and is approximately commensurate with age of
maturity (Osenberg et al., 1992). These changes in the diet and habitat may cause a

concurrent shift in the parasite fauna (Wilson et al., 1996; Zelmer and Arai, 2004).

69

Young-of-the-year (YOY) largemouth bass also undergo diet shifts that may lead
to changes in their parasite communities. Young-of-the-year largemouth bass remain in
the littoral zone for the first few weeks to months of life feeding on invertebrates
(Gilliam, 1982; Olson, 1996; Post, 2003). When they become large enough to eat fish,
largemouth bass switch to a diet of piscivory, primarily preying on juvenile bluegill
(Gilliam, 1982; Olson, 1996; Post, 2003) and continue to prey on fishes throughout their
life. Since largemouth bass eat aquatic invertebrates such as copepods, arnphipods and
mayflies for the first few weeks to months of life (Sule, 1981; Gilliam, 1982; Fischer and
Kelso, 1990; Olson, 1996; Dibble and Harrel, 1997; Post, 2003), they may acquire
parasites that use these invertebrates as intermediate hosts. As is the case with juvenile
bluegill, while living in the vegetated littoral zone, largemouth bass are vulnerable to
colonization by larval trematodes shed by mollusks. Since largemouth bass become
piscivorous early in life, primarily eating juvenile bluegill, they may also acquire
parasites that use bluegill as intermediate or paratenic hosts. Since invertebrate and
bluegill intermediate hosts may be harboring different larval parasites that can infect
largemouth bass, the switch to piscivory may cause a shift in parasite communities of
largemouth bass.

Many studies have reported on the parasite communities of bluegill (Esch, 1971;
McDaniel and Bailey, 1974; Cloutman, 1975; Esch et al., 1976; Jilek and Crites, 1980;
Fischer and Kelso, 1990; Fiorillo and Font, 1996; Wilson et al., 1996; Muzzall and
Peebles, 1998; Steinauer and Font, 2003; F ellis and Esch, 2004; Bhuthimethee et al.,
2005; Fellis and Esch, 2005), yet none of these studies have examined the chronology of

parasite infection in bluegill. Only two of these studies have reported on parasite

70

communities of juvenile bluegill (Fisher and Kelso, 1990; Steinauer and Font, 2003), but
neither of them focused on when parasite species initially colonized juvenile bluegill.

The objectives of the present study were to identify fish lengths at which parasite
species first infected juvenile bluegill and YOY largemouth bass from Three lakes H
(TL) and Gull Lake (GL), Michigan and to determine if parasite community composition
changed with length in juvenile bluegill fi'om TL and GL and YOY largemouth bass from
GL; and also to compare colonization of parasites in juvenile bluegill and YOY

largemouth bass fiom TL and GL.

71

MATERIALS AND METHODS

Description of Study Sites

Study sites from TL and GL are described in Chapters One and Two.
Fish Collection and Examination

Descriptions of fish collections in TL and GL are in Chapters One and Two. Fish
in both lakes were examined as described in Chapter One.
Parasite Preparation and Identification

Parasites from fish in both lakes were prepared and identified as described in
Chapter One.
Data Analysis

The standard length (SL) of fish at which each parasite species was first acquired
was identified for juvenile bluegill and YOY largemouth bass in TL and GL irrespective
of fish cohort. Also, percentages of adult helminth parasite species in five mm length
classes (arbitrarily determined) of juvenile bluegill and YOY largemouth bass were
calculated to determine if parasite community structure changed as fish became older and
larger. Adult parasite species in this analysis were Actinocleidus sp., Anchoradiscus sp.,
Monogene sp. A, Monogene sp., Azygia sp., Crepidostomum sp., Coptogonimus sp.
adults, Leptorhynchoides thecatus, Neoechinorhynchus cylindrarus, Pomphorhynchus
bulbocolli, Camallanus sp. and Spinirecrus sp. Because there were no YOY largemouth
bass from TL examined in several length classes, percentages of adult parasite species

were not calculated for these fish.

72

RESULTS

The standard lengths (SL) at which TL and GL juvenile bluegill first acquired
parasite species are in Figures 10 and 11. Numbers of juvenile bluegill in TL and GL
examined in each length interval are in Appendices H and III. Larval trematodes such as
Coptogonimus sp. metacercariae and Posrhodiplosromum minimum, the two most
prevalent and abundant parasite species of juvenile bluegill (Tables 1 and 14), were the
first parasites to colonize juvenile bluegill in both lakes. Coprogonimus sp. was found in
the smallest bluegill examined in each lake. Proteocephalus ambloplitis was the first
parasite acquired through ingestion to colonize bluegill in TL. Pomphorhynchus
bulbocolli was the first parasite acquired by ingestion by GL bluegill. Monogenes and
protozoans did not appear to have any colonization patterns with length of juvenile
bluegill in either lake.

The standard lengths at which TL and GL YOY largemouth bass first acquired
parasite species are in Figures 12 and 13. Numbers of YOY largemouth bass in TL and
GL examined in each length interval are in Appendix IV and V. Coplogonimus sp.
metacercariae, Monogene sp., Coptogonimus sp. adults and Proreocephalus ambloplitis
were the first species to colonize YOY largemouth bass fi'om TL and were found in the
smallest largemouth bass examined in TL. Coptogonimus sp. metacercariae, T richodina
sp. and Camallanus sp. were the first species to colonize YOY largemouth bass from GL
and were found in the smallest largemouth bass examined fi'om GL. Monogenes and
protozoans did not appear to have any colonization patterns with length of YOY

largemouth bass from either lake.

73

The percentages of adult parasite species fi'om TL and GL juvenile bluegill in five
mm length classes are in Figures 14 and 15. No adult parasite species were found in the
smallest length class (15-19 mm) of TL or GL juvenile bluegill. The percentage of adult
parasite species in the parasite community generally increased with increased length of
TL and GL juvenile bluegill.

Overall, 56% of parasite species from GL YOY largemouth bass were adults.
The percentages of adult parasite species fiom GL YOY largemouth bass in five mm
length classes are in Figure 16. The percentage of adult parasite species varied between

56-72% and did not show a general trend with increasing fish length.

74

DISCUSSION

Coptogonimus sp. metacercariae were found in the smallest juvenile bluegill and
YOY largemouth bass in TL and GL. Juvenile bluegill and YOY largemouth live in
vegetated habitats with mollusks that shed trematode cercariae that can infect fish
through penetration. Because larval trematodes, such as Coptogonimus sp.
metacercariae, are acquired passively by fish, it is not surprising that a larval trematode is
among the first parasites acquired in both species of fish in both lakes. Since bluegill and
largemouth bass in the present study had such high mean abundances of Coptogonimus
sp. metacercariae (Tables 2, 5, 14 and 15) there are likely a large number of cercariae in
the environment. This large number of cercariae would increase the likelihood that even
a very young and small fish would become infected with this parasite. Also, small fish
have limited gape size and would not be able to eat the intermediate hosts for many of the
adult parasite species found in the present study.

In general, for both fish species examined in TL and GL in the present study,
parasites acquired via ingestion using the same intermediate host group are recruited
within a narrow range of fish lengths. For example, in TL juvenile bluegill, all parasites
using copepods as intermediate hosts (Proreocephalus cmrbloplitis, Carnallanus sp.,
Spiroxys sp. and Haplobothrium globuliforme) were acquired between 17 and 23 mm.
Parasites using larger intermediate hosts, such as Spinitecrus sp. which likely uses a
mayfly (Hoffman, 1999), are not recruited by bluegill until they reach larger lengths and
have a larger gape size. In GL, the parasite species P. amblopliris and H. globuliforme,

are first acquired by juvenile bluegill between 28-30 mm SL.

75

The exception to recruitment of parasite species that use the same intermediate
host group in a narrow range of lengths was P. bulbocolli in GL juvenile bluegill.
Pomphorhynchus bulbocolli uses an amphipod intermediate host and was first acquired
by bluegill in GL at 20 mm SL, but Leptorhynchoides thecatus which also uses an
amphipod intermediate host was not first recruited until 32 mm SL. Esch et al. (1976)
suggested that midges may be serving as intermediate hosts for this parasite in GL after
examination of 6,000 arnphipods in GL, none of which were infected with P. bulbocolli.
However, there are no reports of midges hosting P. bulbocolli or other acanthocephalan
species. The amphipod intermediate host of this parasite would be a large prey item for a
20mm bluegilL so it may be that P. bulbocolli is not using arnphipods as intermediate
hosts in GL. The notion of Esch et al. (1976) that arnphipods may not serve as
intermediate hosts for P. bulbocolli in GL is also supported by the recruitment data from
TL bluegill. In TL bluegill, P. bulbocolli, the only parasite of TL bluegill using an
amphipod intermediate host, is not first recruited by these fish until 32 mm SL. With the
exception of P. bulbocolli in GL bluegill, parasites using arnphipods as intermediate hosts
are not acquired by bluegill until 32 mm SL.

In largemouth bass, the same general pattern exists that most of the parasites
sharing the same intermediate host are recruited within a narrow range of lengths. In GL
largemouth bass, both parasite species that use copepods as intermediate hosts,
CamaIlanus sp. and P. ambloplitis, were recruited at 21 and 22 mm SL, respectively. In
TL largemouth bass, two of the parasites using copepods as intermediate hosts, Spirortys
sp. and Camallanus sp were first recruited at 40 mm SL. However, P. ambloplitis, which

also uses a copepod intermediate host, is first recruited by TL largemouth bass at 19 mm

76

SL. The sample size of fish in TL examined between 23 and 37 mm was small (n=11).
Spiroxys sp. and CamaIIanus sp., which were infi'equent parasites (Table 2), could have
been recruited at smaller fish lengths, but they were not found due to small numbers of
fish examined and low prevalence.

YOY largemouth bass have a higher percentage of adult parasite species than age
0 bluegill in either lake. By the end of the 2003 sampling year the mean length of age 0
bluegill is approximately 22 mm SL in TL and 26 mm SL in GL. Bluegill of this length
have acquired eight parasite species in TL and four parasite species in GL, whereas YOY
largemouth bass have acquired 16 parasite species in TL and 14 parasite species in GL.
Since YOY largemouth bass have a larger gape size than bluegill, they are able to eat a
wider variety of prey items that may be serving as parasite intermediate hosts.

In bluegill from TL and GL, percentages of the parasite community made up of
adult parasite species generally increased with fish length. As juvenile bluegill begin to
spend more time foraging in the limnetic zone of a lake, and their diet and habitat usage
becomes more like that of adult bluegill, their parasite communities also become more
similar to parasite communities of adult bluegill. Muzzall and Peebles (1998) reported

adult parasite species comprised 69% of the adult bluegill parasite species from
Michigan. As juvenile bluegill increased in length in the present study, the percentage of
adult parasite species in the parasite community increased, but did not reach 69%.
Osenberg et al. (1992) stated that juvenile bluegill approximately 45-75 mm in SL use
both littoral and limnetic habitats. As juvenile bluegill spend an increasing amount of
time foraging in the limnetic habitat, their percentage of adult parasite species may

approach 69%, as in adult bluegill reported in Michigan (Muzzall and Peebles, 1998).

77

Gilliam (1982) reported that bluegill between 0—25 mm 8L occupy a different
position in the water column and are found different distances from shore than bluegill
between 26-50 mm. Some of this habitat difference is attributed to larval bluegill living
in the limnetic zone of the lake until they are approximately 12-14 mm SL (Werner,
1967; Werner and Hall, 1988). Data fi'om the present study suggest that there may also
be a slight habitat shift occurring in bluegill between 20 and 24 mm. In the 15-19 mm
length class, bluegill have no adult parasites and between 20 and 24 mm, bluegill begin to
acquire adult parasites. Since parasites are a reflection of the diet and habitat of a fish, it
can be inferred that bluegill undergo a habitat and/or diet shift in this length range due to
the dramatic shift in the percentage of adult parasite species in the parasite community of
juvenile bluegill in TL and GL. However, Azygia sp. and Camallanus sp. are infrequent
parasites (Tables 1 and 14). Since 11 bluegill were examined between 15-19 mm SL in
TL and only one bluegill was examined within this length range in GL, it may be that
bluegill between 15-19 mm SL had acquired these parasites, but they were not found due
to small numbers of fish examined and low prevalences of these parasites. Ifadult
parasites of these species had been acquired by juvenile bluegill between 15-19 mm SL,
then the acquisition of adult parasites may be reflective of the return to the littoral areas
of the lake from the open water (Werner, 1967; Werner and Hall, 1988).

Percentages of adult parasite species of GL YOY largemouth bass do not appear
to have any visible trends with length. Until largemouth bass begin eating fish, their diet
consists of invertebrates. Some of the invertebrates largemouth bass prey on serve as
intermediate hosts for parasites that use largemouth bass as definitive hosts. Even though

GL YOY largemouth bass are acquiring adult parasites through ingestion, they are still

78

vulnerable to penetration by trematode cercariae and their percentage of adult parasites
fluctuates as these fish become longer. The majority of the diet of YOY largemouth bass
consists of invertebrates until they are approximately 50 mm SL (Olson, 1996). Once a
majority of the diet of YOY largemouth bass consists of fish (which may be serving as
parasite intermediate hosts), there may be a shift to a larger percentage of the parasite
species in the community being comprised of adults. Esch (1971) reported 83% of the
parasite species of adult largemouth bass in GL as adults. In the present study, 10 fish
were examined with lengths greater than 50 mm with 62% of their parasite species
comprised of adults. Because YOY largemouth bass that have not switched to piscivory
do not have the same diet and habitat as adults, the parasite communities of YOY
largemouth bass may have less adult parasite species than adult largemouth bass.
Summary

The parasites hosted by a fish are a reflection of the diet and habitat of the fish
host. Larval trematodes, particularly Coprogonimus sp., are among the first parasites to
colonize juvenile bluegill and YOY largemouth bass in TL and GL. The vegetated
littoral habitat of these fish is home to many species of mollusks shedding cercariae that
are passively acquired by fish. Because the diets and habitats of juvenile bluegill and
YOY largemouth bass change over time, new parasites are acquired by these fish. In
bluegill in TL and GL, the percentage of adult parasite species generally increases with
increasing length. In YOY largemouth bass from GL, the percentage of the parasite
community consisting of adult parasites generally does not increase with length and was

lower than the percentage of adult parasites in piscivorous adult largemouth bass, which

79

may suggest that all YOY largemouth bass examined from GL had not switched to

piscivory.

80

CONCLUSION

There are several similarities between parasite communities of TL and GL
bluegill and between TL and GL bass that help to extend our general knowledge of
parasite communities of juvenile centrarchid fishes. Fish species generally hosted the
same parasite species between lakes and the most abundant parasites in each fish species
in both lakes were larval trematodes. Prior studies in other areas of the United States
have also shown larval trematodes to dominate the parasite fauna of juvenile centrarchid
fishes (Fischer and Kelso, 1987, 1988, 1990; Iandry and Kelso 1999; Steinauer and Font,
2003). In some of these studies, including the present study, larval parasites, particularly
larval trematodes, have been implicated as potential causes of parasite-induced host
mortality. This suggests that larval trematodes can be a major selective pressure
influencing the survival of juvenile bluegill.

The trophic status of the lake in which a fish resides and the trophic status of the
host are important determining factors of the parasite communities of juvenile bluegill
and YOY largemouth bass. Data from the present study were in agreement with the
percentage of autogenic and allogenic parasite species found in adult bluegill and
largemouth bass in GL reported by Esch (1971). However, in the present study, juvenile
bluegill parasite communities were more similar between lakes than juvenile bluegill and
YOY largemouth bass within a lake. This suggests that trophic status of the host is a
more important determining factor of the parasite community than the lake trophic status.

Fish habitat and diet are the major determinants of parasite communities.

Because parasite communities are structured as functions of fish diet and habitat, our

81

knowledge of the diet and habitat of these fishes can be reinforced through surveying
their parasite fauna. As juvenile bluegill in both lakes became longer and older, adult
parasite species made up a greater percentage of the parasite community. Furthermore,
juvenile bluegill and YOY largemouth bass acquired new penetrating larval trematode
species and new parasite species with direct life cycles. This suggests that as juvenile
bluegill and YOY largemouth bass age, their diet and/ or habitat change. This knowledge
inferred from the parasite data in the present study corroborates with diet and habitat
changes in juvenile bluegill and YOY largemouth bass documented by Gilliam (1982);

Werner and Hall (1988); Osenberg et al. (1992), Olson (1993) and Post (2003).

82

Table 1. Prevalence, mean abundance : SD (maximum) and site of infection of parasites

of 393 juvenile Lepomis macrochirus in 2003 and 2004 fi'om Three Lakes H, Michigan.

83

 

 

2003 2004 Site of Infection
n=209 n=l84
Monogenea
Actinocleidus sp. 1%1' 5% Gills
Anchoradiscus sp. 2% 5% Gills
Monogene sp. 9% 1% Gills
Trematoda
Azygia sp. 11% 4% Stomach, Pyloric
0.2 1 WI 41110.2 Ceca, Intestine
(7) (1)
Clinostomum sp.* <1% 0% Muscle
<0.l : 0.1 -
(1) '-
Crepidostomum sp. 0% 1% Ceca
— 0.1 i 0.9
- (12)
Cryptogonimus sp. * >99% >99% Muscle,
244.2 : 354.2 84.4 1 150.3 Brain, Gills,
(2387) (1563) Mesenteries
Diplostomum sp.‘ 12% 11% Vitreous Humor
0.3 i 1.2 0.2 :1; 0.8
(9) (6)
Neascus sp. * 50% 29% Muscle, Mesenteries,
3.3 i 9.3 1.3 1 3.3 Kidney
(l 14) (28)
Posthodiplostomum 62% 73% Liver, Kidney
minimum“ 1 1.8 3; 15.8 3.8 i 7.0 Mesenteries,
(93) (57) Gonad
Cestoda
Haplobothrium 7% 7% Liver, Mesenteries,
globulifbrme“ 0.1 1 0.5 0.1 :1; 0.3 Gills
(6) (2)
Table 1.

84

 

 

 

Pmteocephalus 52% 32% Liver, Mesenteries
ambloplitis" 0.9 i 1.7 0.6 i 1.2
(13) (9)
Nematoda
Coma/[anus sp. <1% 2% Intestine
<0.]:0.2 <0.li0.1
(1) (l)
Spinitectus sp. 17% l 1% Intestine
0.6 i 1.8 0.4 i 1.3
(14) (3)
Spiroxys sp.* 4% 1% Muscle
<0.1:0.3 <0.]:0.1
(2) (l)
Acanthocephala
Pomphorhjmchus <1% 2% Liver
bulbocolli <0.l : 0.2 <0. I: 0.2
(2) (2)
Neoechinorhynchus 1% 2% Intestine
cylindratus" <0.1 i 0.3 <0. I: 0.1
(5) (1)
Protozoa
Myxobolus sp. 8% 4% Gills
Trichodina sp. 6% 10°/o Gills
= = =

 

Table l (con’t).
* Indicates larval parasite.
T Parasite prevalence.

I Parasite mean abundance :1; SD (maximum).

85

Proteocephalus 52%
ambloplitis" 0.9 : 1.7
(13)
Nematoda
Camallanus sp. <1%
<0.] : 0.2
(1)
Spinitecrus sp. 17%
0.6 : 1.8
(14)
Spirouys sp.‘ 4%
<0.1 : 0.3
(2)
Acanthocephala
Pomphorhynchus <1%
bulbocolli <0.] : 0.2
(2)
Neoechinorhynchus 1%
cylindratus" <0.l : 0.3
(5)
Protozoa
Myxobolus sp. 8%
Trichodina sp. 6%
—

 

__

 

Table 1 (con’t).

* Indicates larval parasite.

T Parasite prevalence.

I Parasite mean abundance : SD (maximum).

32%
0.6 : 1.2
(9)

2%
<0.1:0.l
(1)

11%
0.4 : 1.3
(8)

1%
<0.1: 0.1
(1)

2%
<0. 1: 0.2

(2)

2%
<0.1: 0.1
(l)

4%

10%

Liver, Mesenteries

Intestine

Intestine

Muscle

Liver

Intestine

Gills

Gills

 

Table 2. Prevalence (%), mean abundance : SD (maximum) and site of infection of

parasites of 26 young-of-the-year Micropterus salmoides fiom Three Lakes 11, Michigan.

86

 

Parasite

Monogenea
Monogene sp. A

Monogenea sp.

Trematoda
Azygia sp.

C ryptogonimus sp.

Cryptogonimus sp. *

Diplostomum sp. *

Neascus sp.*

Posthodiplostomum
minim um *

Cestoda
Proteocephalus
ambloplitis“

Nematoda
Carnallanus sp.

Table 2.

15%
0.2 i 0.51
(2)
4%
0.2 i 0.6
(3)

85%

34.2 : 55.1

(249)

35%
0.6 i 1.0
(4)

50%
2.4 i 5.3
(26)

38%
1.0 i 1.6
(6)

88%
4.3 i 2.9
(11)

4%
0.13502
(1)

87

Site of Infection

Gills

Gills

Stomach, Pyloric
Ceca, Intestine

Stomach, Pyloric
Ceca, Intestine

Muscle, Cartilage,
Brain, Gills,
Mesenteries

Vitreous Humor

Muscle,
Mesenteries,
Kidney

Liver, Kidney,
Cartilage, Gills,
Mesenteries

Liver, Mesenteries,

Gonad

Intestine, Pyloric
Ceca, Stomach

 

Spiroxys sp. * 4% Muscle
0.1 : 0.3
(1)
Acanthocephala
Neoechinorhynchus 3 5% Intestine
cylindratus 1.4 : 4.1
(20)
Pomphorhynchus 8% Intestine,
bulbocolli 0.1 : 0.3 Mesenteries,
(1) Muscle
Protozoa
T richodina sp. 8% Gills
Table 2 (con’t).
* Indicates larval stage.

T Parasite prevalence.

I Parasite mean abundance : SD (maximum).

88

 

Cohort N Cryptogoninrus

Neascus Posrhodiplostomum Proteocephalus

 

sp. sp. minimum ambloplitis
2001 98%* 73°/ 95% 68%
66 470.7 : 489.91 4.8 : 6.9 18.2 : 22.2 1.4 : 1.9
(2387) (29) (93) (12)
2002 100% 62% ‘ 98% 55%
91 265.5 : 249.8 4.6 : 12.6 14.6 : 13.2 1.4 : 2.1
(1563) (114) (57) (13)
2003 >99% 24% 72% 26%
235 48.0 : 71.3 0.8 : 2.6 2.7 : 3.0 0.3 : 0.8
(474) (28) (19) (4)

* Parasite prevalence.

1‘ Mean : SD (maximum).

Table 3. Prevalence and mean abundance : SD (maximum) of parasites of juvenile

Lepomis macrochirus with greater than 30% overall prevalence by cohort from Three

Lakes 11, Michigan.

89

 

 

 

 

Month N ervptogonimus Neascus Posrhodiplostomum Proteocephalus
sp. 3). minimum ambloplitis
June, 2003 19 94%* 22°/ 89% 72%
106.9 :116.71‘ 0.7 :1.8 8.1 : 13.2 1.5 :1.4
at a a a
July 12 100% 70% 90% 60%
602.8: 525.0 2.5 : 2.9 7.0 : 5.4 1.3 : 1.6
b ab a a
August 20 100% 83% 100% 67%
742.7: 597.2 4.4 : 5.1 12.2 : 14.8 1.7 : 2.7
b b a a
September 9 100% 100% 100% 80%
381.2: 182.7 9.1 : 8.9 44.6 : 23.6 1.0 : 1.0
b b b a
October 6 100% 100% 100% 33%
586.3: 430.5 17.8 : 7.4 53.0 : 21.8 0.7 : 1.2
b c b a

 

 

* Parasite prevalence.
T Parasite mean abundance : SD (maximum).
I Mean abundances followed by the same letter within the same column are not

significantly different from each other.

Table 4. Monthly prevalence, mean abundance : SD of parasites with greater than 30%

overall prevalence from the 2001 cohort ofLepomis macrochirus from Three Lakes 11,

Michigan.

90

Table 5. Monthly prevalence, mean abundance: SD of parasites with greater than 30%
overall prevalence from the 2002 cohort of Lepomis macrochirus from Three Lakes H,

Michigan.

91

 

 

 

 

Month N ervprogonimus Neascus Posthodiplostomum Proteocephalus
sp. sp. minimum ambloplitis
June, 2003 11 100%“ l7°/ 100% 67%
31.45 i 6461 0.7: 1.8 4.8 : 4.6 0.8 : 0.9
331: a a a
July 3 100% 40% 100% 80%
441.0 : 48.8 13:12 6.3 :1.5 1.0 :1.0
b ab abc a
August 12 100% 58% 100% 67%
257.2 : 118.9 1.6: 1.7 6.8 : 6.6 1.9 : 1.4
b ab 3 a
September 21 100% 76% 100% 80%
312.0 : 206.0 8.5: 24.4 18.1 : 11.7 1.3 : 3.1
b ab be a
October 16 100% 81% 100% 33%
336.9 : 345.6 7.4 : 7.4 27.9 : 10.4 1.3 : 1.6
b b c a
April, 2004 3 100% 100% 100% 100%
216.0 : 165.0 8.7 : 9.3 21.7 : 9.1 2.0 : 1.0
ab ab abc a
May 4 100% 100% 100% 25%
452.8 : 741.7 3.5 : 2.4 31.0 : 25.5 0.5 : 1.0
ab ‘ ab abc a
June 4 100% 25% 75% 50%
58.0 : 119.0 0.3 : 0.5 10.5 : 10.7 3.5 : 4.4
ab ab ab a
July 17 100% 65% 94% 47%
224.6 : 115.3 2.8 : 3.4 6.7 : 6.2 1.2 : 1.6
b ab a a
_
Table 5.

* Parasite prevalence.

 

I Parasite mean abundance : SD (maximum).

1 Mean abundances followed by the same letter within the same column are not

significantly different from each other.

Table 6. Monthly prevalence, mean abundance: SD of parasites with greater than 30%
overall prevalence from the 2003 cohort of Lepomis macrochirus from Three Lakes H,

Michigan.

93

 

 

 

 

Month N Cryptogonimus Neascus Posthodiplostomum Proteocephalus
jg. sp. minimum ambloplitis
June, 2003 2 100%“ 50% 100% 50%
26.0 :1: 14.11- 0.5 : 0.7 5.5 : 3.5 0.5 : 0.7
abch 3 b a
July 0 —‘I -— - -
August 5 100% 29% 0% 20%
4.8 : 3.4 0 0 0.2 : 0.4
a a a a
September 35 100% 26% 89% 23%
28.8 : 15.0 0.4 : 0.8 2.7 : 2.1 0.3 : 0.5
ed a be 3
October 38 100% 67% 100% 11%
42.9 : 41.7 0.8 : 2.2 4.6 : 3.2 0.1 : 0.4
cd 3 c a
April, 2004 13 100% 38% 85% 31%
20.8 : 13.7 0.5 : 0.8 4.9 : 5.4 0.8 : 1.5
bc a be a
May 55 98% 13% 62% 31%
“9:86 04:13 16:21 04:07
ab a ab 3
June 65 100% 8% 62% 31%
44.18 : 27.6 0.2 : 0.6 1.7 : 2.3 0.4 : 0.6
d a ab a
July 23 100% 78% 78% 47%
209.47 : 129.5 5.1 : 6.1 3.9 : 3.2 0.3 : 0.9
e b c a
—
Table 6.

* Parasite prevalence.

T Parasite mean abundance : SD.

 

I Means followed by the same letter within the same column are not significantly

different from each other.

\1 Indicates no fish were examined.

 

Month

Cryptogonimus Neascus Posthodiplostomum ProteocephaluT

 

sp. sp. minimum ambloplitis
June, 2003 51.26 22.8 12.53 2.05
July 5.39 0.25 0.59 3.33
August 164.98 1.90 6.37 1.09
September 382.74 69.95 7.55 7.29
October 354.41 7.99 3.89 2.01
April, 2004 126.10 9.96 3.80 0.50
May 1215.17 1.62 26.53 2.00
June 89.65 0.34 13.93 12.93
July 59.21 4.04 5.67 2.03

 

Table 7. Variance to mean abundance ratio for the most common parasites (parasites with

>3 0% prevalence overall) for the 2002 cohort ofLepomis macrochirus from Three Lakes

 

 

11, Michigan by month.

95

 

 

Month C Iyptogonimus Neascus Posthodiplostomum Proteocephalus

 

sp. sp. minimum ambIopliris

June, 2003 7.6 1.0 2.27 1.00
July at: a: a at:

August 2.44 T T 1.00

September 7.81 1.59 1.66 1.00

October 38.00 5.95 2.20 1.31

April, 2004 8.99 1.11 5.89 2.60

May 6.22 4.56 2.72 1.08

June 14.80 2.13 3.14 0.97

July 80.00 0.25 0.17 0.60

 

 

 

* Indicates no fish examined.

T Indicates no fish infected.

Table 8. Variance to mean abundance ratio for the most common parasites (parasites

with >30% prevalence overall) for the 2003 cohort ofLepomis macrochirus from Three

Lakes H, Michigan by month.

96

 

2003 2004

Brillouin’s diversity 0.16 : 0.13 0.12 : 0.10
(0-0.97) (0-0.44)

Brillouin’s evenness 0.30 : 0.20 0.28 : 0.24
(0-1.00) (0-1.00)

Species Richness 3.7 : 1.5 2.9 : 1.5

(1-9) (1-8)
Adjusted Species 3.4 : 1.3 2.7 : 1.3
Richness (1-7) (1-6)

 

Table 9. Mean : SD (range) of Brillouin’s diversity and evenness and species richness
and adjusted species richness for parasite infiacommunities of Lepomis macrochirus from

Three Lakes H, Michigan.

97

 

Cohort Brillouin’s Brillouin’s Species Adjusted Species

 

Diversity Evenness Richness Richness
2001 0.15 : 0.14 0.25 : 0.19 4.5 : 1.6 4.0 :1.3
(0-0.97) (0070) (1—9) (1-7)

2002 0.17 i 0.14 0.28 i 0.19 4.4 11.3 4.0 11.2
(0.090) (0-1) (1-7) (1-7)

2003 0.13 i 0.10 0.31 i 0.23 2.6 :12 2.5 i 1.1
(0044) (0-1) (1-8) (1-5)

 

Table 10. Mean : SD (range) of Brillouin’s diversity and evenness and species richness

and adjusted species richness for parasite infracommunities of juvenile Lepomis

macrochirus from Three Lakes H, Michigan by cohort.

98

 

 

 

 

 

Brillouin’s Brillouin’s Species Adjusted
Diversity Evennees Richness Species

Richness

June, 2003 0.21 : 0.20" 0.34 : 0.21 3.6 : 1.2 3.0 : 0.8
bT b a a

July 0.07 : 0.07 0.08 : 0.01 4.3 : 1.6 3.8 : 1.3
a a a ab

August 0.11:0.10 0.16:0.16 5.9:1.3 5.1:1.1
ab a b b

September 0.19 : 0.06 0.35 : 0.13 3.8 : 0.7 3.8 : 0.7
b b a ab

October 0.22 : 0.12 0.38 : 0.20 4.2 : 1.5 4.0 : 1.1
b b ab ab

* Mean : SD.

T Means followed by the same letter within the same column are not significantly

different from each other.

Table 11. Mean : SD of Brillouin’s diversity and evenness and species richness and
adjusted species richness for parasite infracommunities of for the 2001 cohort of juvenile

Lepomis macrochirus from Three Lakes 11, Michigan by month.

99

 

 

 

 

 

 

Brillouin’s Brillouin’s Species Adjusted

Diversity Evermeas Richness Species

Richness

June, 2003 0.21 : 019* 0.38 : 0.27 3.3 : 1.2 3.0 : 0.8
81' a ab a

July 0.04 : 0.01 0.08 _+_ 0.01 3.7 : 0.6 3.3 : 0.6
a a abc ab

August 0.11 :0.06 0.18:0.10 4.8: 1.1 4.3 :09
a 8 abc ab

September 0.20 : 0.19 0.29 : 0.18 4.4 : 1.4 4.1 : 1.4
a a abc ab

October 0.21:0.09 0.25:0.14 4.4:1.1 41:10
a a abc ab

April, 2004 0.27 : 0.01 0.36 _+_ 0.13 5.6 : 0.6 5.6 : 0.6
a a be b

May 0.22 : 0.14 0.39 : 0.28 4.3 : 1.9 4.0 : 1.4
a a abc ab

June 0.12 : 0.08 0.27 : 0.22 3.0 : 1.4 3.0 : 1.4
a a a a

July 0.12:0.07 0.21:0.15 51:10 42:08
a a c ab

* Mean : SD.

T Means followed by the same letter within the same column are not significantly

different from each other.

Table 12. Mean : SD of Brillouin’s diversity and evenness and species richness and

adjusted species richness for parasite infracommunities of for the 2002 cohort of juvenile

Lepomis macrochirus from Three Lakes 11, Michigan by month.

100

 

 

 

 

 

 

Brillouin’s Brillouin’s Species Adjusted
Diversity Evenness Richness Species
Richness
June, 2003 0.22 : 0.16“ 0.45 : 0.17 3.0 : 1.4 3.0 : 1.4
313‘" ab ab abc
July --I - - -
August 0.03 : 0.07 0.04 : 0.09 1.8 : 0.4 1.2 : 0.4
a a a a
September 0.14 : 0.06 0.37 : 0.18 2.7 : 0.8 2.5 : 0.7
b b a b
October 0.16 : 0.09 0.39 : 0.21 2.7 : 1.1 2.7 : 1.1
b b a be
April, 2004 0.20 : 0.11 0.46 : 0.24 2.8 : 1.2 2.8 : 1.2
b b a be
May 0.14 : 0.11 0.40 : 0.30 2.3 : 1.0 2.2 : 1.0
b b a ab
June 0.08 : 0.08 0.19 : 0.15 2.3 : 1.0 2.2 : 0.9
a a ab b
July 0.11: 0.07 0.20 : 0.12 4.3 : 1.4 3.6 : 1.0
ab ab b c
* Mean : SD.

T Means followed by the same letter within the same column are not significantly
different fiom each other.

1 Indicates no fish were examined

Table 13. Mean : SD of Brillouin’s diversity and evenness and species richness and

adjusted species richness for parasite infracommunities of for the 2003 cohort of juvenile

Lepomis macrochirus from Three Lakes 11, Michigan by month.

101

Table 14. Prevalence, mean abundance : SD (maximum) and site of infection of

parasites of 117 juvenile Lepomis macrochirus from Gull Lake, Michigan by year.

102

Sampling Year

 

 

Parasite 2003 2004 Site of Infection a
n=54 n=65
Actinocleidus sp. 4% T 3% Gills
Anchoradiscus sp. 2% 6% Gills
Monogenea sp. 0% 2% Gills
Trematoda
Azygia sp. 0% 6% Stomach, Ceca,
- 0.1 : 0.2 Intestine
- (1)
Captogonimus sp. * 93% 100% Muscle, Cartilage,
50.2 : 50.31 45.0 : 42.2 Brain, Gills,
(216) (214) Mesenteries
Diplostomum sp. * 4% 74% Vitreous Humor
<0.1:0.1 37:52
(1) (29)
Neascus sp. * 13% 22% Muscle,
0.3 : 1.3 0.8 : 2.1 Mesenteries, Kidney
(9) (12)
Posthodr'plostomum 33% 80% Liver, Kidney,
minimum" 0.8 : 2.6 2.6 : 2.5 Cartilage, Gills,
(19) (11) Mesenteries, Gonad
Cestoda
Proteocephalus 2% 6% Liver, Mesenteries,
ambloplitis“ <0.l : 0.1 0.1 : 0.2 Gills
(1) (1)
Table 14.

103

qulobothrium 0% 2% Liver, Mesenteries
globuliforme * -- <0.l : 0.1
-- (1)
Nematoda
Spinitectus sp. 22% 20% Intestine
0.5 :13 0.2 i 0.5
(7) (2)
Acanthocephala
Leptorhynchoides 4% 14% Intestine
thecatus <01 3: 0.2 <0.1 j; 0.2
(1) (1)
Leptorlo’nchoides 6% 28% Liver, Mesenteries
thecatus“ 0.1 i 0.4 0.1 i 0.3
(2) (1)
Neoechinorlynchus 2% 1% Liver
cylimb'atus" <0.l : 0.1 <0.] i 0.1
(1) (1)
Pomphorhynchus 67% 20% Intestine
bulbocolli 1.6 i 1.6 0.2 10.6
(5) (3)
Protozoa
Myxobolus sp. 4% 2% Gills
T richodina sp. 2% 2% Gills

 

 

 

_Table 14 (con’t).
* Larval or immature stage
T Prevalence

1 Mean abundance : SD (maximum)

104

Table 15. Prevalence, mean abundance : SD (maximum) and site of infection of

parasites of 86 juvenile Micropterus salmoides from Gull Lake, Michigan.

lOS

 

 

Parasite Site of Infection
Monogenea
Monogene sp. A 1%1' Gills
Monogenea sp. 9% Gills
Trematoda
Azygr'a sp. 17% Stomach, Ceca,
0.4:].41: Intestine
(10)
C linostomum sp. * 1%
>01: 0.1
(1)
Coptogonimus' sp. 33% Stomach, Ceca,
11.4: 39.1 Intestine
(281)
Coptogonimus sp.* 83% Muscle, Cartilage,
16.0: 28.0 Brain, Gills,
(136) Mesenteries
Diplostomum sp. * 3% Vitreous Humor
>0. 1: 0.2
(1)
Neascus sp.* 7% Muscle,
0.3: 1.8 Mesenteries,
(16) Kidney
Posthodiplostomum 7% Liver, Kidney,
minimum“ 0.1: 0.3 Cartilage, Gills,
(1) . Mesenteries
Cestoda
Proteocephalus 6% Liver, Mesenteries,
ambloplitis“ 0.1_+_ 0.4 Gonad
(2)

Table 15.

Nematoda
Carnallanus sp.*

Spinitectus sp.

Acanthocephala
Leptorhynchoides
thecatus

Leptorhynchoides
thecatus“

Neoechinorhynchus
cylincb’atus

Pomphorhynchus
bulbocolli

Protozoa
Myxobolus sp.

Trichodina sp.

47%
2.7: 5.1
(26)

10%
0.4: 2.1

(13)

19%
0.4: 1.3

(10)

27%
0.5: 1.3

(10)

13%
0.2: 0.6
(3)

72%

5.8: 6.9
(28)

6.9%

17.4%

Intestine, Ceca,
Stomach

Intestine, Ceca,

Stomach

Intestine

Mesenteries, Liver

Intestine

Intestine,
Mesenteries,
Muscle

Gills

Gills

 

Table 15 (con’t).

* Indicates larval stage

T Prevalence

I Mean abundance : SD (maximum)

 

Sampling Year
2003 2004

Brillouin’s diversity 0.10 i 0.09 0.20 i 0.12
(0-0.296) (0-0.46)

Brillouin’s evenness 0.25 i 0.23 0.39 i 0.21
(0-0.90) (0-0.84)

Species Richness 2.5 3; 1.1 3.6 i 1.2

(0-5) (1-7)
Adjusted Species 2.4 i 1.0 3.5 :I_- 1.2
Richness (0-5) (1-7)

 

 

Table 16. Mean : SD (range) of Brillouin’s diversity and evenness and species richness
and adjusted species richness for parasite infracommunities of juvenile Lepomis

macrochirus from Gull Lake, Michigan from the 2003 and 2004 sampling years.

108

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APPENDIX I

Protozoa

Life cycles of parasites in this group are highly variable. Some parasites in this
group have a direct life cycle, while others require an intermediate host. The parasite
Trichodina sp., which was encountered in the present study, has a direct life cycle
(Hoffman, 1999). The parasite Myxobolus sp., which was also found in the present study,
requires a tubificid worm intermediate host (Markiw and Wolf; 1983). Fish become
infected with this parasite when triactinomyxon spores are released fi'om the tubificid
worm and attach to the fish (El-Matbouli and Hoffman, 1989) or penetrate the fish and
travel throughout the body of the fish via the circulatory system (Gilbert and Granath,
2003)
Trematoda

Life cycles of parasites in this group are also variable, but most species require
use of a mollusk intermediate host. In aquatic systems, eggs, which contain a developing
embryo, are shed by adults in the feces of the definitive host and hatch into miricidia
when contacting water (Roberts and Janovy, 2004). These miricidia then penetrate the
soil tissue of a mollusk or the trematode eggs are eaten by a mollusk intermediate host
where they develop into either a sporocyst or redia (depending on the parasite species)
(Roberts and Janovy, 2004). Sporocysts may go through several generations of
producing daughter sporocysts before producing either cercariae, which is the infective
stage to the fish, or redia which produce cercariae that are shed by the mollusk and

directly penetrate or are ingested by the fish host (Roberts and Janovy, 2004).

130

Cercariae in many of the trematode species in the present study encyst in soft
tissue after penetrating the fish. Once encysted, these larval parasites are called
metacercariae. Two exceptions found in the present study are the trematode Azygia sp.
that has cercaria that are eaten by the fish definitive host (Sillman, 1962) and the
trematode szlostomum sp., has cercaria that will not encyst, but will instead localize
unencysted in the vitreous humor of the eye of the fish intermediate host (Hoffman,
1999)

Monogenea

Monogenea do not use an intermediate host for development; typically afier
copulation (with the exception of one family), eggs are formed and released (Roberts and
J anovy, 2004). Once in the water, the egg releases into an oncomiracidium, a larval
stage, that swims to find a suitable host (Roberts and Janovy, 2004). All monogene
species encountered in the present study produce eggs that hatch in the water into an
oncomiracidium.

Eucestoda

Two variations of cestode lifecycles are used by parasite species found in the
present study. Adult worms of Proteocephalus ambloplitis live in the pyloric ceca and
small intestines of largemouth bass. Fertilized eggs are produced afier copulation and are
passed out in the feces of the fish which are ingested by the appropriate copepod or
amphipod intermediate host and eventually develop into the plerocercoid I (Hunter, 1928;
Fisher and Freeman, 1969, 1973). If an appropriate definitive or paratenic host eats a
crustacean intermediate host containing a mature pleroceroid I, the plerocercoid I

burrows through the fish gut into the body cavity where it develops into the plerocercoid

131

11 stage (Fisher and Freeman, 1969, 1973; Freeman, 1973). Ifa paratenic host harboring
the initial plerocercoid H stage is eaten by the proper definitive host, the worm again
burrows through the gut wall into the body cavity in order to undergo further grth and
development (Fischer and Freeman, 1973). In the definitive host, the initial plerocercoid
II will develop parenterically into the middle plerocercoid H. Upon receiving the right
stimulus, which may be a rise in temperature, an increase in fish gonadotropic and
gonadal hormones, an increase in photoperiod or a combination of these factors, the
middle plerocercoid II moves back into the lumen of the intestine where it will develop
into an adult worm capable of sexual reproduction (Fischer and Freeman, 1969, 1973;
Freeman, 1973; Esch et al., 1975).

Haplobothrium globuliforme uses a bowfin, Amid calm, definitive host
(Hoffman, 1999). The worm will pass eggs in the feces of the fish which are ingested by
the copepod intermediate host (Hoffman, 1999). Within the copepod, the egg develops
into a procercoid (Hoffman, 1999). When a copepod infected with a mature procercoid is
eaten by a fish second intermediate host, the procercoid burrows through the gut wall and
encysts in the liver developing into a plerocercoid (Hoffman, 1999). The worm
completes its life cycle when a fish intermediate host with a mature plerocercoid is eaten
by the bowfin definitive host (Hoffman, 1999).

Nematoda

Nematodes have highly variable life cycles. The species of nematodes involved
in the present study are Spinitectus sp., CamaIIanus sp., and Spiroxys sp. Adults of
CamaIIanus sp. live in the intestine of fish where eggs are fertilized and larvae are

produced within the female (Stromberg and Crites, 1974). Female worms hang out the

132

vent of fish and the female worm bursts when coming into contact with water, thus
releasing larvae (Stromberg and Crites, 1974). Larvae are eaten by copepods and molt
twice before they are infective to the fish definitive host (Stromberg and Crites, 1974).
Adults of Spinitectus sp. live in the intestine of fish, where they mate and produce eggs
(Jilek and Crites, 1982). Eggs are passed from the female worm into the intestinal lumen
of the fish and into the environment via the feces of the definitive host. The eggs are
ingested by an arthropod intermediate host which may be a mayfly nymph, dragonfly
nymph, stonefly larvae or collembolan larvae, where the eggs hatch and larval worms
develop (J ilek and Crites, 1982). When an arthrOpod with mature larvae is ingested by a
bluegill or other definitive host, the larval worms establish in the intestine of the fish
(J ilek and Crites, 1982). Adults of Spiroxys sp. live in the gastrointestinal tract of turtles
(Hedrick, 1935). Eggs of Spiroxys sp. are passed from the female worm and shed in the
feces of the definitive host (Hedrick, 193 S). Larvae hatch from eggs upon coming into
contact with water and are eaten by a copepod first intermediate host (Hedrick, 193 5).
The copepod with mature larvae is then eaten by a second intermediate host, which may
be either a dragonfly nymph or a fish, such as a bluegill and largemouth bass, where the
larvae will undergo development necessary to infect the definitive host (Hedrick, 193 5).
Acanthocephala

For acanthocephalans using fish as definitive hosts, eggs are passed fi'om female
worms into the lumen of the intestine and passed into the aquatic environment via feces
(Schmidt, 1985). The egg is then ingested by an aquatic crustacean and hatches into an
acanthella which develops into a cystacanth, the infective stage to the definitive host

(Schmidt, 1985).

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