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This is to certify that the

thesis entitled

Microhabitat analysis of bass tapeworm:

Proteooephalus ambloplitisa infrapopulations

in four species of centrarchids from Gull
Lake., Michigan.

presented by

 

Merritt Gale GiJJjJJand III

has been accepted towards fulfillment
of the requirements for

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6/01 c‘JClFIC/DateDuopes-pJS

MICROHABITAT ANALYSIS OF BASS TAPEWORM, PROTEOCEPHALUS
AMBLOPLITIS, INFRAPOPULATIONS IN FOUR SPECIES or CENTRARCHIDS
FROM GULL LAKE, MICHIGAN
By

Merritt Gale Gillilland III

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

2002

ABSTRACT
MICROHABITAT ANALYSIS OF BASS TAPEWORM, PROTEOCEPHALUS
AMBLOPLITIS, INFRAPOPUALTIONS IN FOUR SPECIES OF CENTRARCHIDS
FROM GULL LAKE, MICHIGAN
By

Merritt Gale Gillilland III

A total of 242 centrarchids (54 Micropterus dolomieu, 88 M. salmoides, 50
Ambloplites rupestris and 50 Lepomis macrochirus) were collected from April —
September 2000 and April — July 2001 from five locations in Gull Lake, Michigan and
examined for Proteocephalus ambloplitis. The overall prevalence of P. ambloplitis in
smallrnouth and largemouth bass was 100%. The number of P. ambloplitis, from each
microhabitat in the fish host, was compared between females and males of the same
species and females and males of different species. Proteocephalus ambloplitis had a
significantly higher overall mean intensity i SD (72.5 :I: 44.8) and a higher mean
intensity in the ovaries (34 :I: 18.9) of smallmouth bass when compared to largemouth
bass. In smallrnouth bass the gonads were most heavily infected and in largemouth bass
the liver and mesentery were the most infected organs. Rock bass and bluegill were
examined to investigate their role in the transmission of P. ambloplitis to the definitive
host. Based upon the dietary composition of the smallrnouth and largemouth bass, other
second intermediate hosts may also be involved in the transmission of P. amblopliris.
Proteocephalus ambloplitis may be contributing to a reduction in the reproductive

potential of smallrnouth bass from Gull Lake, Michigan.

DEDICATION

I would like to dedicate this thesis to my parents, Gale and Mary Gillilland, for a lifetime
of encouragement and for helping me through all the rough spots.

iii

ACKNOWLEDGMENTS

To begin with, I would like to thank my advisor, Dr. Patrick M. Muzzall, for his help and
guidance over the years. Thank you also to my guidance committee, Dr. Donald Hall and
Dr. Thomas Coon, for their constructive criticism throughout this project.
Acknowledgments are due to Mr. Jim Dexter, Michigan Department of Natural
Resources (MDNR), for helping to get this project started and for giving me many
helpful tips along the way; Mr. Bob Day and Mr. Jim Grant, Michigan Department of
Environmental Quality (MDEQ), for allowing me use of an MDEQ fyke net; and to Dr.
Michael Klug and Dr. Steve Hamilton, Kellogg Biological Station (KBS), for allowing
me use of the boathouse, boats, and many other facilities at KBS. Much thanks to the
residents of Gull Lake who readily caught fish for me throughout the summers of 2000
and 2001: Mr. Doyle Boss, Mr. Dennis McGraill, Mr. Bob Smith, Mr. Dale Boersma, and
Mr. Lloyd Anspaugh. I would especially like to give thanks to Mr. Doyle Boss “Master
Fisherman” for his enormous help in the field and for sharing his vast knowledge on the
art of bass fishing. Thank you to Mr. Karl Strauss, Dr. Matt Zwiernik and Dr. Denise
Kay, Aquatic Toxicology Laboratory (ATL), for granting me access to an electrofishing
boat and for helping to catch fish; Mr. Dan Anson, MDNR, for catching largemouth bass
in April 2001; and Dr. John Giesy (ATL), for helping with the 3-Way and 2-Way
ANOVA. I am especially grateful to my father, Mr. M. Gale Gillilland Jr., and my
nephew, Mr. Ryan Gillilland, for helping me fish, even though we did not catch much.
Lastly, thanks to my wife, Carolyn, for all of her support, encouragement, and assistance

in the field on several occasions.

iv

TABLE OF CONTENTS

LIST OF TABLES .................................................................................. vii
LIST OF FIGURES .................................................................................. ix
INTRODUCTION .................................................................................... 1
REVIEW OF THE LITERATURE ........................................................ 3
Life Cycle ........................................................................... 3
Host Terminology for Proteocephalus ambloplitis ............................ 5
Life Stage Terminology for Proteocephalus ambloplitis ..................... 6
Pathology Associated with Proteocephalus ambloplitis ....................... 7
Seasonal patterns of Proteocephalus ambloplitis ............................... 9
MATERIALS AND METHODS .................................................................. 12
Description of Study Area ................................................................ 12
Sampling and Examination of Fish ...................................................... 12
Worm Identification ........................................................................ 15
Worm Preparation .......................................................................... 15
Definition of Terms ........................................................................ 16
Data Analysis ............................................................................... 18
RESULTS ............................................................................................ 20
THE DEF INITIVE HOSTS ............................................................... 20
Smallmouth Bass — Descriptive Statistics ...................................... 20
Proteocephalus ambloplitis in Smallmouth Bass ............................. 20
Parenteric Microhabitats in Smallmouth Bass ................................. 21
Enteric Microhabitats in Smallmouth Bass .................................... 27
Largemouth Bass - Descriptive Statistics ...................................... 27
Proteocephalus ambloplitis in Largemouth Bass ............................. 29
Parenteric Microhabitats in Largemouth Bass ................................. 30
Enteric Microhabitats in Largemouth Bass .................................... 33

Descriptive Comparisons Between Smallmouth Bass and
Largemouth Bass ......................................................... 34

Comparisons of Proteocephalus ambloplitis between

Smalhnouth Bass and Largemouth Bass .............................. 35
THE SECOND INTERMEDIATE HOSTS ............................................ 38
Rock Bass — Descriptive Statistics .............................................. 38
Proteocephalus ambloplitis in Rock Bass ..................................... 38
Bluegill — Descriptive Statistics ................................................. 39
Proteocephalus ambloplitis in Bluegill ........................................ 39
DISCUSSION ....................................................................................... 41

TABLE OF CONTENTS (CON’T)

CONCLUSION ...................................................................................... 49
APPENDIX A ....................................................................................... 51
APPENDIX B ....................................................................................... 53
APPENDD( C ....................................................................................... 55
APPENDIX D ....................................................................................... 57
APPENDIX E ........................................................................................ 59
LITERATURE CITED ............................................................................. 61

vi

LIST OF TABLES

Table 1. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis from 6 microhabitats in smallrnouth bass collected in 2000 and 2001 . Page
25.

Table 2. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis from 6 microhabitats in female smallmouth bass collected in 2000 and 2001.
Page 26.

Table 3. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis from 6 microhabitats in male smallmouth bass collected in 2000 and 2001.
Page 26.

Table 4. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis from 6 microhabitats in largemouth bass collected in 2000 - 2001. Page 33.

Table 5. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis from 6 microhabitats in female smallmouth bass collected in 2000 - 2001.
Page 33.

Table 6. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis fi'om 6 microhabitats in male smallrnouth bass collected in 2000 - 2001. Page
34.

Table 7. The prevalence (P) and mean intensity (MI) of Proteocephalus ambloplitis in
smallrnouth bass and largemouth bass examined from Gull Lake, Michigan, collected in
2000 -— 2001. Page 36.

Table 8. The prevalence (P) and mean intensity (MI) of Proteocephalus ambloplitis fiom
parenteric microhabitats in female smallmouth and largemouth bass examined from Gull
Lake, Michigan, collected in 2000 — 2001. Page 36.

Table 9. The prevalence (P) and mean intensity (MI) of Proteocephalus amblopliris fiom
parenteric microhabitats in male smallmouth and largemouth bass examined from Gull
Lake, Michigan, collected in 2000 — 2001. Page 37.

Table 10. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis from 4 microhabitats in rock bass collected in 2000. Page 39.

Table 11. The prevalence, mean intensity, mean abundance, and range of Proteocephalus
ambloplitis from 2 microhabitats in bluegill collected in 2000. Page 40.

vii

LIST OF TABLES (CON’T)
Table B. 1. Number of smallrnouth bass examined, mean length, and length range per
month sampled from Gull Lake, Michigan, collected in 2000 and 2001. Page 54.

Table C. 1. Number of largemouth bass examined, mean length, and length range per
month sampled from Gull Lake, Michigan, collected in 2000 and 2001. Page 56.

Table D. 1. Number of rock bass examined, mean length, and length range per month
sampled from Gull Lake, Michigan, collected in 2000. Page 58.

Table E. 1. Number of bluegill examined, mean length, and length range per month
sampled from Gull Lake, Michigan, collected in 2000. Page 60.

viii

LIST OF FIGURES

Figure 1. Life cycle of Proteocephalus ambloplitis (Modified from Hugghins, 1959).
Page 4.

Figure 2. Location of Gull Lake, Michigan, and five sampling sites where centrarchids
were collected in 2000 and 2001. Page 13.

Figure 3. Bass tapeworm; A) plerocercoid — initial and middle, B) adult proglottid, and
C) scolex. Page 17.

Figure 4. Mean intensity (number of smallmouth bass examined) per month for
Proteocephalus ambloplitis collected in 2000 and 2001. Page 22.

Figure 5. Six microhabitats where Proteocephalus ambloplitis was found (number of
worms removed) in smalhnouth bass collected in 2000 and 2001. Page 23.

Figure 6. Spearman's rank correlation coefficient showing a relationship between length
and number of worms in smallrnouth bass collected in 2000 and 2001. Page 24.

Figure 7. Prevalence of adult and gravid Proteocephalus ambloplitis removed from the
digestive tract of smallrnouth bass (number of fish examined) for each month sampled in
2000 and 2001. Page 28.

Figure 8. Mean intensity (number of largemouth bass examined) per month for
Proteocephalus ambloplitis collected in 2000 and 2001. Page 31.

Figure 9. Six microhabitats where Proteocephalus ambloplitis was found (number of
worms removed) in largemouth bass collected in 2000 and 2001. Page 32.

Figure A. 1. Water temperature recorded at 1 meter depth from Gull Lake, Michigan in
2000 and 2001. Page 52.

ix

INTRODUCTION

Bass tapeworm, Proteocephalus ambloplitis Leidy, 1887 (Eucestoda:
Proteocephalidae) is a common parasite of fishes from North American lakes (Hoffman,
1999). It is a ployzoic cestode, which is nearctic in distribution, has a heteroxenous life
cycle, and is simultaneously hermaphroditic with cross-fertilization. The definitive hosts
are usually in the genera Micropterus and Ambloplites (Centrarchidae). Fischer and
Freeman (1969) suggested that P. amblopliris is one of the most common parasites of the
smallrnouth bass, Micropterus dolomieu. Fish in many families are known to be second
intermediate hosts of P. ambloplitis, such as: Catostomidae, Centrarchidae, Ictaluridae,
Lepisosteidae, Percidae, and Salmonidae (Becker and Brunson, 1968; and Amin, 1990).
This parasite is found less frequently in fishes from lotic environments probably due to
the habitat requirements of the crustacean first intermediate host (V emard, 1940).

Proteocephalus ambloplitis can affect reproduction in the fish definitive host
(Fischer and Freeman, 1969; Esch and Huffines, 1973; Esch et al., 1975, McCormick and
Stokes, 1982). The scar tissue formed by the movements of larval bass tapeworm
through the gonads can cause a decline in the number of eggs released or number of
sperm produced (Esch and Huffines, 1973; McCormick and Stokes, 1982). Eventually,
as the scar tissue becomes more numerous, castration of the fish host may occur. It has
been suggested that the bass tapeworm may be contributing to a decline in the
reproductive potential of smallmouth bass, Micropterus dolomieu, in Gull Lake,
Michigan (Esch and Huffmes, 1973; Dexter, 1996). According to Dexter (1996), Gull

Lake offers more suitable habitat for smallmouth bass than largemouth bass, M.

salmoides. The lake is mesotrophic, having cool and clear water, with little vegetation.
According to net surveys, however, largemouth bass are the more abundant species
(Dexter, 1996). It is usually thought that weedy lakes with mud bottoms, ponds, and
sluggish streams are habitats for largemouth bass, and that smallrnouth bass are found
more often in large, cool, clear lakes and streams (Hubbs and Bailey, 1938). Anecdotal
surveys over the last 50 years from Gull Lake have reported a high level of parasitism,
especially in the gonads of smallrnouth bass, by P. ambloplitis (see Dexter, 1996). Esch
and Huffines (1973), also reported that infections of P. ambloplitis in smallrnouth bass
were extensive and that larval P. ambloplitis may “be an important factor in regulating
the population of smallrnouth bass” in Gull Lake.

One would assume the mean intensity of P. ambloplitis to be higher in
smallmouth bass than in largemouth bass, if indeed P. ambloplitis is affecting the
reproductive potential of smallrnouth bass to such an extent that largemouth bass are out
breeding them, thus becoming more abundant. Furthermore, one would also expect the
mean intensity of P. ambloplitis to be higher in the gonads of smallrnouth bass. Three
hypotheses were formed for this study, they were: 1) the mean intensity of P. ambloplitis
is significantly higher in smallmouth bass when compared to the largemouth bass; 2) the
mean intensity of P. ambloplitis is significantly higher in the gonads of smallrnouth bass
when compared to largemouth bass; 3) bluegill are contributing more to the transmission
of P. ambloplitis than rock bass based upon smallrnouth and largemouth bass diets.

Esch et al. (1975) reported the prevalence of P. ambloplitis in smallmouth bass
from Gull Lake. By comparing these data generated by Esch et al. (1975) to those

observed in the present study it will be determined if the prevalence of P. ambloplitis has

increased in smallmouth bass over time. Esch (1971) also reported the prevalences of
adult and gravid P. ambloplitis in smallrnouth bass and largemouth bass. Rock bass, and
bluegill were not infected with adult or gravid worms from Gull Lake. Esch (1971) did
not report the prevalence of plerocercoids in any of these fish species and only noted if
they were present or absent. One objective of this study will be to compare the
prevalence of adult and gravid P. ambloplitis in the present study to other studies that
were performed in Gull Lake.

This is the first study to quantify the mean intensity of P. ambloplitis in
smallrnouth bass and largemouth bass by specific organ of infiltration in North America.
By examining the infrapopulation biology of P. ambloplitis in these two centrarchid
species it will be possible to compare microhabitat utilization of this worm. This
microhabitat analysis will allow for statistical comparisons within a fish species and

between smalhnouth and largemouth bass.

REVIEW OF THE LITERATURE

Life Cycle

Cooper (1915), Moore (1926), Bangharn (1927), Hunter (1927), and Hunter
(1928) attempted to understand the complete life cycle of P. ambloplitis. However, it
was not until the work of Fischer and Freeman (1969, 1973) and Freeman (1973) that the
entire life cycle was revealed (Figure 1). Adult and gravid worms live in the lumen of the
gut or pyloric ceca of the definitive host. The gravid proglottids and eggs are passed with

the fish feces and enter the aquatic environment. Upon contact with the water the eggs

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are released from the proglottids and settle onto the substrate and surrounding
submergent vegetation. Five species of cyclopoid copepod crustacean (Cyclops albidus,
C. leuckarti, C. prasinus, C. vulgaris, and C. serulatus), and one amphipod crustacean
(Hyalella azteca) may ingest the eggs becoming a first intermediate host (Hunter, 1928).
The egg hatches, releasing the oncosphere, which then penetrates the hemocoel of the
crustacean and the plerocercoid I develops. The first intermediate host may then be eaten
by the fish second intermediate host, usually a centrarchid or percid fish (Fischer and
Freeman, 1969). After consumption, the plerocercoid I bores through the gut and enters
the body cavity of the fish second intermediate host. Further development may occur
parenterally, which results in the formation of the initial plerocercoid II. The definitive
hosts, which are usually the smallmouth bass or the largemouth bass, eat the fish second
intermediate host becoming infected. The ingested initial plerocercoid 11 does not attach
to the gut wall of the definitive host but bores into the body cavity and encysts within
various organs and tissue (Eure, 1976). Development of the worm continues within the
viscera of the definitive host, which produces the middle plerocercoid II. The parenteric
middle plerocercoid II waits for some cue, which may be temperature-dependent or
hormonal, and then migrates from the viscera back into the lumen of the gut or pyloric
ceca (Esch et al., 1975). There it becomes a terminal plerocercoid II and completes the

life cycle by developing into the adult and gravid worm.

Host Terminology for Proteocephalus ambloplitr's

Fischer and Freeman ( 1973) stated that it is not known if fish other than bass are

second intermediate hosts or paratenic hosts. A paratenic or transport host is described as
being “an organism which serves to transfer a larval stage or stages fi'om one host to
another but in which little or no development takes place” (Anderson, 1992).
Proteocephalus ambloplitis plerocercoids do increase in size within the fish second
intermediate host but do not develop into the middle plerocercoid 11 (Fischer and
Freeman, 1973). Further development is required parenterally in the bass definitive host
in order for the middle plerocercoid II to move into the gut lumen, and become gravid.
Even though some growth does take place in the fish second intermediate host the
development is not essential in order to infect the definitive host. Bass, primarily
fingerlings, have been shown to acquire P. ambloplitis by ingesting infected crustaceans
without the need of the fish second intermediate host (Moore, 1926). In this case, the
ingested plerocercoid I would leave the gut, enter the viscera, and develop into the middle
plerocercoid 11.

Bass can become infected by cannibalism or by eating other infected definitive
host species. If a bass infected with the middle plerocercoid II is eaten by another bass
that fish could become infected. The ingested middle plerocercoid 11 may either be
passed with the feces or it may move through the gut wall, and enter the viscera. It is

also possible for a bass to ingest an infected crustacean and become infected.

Life Stage Terminology for Proteocephalus ambloplitis

Freeman (1973) redescribed the different life stages of P. 'ambloplin's, based upon
his work regarding the ontogeny of cestodes. The definition of a procercoid is “a

metacestode which does not develop a scolex” (Freeman, 1973). Proteocephalus

ambloplitis in the crustacean first intermediate host has a scolex and does not fit the
definition of a procercoid. Freeman (1973) concluded that procercoids with a scolex
needed a different name that would better describe the morphological characteristics seen
in the crustacean first intermediate host. Freeman (1973) suggested the terms below be
used when referring to different life stages of P. ambloplitis. In the crustacean first
intermediate host the term “procercoid” is changed to “acaudate invaginated
glandacetabulo-plerocercoid”. This term is very descriptive of the cestodes morphology;
“acaudate” refers to the absence of the cercomer, the prefix “glan -” describes the
secretory apical end, and the suffix “- acetabulo” refers to the acetabulum or suckers.
The new term for visceral worms in the fish second intermediate and definitive host is
“invaginated glandacetabulo-plerocercoid II” which replaces “plerocercoid”. Lastly, the
term “acetabulo-plerocercoid before proglottisation” describes the plerocercoids within
the gut lumen of the definitive host. The loss of the prefix “gland -“ describes the loss or
reduction of the apical organ during penetration into the gut of the bass. Modified forms

of these terms will be used herein and are in accordance with Fisher and Freeman (1973).

Pathology associated with Proteocephalus ambloplitis

The effects of P. ambloplitis on fish second intermediate and definitive hosts have
been investigated by Amin (1990), Bailey (1984), Becker and Brunson (1968), Esch and
Huffines (1973), Esch et al. (1975), Fischer and Freeman (1969), Hugghins (1959), Joy
and Madan (1989), McCormick and Stokes (1982), and Moore (1926). The movement of

the plerocercoid 11 through the viscera can have severe effects on fish health and

reproduction. It has been demonstrated that fibrosis of the gonadal tissue can occur if
penetrated by parenteric plerocercoids, which could ultimately lead to “parasitic
castration” and a decrease in reproductive potential of the fish host. Moore (1926), stated
(pg. 91) “. . . infestation by the worms inhibits the development of both egg and spawn
and promotes general sterility”, and Hugghins (1959) suggested (pg. 40) that P.
ambloplr’tis is “the most damaging tapeworm of fresh-water fishes.”

Esch and Hufi'mes (197 3) examined the histopathology associated with P.
ambloplitis from the smallrnouth bass of Gull Lake, Michigan. They reported a definite
reduction in the reproductive potential of bass based on histologic study. They also
found the damage usually more severe in young males. Similarly, Esch et al. (1975)
found the most extreme pathology in the testes of young male smallmouth bass. Esch
and Huffines (1973) observed extensive scarring throughout the oviducts of females and
that cysts containing necrotic tissue were present, suggesting this could prevent the
shedding of eggs.

McCormick and Stokes (1982) reported on the severity of P. ambloplitis
infections in female M. dolomieu from northeastern Minnesota, and found parenteric
plerocercoids invading advanced vitellogenic oocytes. The damage to the oocytes was
extensive and the nutrient rich yolk material was lost and absorbed by the worm. Joy and
Madan (1989) found 85% of M. salmoides and 91% of spotted bass, M. puncrulatus,
infected with P. ambloplitis from Beech Fork Lake, West Virginia. Liver damage was
characterized by the paucity of bile ducts, congested blood vessels, replacement of liver
parenchyma by plerocercoids, fibrous adhesions, and collagen formation. Joy and Madan

(1989) concluded the severe damage to the liver of these fish may play an important role

in regulating bass populations in this lake. These authors suggested, that based on
intensity, M. salmoides is the favored host species. Fischer and Freeman (1969) found all
877 M. dolomieu examined from Lake Opeongo, Ontario, infected with parenteric
plerocercoids. These authors suggested that the wandering plerocercoids could damage
the gonads to such an extent that spawning is inhibited.

Amin (1990) studied P. amblopliris in 13 species of fish from 2 southeastern
Wisconsin lakes. He determined that 55% of the plerocercoids in smallmouth bass,
found during the summer, were associated with the gonads. Further, the plerocercoid
penetration of the ovarian expansive stroma was commonly observed and the unilateral
hypertrophy of the ovaries resulted in the destruction of many eggs. Damage was also
done to the hepatic tissue of bluegill by parenteric plerocercoid movement through the
viscera. Bailey (1984) reported that plerocercoids of P. ambloplitis were causing the
formation of fibrotic liver cysts in the bluegill intermediate host. This author described
the cysts as being composed of strands of melanotic connective tissue that were restricted

to areas of plerocercoid infection.

Seasonal Patterns of Proteocephalus ambloplitis

The parenteric middle plerocercoid II in the bass definitive host migrates fi'om the
viscera to the gut lumen or pyloric ceca to finish development by becoming gravid. The
timing of this movement has been theorized by many researchers as being seasonal. In
the early spring fish have no P. ambloplitis in the digestive tract, but as the water warms

the plerocercoids migrate to the gastrointestinal tract. Throughout the summer the

prevalence of adult and gravid P. ambloplitis in the gastrointestinal tract increases.
Furthermore, as the fall season approaches water temperature begins to drop and the adult
and gravid worms in the gastrointestinal tract are voided and no enteric worms are
reported from fish in the winter season (Esch et al., 1975), even though they did not
examine any fish from the winter.

Some aspect of the seasonal patterns of P. ambloplitis in bass and other fish from
the United States and Canada has been investigated by Fischer and Freeman (1969,
1973), McDaniel and Bailey (1974), Cloutman (1975), Esch et al. (1975), Eure (1976),
Ingham and Dronen (1982), Amin (1990), Amin and Cowen ( 1990), Fischer and Kelso
(1990), and Szalai and Dick (1990). Although all of these studies correlate temperature
and season to the plerocercoid migration, they suggest that hormones may be a factor due
to the correlation with spawning times.

Fischer and Freeman (1969) investigated the seasonal patterns of P. ambloplitis in
smallrnouth bass from Lake Opeongo, Ontario. They found that a rise in temperature
from 4°C to 7°C triggered the migration of parenteric plerocercoids into the gut lumen.
They followed up this finding with lab experiments and were able to duplicate this
temperature-dependent migration of P. ambloplitis in smallrnouth bass. These authors
also reported that as the summer progressed the incidence of P. ambloplitis in the gut
declined, became less frequent in the early fall, and did not persist in the gut during the
winter. It was also noted that no worms were found in the gut during the month of April,
however; parenteric plerocercoids were found penetrating the gut wall in May and early
June.

Esch et al. (1975) studied the population biology of P. ambloplitis in smallmouth

10

bass from Gull Lake, Michigan. These researchers found that as the lake warmed from
4°C in April the prevalence of adult P. ambloplitis in the gut increased. The overall
percent occurrence of adult worms reached 50% in late May and remained that way until
the prevalence decreased in late August Similar to Fischer and Freeman (1969), Esch et
al. (1975) also suggested that smallrnouth bass in Gull Lake are free of P. ambloplitis in
winter. Esch et al. (1975) did not report the intensity of P. ambloplitis in smallrnouth
bass from Gull Lake. It was also reported by Esch et al. (1975) that the recruitment of
adult tapeworms occurs only once a year in bass. Esch at al. (1975) and Fischer and
Freeman (1969) are in agreement that it is the rise in temperature from 4°C to 7°C that is
essential for the migration into the gut, and that event would only occur once in the
spring. Finally, Esch et al. (1975) suggested that other events might influence
plerocercoid migration, such as increasing photoperiod or increases in gonadotrophic and

gonadal hormones.

ll

MATERIALS AND METHODS

Description of Study Area

Gull Lake is located within Barry and Kalamazoo Counties in southwestern
Michigan (Figure 2). Gull Lake is mesotrophic and has a drainage area of approximately
17,000 acres and the total surface area of lake is 2,030 acres (6.4 kilometer long and 1.6
kilometer wide); the deepest area of the lake is 33.5 meter while 30% of the lake is less
then 3 meter deep and the lake bottom is composed primarily of sand, gravel, and rubble;

water quality is excellent (Esch, 1971; Dexter, 1996).

Sampling and Examination of Fish

Four species of centrarchids were examined for P. ambloplitis in this study. Two
species (smallmouth bass, Micropterus dolomieu and largemouth bass, M. salmoides) are
considered definitive hosts; the remaining two species (rock bass, Ambloplites rupestris
and bluegill, Lepomis macrochirus) are considered second intermediate hosts. Fish were
collected in April — September 2000 and April - July 2001 from five different sampling
sites KBS-l, KBS-2, Miller’s Marsh, South Lake, and North Lake (Figure 2). KBS-l,
KBS-2, South Lake and North Lake have sand and cobble substrate with no vegetation;
fish were caught at the depth of 2 — 8 meters. Miller’s Marsh is approximately 1 — 3
meters in depth and has a soft bottom with submergent and emergent vegetation, and

woody debris. Smallmouth bass were not collected from this site. Fish caught fi'om

l2

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different sites were combined for the analyses. Fish were collected during three seasons
that are defined as: spring (April and May), summer (June — August), and fall
(September). Water temperature was also taken at the depth of 1 meter at the time of
sampling (Appendix A).

Several different methods were used to capture fish. The most successful one was
angling, using either worm and bobber rigs or artificial lures. Fish were also sampled
using a 30.5 x 1.2 meter shallow water fyke net with 3 centimeter mesh size, and by
electrofishing. Fish collected for this project by residents of Gull Lake were frozen and
picked up at a later date. Fish that I collected were placed within coolers of water and
transported to Michigan State University, killed by an overdose of the anesthetic MS-222
(Tricaine methane sulfonate), put into zip-lock bags, individually labeled, frozen, and
examined later. Two fish were examined within 2 hours of collection to obtain live
worms.

At time of necropsy the fish was sexed and standard length measurement (mm)
was taken. Organs and tissues (testes, ovaries, liver, spleen, mesentery, stomach,
intestine, and pyloric ceca) were removed and placed into separate petri dishes. Each
organ and tissue was then carefully dissected and all life stages of P. ambloplitis were
counted, removed, and preserved in 70% ethyl alcohol. In many cases the amount of
fibrous adhesions surrounding the organs was great, and many organs could not be
differentiated. However, with great care, the fibrous adhesions were peeled away from
the organs. This peeling procedure also removed the mesentery; therefore both tissue

types (mesentery and fibrous adhesions) were placed into a petri dish and examined.

14

Worm Identification

Amin and Boarini (1992) described the various plerocercoids of P. ambloplitis
from several fish species using morphometric characteristics that were given as a mean
(mm) 2!: SD. The initial plerocercoid II from the bluegill has a body length of 11.10 i
9.20, scolex width 0.95 :1: 0.23, lateral sucker diameter 0.29 :t: 0.10, and accessory apical
sucker diameter 0.28 at 0.11. The middle plerocercoid II and initial plerocercoid II from
the body cavity of Micropterus spp. have a body length of 4.69 :t: 6.53, scolex width 0.60
i 0.20, lateral sucker diameter 0.20 :t 0.06, and accessory apical sucker diameter 0.20 :h
0.06. The terminal pleroceroid H from the gut lumen of Micropterus spp. has a body
length of 41.34 i 44.49, scolex width 0.71 :t 0.16, lateral sucker diameter 0.29 i 0.05,
and accessory apical sucker diameter of 0.05 :l: 0.07.

Adult and gravid worms were identified according to Hoffman (1999). The
vestigial apical sucker is present; testes are dorsal to the uterus; cirrus pouch is lateral,
extending over 1/3 of the proglottids; vitellaria are marginal; vaginal opening is lateral
and anterior to genital atrium; eggs are dumbbell shaped, and embryonated. All gravid
worms were identified by having the characteristic dumbbell shaped eggs. Drawings of

various life stages are in Figure 3.

Worm Preparation

Live worms were removed and placed in a petri dish containing hot water (~ 80°

C). After 30 minutes the worms had relaxed, died and were then preserved in 10%

15

formalin. Worms removed fi'om fi'ozen fish were preserved in 70% ethyl alcohol.
Preserved worms were then stained using borax carmine and dehydrated in a graded
ethanol series. Stained worms were cleared in xylene and permanently mounted onto

slides using Canada Balsam.

Definition of Terms

Prevalence is defined as the percentage of fish infected with Proteocephalus
ambloplitis, mean intensity is the mean number of P. ambloplitis in infected fish, m_;_can
abundance is the mean number of P. ambloplitis in all fish examined. The definitive
m are the smallmouth bass and largemouth bass; second intermediate hosts are the
rock bass and bluegill. Even though rock bass have been shown to serve as definitive
hosts in other studies, I feel since no enteric worms were found in this species it is more
appropriate to classify this fish as a second intermediate host in Gull Lake. Life cycle
terminology that I use is in accordance with Fischer and Freeman (1973). In the fish
second intermediate host the term initial plerocercoid II will be used to describe the
worms. Four different developmental stages of P. ambloplitis were found in the fish
definitive host, they are, middle plerocercoid [I (found in the visceral organs), _t_;___erminal__:__
pgtrocercoid II. flult worm, and avid worm (found in the lumen of the digestive tract).
Adult worms are strobilized but are not producing eggs; gravid worms are strobilized and
are producing eggs. Mulation will be defined as all of the parasites of a single

species in one host (Esch and Fernandez, 1993). In this study I will define 2 major types

of infrapopulations within each fish host, they are the mteric immation (located

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outside the digestive tract) and enteric inframpulation (located inside the digestive tract).
Both infrapopulations are comprised of several microhabitats. The parenteric
infrapopulation is comprised of six microhabitats and they are the gonad (combined
female and male fish), testes, ovaries, liver, spleen, and mesentery. Worms recovered
from these microhabitats were all plerocercoids (initial or middle). The enteric
infrapopulation is comprised of two microhabitats and they are the pyloric ceca and small
intestine. Worms recovered from these microhabitats were of three different

developmental stages (terminal plerocercoid, adult, and gravid).

Data Analysis

A three-way nonparametric AN OVA was used to evaluate differences in the mean
intensity and test for interaction between fish species (smallmouth bass and largemouth
bass), sex, and microhabitat. A two-way nonparametric AN OVA and Tukey’s posthoc
test was used to evaluate differences in the mean intensity and test for interaction
between sex and microhabitat within fish species. Further analyses within fish species
were done by rank transforming the data and using a one-way ANOVA and Tukey’s
posthoc test for multiple comparisons. A Mann—Whitney U-test was used to compare
overall mean intensity of P. ambloplitis between male and female fish of the same
species and overall mean intensity among fish species. A Kruskal—Wallis nonparametric
one-way AN OVA test was used to compare mean intensity and fish lengths among
months sampled. Paired and unpaired t-tests were used to compare male and female fish

lengths. Chi-square analysis was performed to compare the prevalence of intestinal

l8

worms in smallrnouth bass for each month to look for a seasonal pattern in the summer
and fall, and to compare the prevalence of worms found in rock bass and bluegill. A
Spearman’s rank correlation coefficient was generated to investigate if a correlation
existed between the number of worms and fish length. All mean intensity and mean
abundance values are expressed as a mean :t standard deviation (SD). All descriptive and
statistical calculations were done using E-Z Stat for windows® version 1.0.1; Systat 10®

for windows; and PC — SAS version 8.1® for windows.

19

RESULTS
THE DEFINITIVE HOSTS

Smallmouth Bass - Descriptive Statistics

A total of 54 (32 female and 22 male) smallmouth bass was collected in June —
September 2000 and in May - June 2001 and examined for P. ambloplitis fiom Gull
Lake. The number of fish examined, mean lengths and length ranges per month can be
found in Appendix B. The mean length (mm) for all fish was 223.1 :1: 42.1. The mean
length for female and male fish was 224.9 i 41.7 and 218.9 1 42.8, respectively. There
was no statistical difference between the lengths of female and male fish (U npaired t-test,
t = 0.514, d.f. = 52, P = 0.608). The mean length of smallrnouth bass, per month,
significantly varied over the June -- September 2000 sampling period (Kruskal-Wallis
test, H =26.6, d.f. = 3, P < 0.001); fish from 2001 were not included in this analysis
because only three fish were examined in two months. This difference occurred because
the fish sampled in September 2000 were smaller than fish sampled from other months.
The mean lengths of smallrnouth bass in 2000 and 2001 were 221.4 1: 42.5 and 250.0 i
18.1, respectively. There was no statistically significant difference in the mean length

between 2000 and 2001 (Unpaired t—test, t = -1.15, d.f. = 52, P = 0.255).

Proteocephalus ambloplitis in Smallmouth Bass

The overall prevalence and mean intensity of P. ambloplitis in smallrnouth bass

was 100% and 72.5 :1: 44.8, respectively, in 2000 - 2001. The mean intensity of P.

20

ambloplitis in female and male fish was 80.4 d: 48.6 and 60.9 :1: 36.7, respectively. There
was a statistically significant difference in the mean intensity of P. ambloplitis among the
months sampled in 2000 (Kruskal-Wallis test, H = 13.8, d.f. = 3, P = 0.003); fish from
2001 were not included in this comparison because the sample sizes were too small
(Figure 4). This difference occurred because the fish in September 2000 were
statistically smaller than fish sampled fi'om other months, and they had fewer worms.
The mean intensity of P. ambloplitis was not significantly different during June, July, and
August 2000 (Kruskal-Wallis test, H = 0.972, d.f. = 2, P = 0.615). The mean intensity of
P. ambloplitis in 2000 and 2001 were 73.7 d: 45.4 and 52.3 i 31.5, respectively. There
was no statistically significant difference in the mean intensity between the years 2000
and 2001 (Mann-Whitney U-test, U = 97, d.f. = 52, P = 0.459) however; these results
may be biased since only two fish were examined in 2001. A total of 3,926 P.
ambloplitis was found in smallrnouth bass, including all life stages. The number of P.
ambloplitis fiom each microhabitat is in Figure 5. A significant correlation did exist
between fish length and the number of P. ambloplitis (Spearman’s correlation, rs = 0.497,

P < 0.001), Figure 6.

Parenteric Microhabitats in Smallmouth Bass

The prevalence, mean intensity, and mean abundance of P. ambloplitis in each
microhabitat of combined female and male fish (Table 1), only female fish (Table 2), and
only male fish (Table 3) were calculated. A total of 3,581 worms were recovered from

parenteric microhabitats. This accounts for 91.2% of all the worms recovered from this

21

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parenteric microhabitats. This accounts for 91.2% of all the worms recovered from this
fish species. All worms found in parenteric microhabitats were middle plerocercoid II
stages. A nonparametric two-way AN OVA was used to evaluate differences in mean
intensity and test for interaction between two main effects (sex and microhabitat) in
smallmouth bass. A statistically significant difference was found between the sexes (2-
Way ANOVA, F = 4.63, d.f. = 1, P = 0.032) and between microhabitats (2-Way
ANOVA, F = 19.99, d.f. = 3, P < 0.0001). Since there was significant interaction
between main effects (2-Way ANOVA, F = 4.85, d.f. = 3, P = 0.028) no further analyses

could be done to test for differences between the sexes.

Table 1. The prevalence, mean intensity, mean abundance, and range of

Proteocephalus ambloplitis from 6 microhabitats in smallmouth bass collected in

 

2000 - 2001.

Microhabitat Prevalence Mean Intensity i SD Mean Abundance :1: SD Range
Parenteric

Gonads 96 26.2 :1: 18.6 25.2 :1: 18.9 0 - 76

Liver 100 15.1 :1: 13.4 15.1 :1: 13.4 0 - 77

Spleen 85 4.5 :1: 6.7 5.6 :l: 6.6 0 - 38

Mesentery 100 20.4 :1: 15.5 20.4 :I: 15.5 3 - 86

Enteric

Pyloricceca 50 12.1 :l: 14.1 6.1i11.6 0-31

Intestine 18.5 1.7 i 0.82 0.31 i 0.74 0 - 39

 

When analyzing the mean intensity of P. mnbloplitis from parenteric
microhabitats found in only female fish (Table 2) highly significant differences occurred
(l-Way ANOVA, F = 31.59, d.f. = 3, P < 0.0001). A statistically significant difference
in the mean intensity existed between the ovaries and liver, ovaries and spleen, and

ovaries and mesentery (P < 0.05 for all pair-wise comparisons, Tukey’s test).

25

When analyzing the mean intensity of P. ambloplitis from parenteric
microhabitats found in only male fish (Table 3) a significant difference occurred (l-Way
ANOVA, F = 4.72, d.f. = 3, P < 0.001). A statistically significant difference in the mean
intensity existed between the testes and spleen (P < 0.05, Tukey’s test). Significant
differences did not occur when the testes were compared to the liver and mesentery (P >

0.10 for all pair-wise comparisons, Tukey’s test).

Table 2. The prevalence, mean intensity, mean abundance, and range of
Proteocephalus ambloplitis from 6 microhabitats in female smallmouth bass

collected in 2000 - 2001.

 

Microhabitat Prevalence Mean Intensity :1: SD Mean Abundance 1: SD Range
Parenteric

Ovaries 94 34.0 i 18.9 31.9 :1: 20.1 0 - 76
Liver 100 14.9 :1: 14.4 14.9 d: 14.4 3 - 77
Spleen 84 5.5 :1: 4.3 4.7 :1: 4.4 0 - l9
Mesentery 100 21.51 18.2 21.511: 18.2 4-86
Enteric

Pyloricceca 44 12.6:1: 10.1 5.5 21:9.1 0-31

Intestine 25 1.75 i 0.88 0.43 :1: 0.87 0 - 3

 

Table 3. The prevalence, mean intensity, mean abundance, and range of

Proteocephalus ambloplitis from 6 microhabitats in male smallmoutb bass collected

 

in 2000 - 2001.

Microhabitat Prevalence Mean Intensity :t SD Mean Abundance i SD Range
Parenteric

Testes 100 15.5:1: 11.8 15.51: 11.8 1-43
Liver 100 15.21: 11.9 15.21119 1-52
Spleen 86 8.1 :1: 9.0 6.9 i 8.8 0 - 38
Mesentery 100 18.9 :1: 10.5 18.9 :1: 10.5 3 - 47
Enteric

Pyloric ceca 38 7.7 :1: 7.3 2.9 :1: 5.8 0 - 21

Intestine 3 2.0 0.06 i 0.35 0 - 2

 

Enteric Microhabitats in Smallmouth Bass

A total of 345 worms were recovered from enteric microhabitats. This accounts
for 8.7% of all the worms recovered from this fish species. Developmentally, 122
(35.3%) terminal plerocercoid II, 64 (18.5%) adult, and 159 gravid (46.0%) worms were
found in smallrnouth bass. The mean intensity of all life stages of P. ambloplitis from
enteric microhabitats, in combined female and male fish, was calculated (Table 1). A
statistically significant difference in the mean intensity existed between the pyloric ceca
and small intestine (Mann-Whitney U-test, U = 226, d.f. = 35, P < 0.001). The overall
prevalence of adult and gravid worms in smallmouth bass was 43%. When the
prevalence of combined adult and gravid P. ambloplitis was compared among months
sampled from 2000 - 2001 significant differences were found (112 = 18.19, d.f. = 4, P =
0.0025). The prevalence was highest in June 2001, however this prevalence may be
misleading since only two fish were examined (Figure 7). When the prevalence of adult
and gravid P. ambloplitis was compared among months in 2000 significant differences

were found (112 = 14.86, d.f. = 3, P = 0.0025), Figure 7.
Largemouth Bass - Descriptive Statistics

A total of 88 (44 female and 44 male) largemouth bass was collected in April —
September 2000 and in April — July 2001 and examined for P. ambloplitis from Gull

Lake. The number of fish examined, mean lengths and length ranges per month can be

found in Appendix C. The mean length (mm) for all fish was 214.7 i 39.7. The mean

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length for female and male fish was 226.3 i 45.3 and 203.2 i 29.4, respectively. A
significant difference existed between the lengths of female and male fish (Paired t-test, t
= 3.5, d.f. = 43, P = 0.001). This is probably due to the April 2001 sample, which was
primarily made up of large females (Appendix C). The mean length of largemouth bass,
per month, was significantly different over the two-year sampling period (Kruskal-Wallis
test, H = 40.3, d.f. = 6, P < 0.001). The mean lengths of largemouth bass in 2000 and
2001 were 199.9 3: 27.4 and 231.0 i 44.8, respectively. The mean length was
significantly larger in the fish sampled from 2001 compared to 2000 (Mann-Whitney U-
test, U = 1,422, d.f. = 86, P < 0.001). Again, this occurred because the fish sampled from

April 2001 were much larger than fish examined in any other months.

Proteocephalus ambloplitis in Largemouth Bass

The overall prevalence and mean intensity of P. ambloplitis in largemouth bass
was 100% and 18.1 :1: 12.9, respectively, in 2000 - 2001. The mean intensity of P.
ambloplitis in female and male fish was 17.9 :1: 12.8 and 18.4 i 13.2, respectively. There
was no statistical difference between the mean intensity of P. ambloplitis in female and
male fish (Paired t-test, t = -0.177, d.f. = 43, P = 0.859). The mean intensity was not
significantly different among the months sampled 2000 — 2001 (Kruskal-Wallis test, H =
9.1, d.f. = 6, P = 0.163), Figure 8; the sample from September 2000 was removed
because the sample size was too small. The mean intensity of P. ambloplitis in 2000 and p
2001 was 18.1 i 14.4 and 18.3 i 11.3, respectively. There was no statistically significant

difference in the mean intensity between the years 2000 and 2001 (Mann-Whitney U-test,

29

U = 1,042, d.f. = 86, P = 0.526) however these results may be biased since too few fish
were collected in April, July and September 2000. A significant correlation did not exist
between fish length and number of P. ambloplitis (Spearman’s correlation, r, = -0.168, P
= 0.116). A total of 1,607 P. ambloplitis was found in largemouth bass, including all life

stages. The number of P. ambloplitis removed from each microhabitat can be found in

Figure 9.

Parenteric Microhabitats in Largemouth Bass

The prevalence, mean intensity, and mean abundance of P. ambloplitis within
each microhabitat of combined female and male fish (Table 4), only female fish (Table
5), and only male fish (Table 6) was calculated. A total of 1,554 worms were recovered
from parenteric habitats. This accounts for 96.7% of all the worms recovered from this
fish species. All worms found in parenteric microhabitats were middle plerocercoid II
stages. A nonparametric two-way AN OVA was used to evaluate differences in mean
intensity and test for interaction between two main effects (sex and microhabitat) in
largemouth bass. A statistically significant difference was found between the
microhabitats (2-Way ANOVA, F = 27.52, d.f. = 3, P < 0.0001). No statistically
significant differences were found between the sexes (2-Way ANOVA, F = 0.02, d.f. = l,
P = 0.889). Since there was no significant interaction between main effects (2-Way
ANOVA, F = 0.93, d.f. = 3, P = 0.475) further analyses could be done to test for
differences between microhabitats (Table 4). A statistically significant difference in the

_ mean intensity existed between the liver and gonads, and the mesentery and gonads (P <

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0.05, for all pair-wise comparisons, Tukey’s test). Significant differences did not occur

when the gonads were compared to the spleen (P > 0.05, Tukey’s test).

Table 4. The prevalence, mean intensity, mean abundance, and range of

Proteocephalus ambloplitis from 6 microhabitats in largemouth bass collected in

 

2000 - 2001.

Microbabitat Prevalence Mean Intensity :t SD Mean Abundance :t SD Range
Parenteric
Gonads 64 3.7:3.0 2.3 13.1 0-19
Liver 86 8.1 i 8.4 7.0 :1: 8.3 0 - 44
Spleen 41 2.1 i 1.5 0.85 i 1.4 0 - 7
Mesentery 93 7.9 i 7.8 7.3 :t 7.8 0 - 44
Enteric
Pyloric ceca 13 4.4 i 3.5 0.55 :1: 1.9 0 - 12
Intestine 2 1.0 0.02 :1: 0.14 O - l

 

Table 5. The prevalence, mean intensity, mean abundance, and range of

Proteocephalus ambloplitif from 6 microhabitats in female largemouth bass collected

 

in 2000 - 2001.

Microhabitat Prevalence Mean Intensity :1: SD Mean Abundance :1: SD Range
Parenteric
Ovaries 70 3.2 :1: 1.9 2.3 :1: 2.2 0 - 9
Liver 86 8.2 i 9.0 3.2 i 2.0 0 - 44
Spleen 4] 18¢ 1.5 0.7: 1.3 0-7
Mesentery 87 7.1 i 6.0 4.5 i 6.1 0 - 34
Enteric
Pyloric ceca 18 5.5 i 3.5 1.0 i 2.5 0 - 12
Intestine 2 1.0 0.02 i 0.15 0 - 1

 

Enteric Microhabitats in Largemouth Bass

A total of 53 worms were recovered from enteric microhabitats. This accounts for 3.3%
of all the worms recovered from this fish species. All stages found in the digestive tract

were terminal plerocercoid II; no adult or gravid worms were found. Worms were

33

Table 6. The prevalence, mean intensity, mean abundance, and range of

Proteocephalus ambloplitis from 6 microhabitats in male largemouth bass collected

 

in 2000 - 2001.

Mlcrohabitat Prevalence Mean Intensity :1: SD Mean Abundance :1: SD Range
Parenteric

Testes 57 4.3 :1: 3.9 2.4 :1: 3.7 0 - l9
Liver 86 8.1 i 7.9 6.9 i 7.8 0 - 31
Spleen 50 3.9 :t 3.3 1.9 i 3.0 0 - 5
Mesentery 98 8.6 i 9.2 8.4 i 9.1 O - 44
Enteric

Pyloric ceca 9 2.2 3: 1.5 0.20 :t 0.76 0 - 4
Intestine 0 0 0 0

 

found more often in the pyloric ceca than in the intestine in which only two worms were

found (Table 4).

Descriptive Comparisons Between Smallmouth Bass and Largemouth Bass

The mean length (mm) for smallrnouth and largemouth bass were 223.1 :1: 42.1
and 214.7 :1: 39.7, respectively. No statistical difference existed between the lengths of
these two fish species (Unpaired t-test, t = 1.18, d.f. = 140, P = 0.239). Female
smallrnouth and largemouth bass had mean lengths of 224.9 :t 41.7 and 226.3 :1: 45.3,
respectively, and they were not significantly different (Unpaired t-test, t = - 0.132, d.f. =
74, P = 0.894). Male smallmouth bass and largemouth bass had mean lengths of 21 8.9 :1:
42.8 and 203.2 :1: 29.4, respectively, and they were not significantly different (Mann-
Whitney U-test, U = 590, d.f. = 64, P = 0.149). Similar lengths indicate similar ages of

fish and thus eliminating any age biases.

34

Comparisons of Proteocephalus ambloplitr’s between smallmouth bass and

largemouth bass

The overall mean intensity of P. ambloplitis in smallrnouth bass and largemouth
bass was 72.5 i 44.8 and 18.1 i 12.9, respectively. The overall mean intensities of P.
ambloplitis were significantly higher in the smallrnouth bass than in largemouth bass
(Mann-Whitney U-test, U = 4,452, d.f. = 140, P < 0.001). The prevalence and mean
intensity of P. ambloplitis for combined female and male smallrnouth and largemouth
bass by microhabitat are in Table 7. The prevalence and mean intensity of P. ambloplitis
removed from parenteric microhabitats in female smallrnouth and largemouth bass was
compiled (Table 8). The overall mean intensity of P. ambloplitis in female smallrnouth
and largemouth bass was 80.4 i 48.6 and 17.9 i- 12.8, respectively. The mean intensity
of P. ambloplr'tis was significantly higher in female smallmouth bass (Mann-Whitney U-
test, U = 1,352, d.f. = 74, P < 0.001) than female largemouth bass. The prevalence and
mean intensity of P. ambloplitis removed from parenteric microhabitats in male
smallrnouth and largemouth bass was compiled (Table 9). The overall mean intensity of
P. ambloplitis in male smallrnouth and largemouth bass was 60.9 i 36.7 and 18.4 :1: 13.2,
respectively. The mean intensity of P. ambloplitis was significantly higher in male
smnnmeuth bass (Mann-Whitney U-test, U = 878, d.f. = 63, P < 0.001) than male
largemouth bass.

A nonparametric three-way AN OVA was used to evaluate differences in mean
intensity and test for interaction among three main effects (sex, microhabitat, and species)

between smallrnouth and largemouth bass. A statistically significant difference was

35

found among the microhabitats (3-Way ANOVA, F = 29.09, d.f. = 3, P < 0.0001) and
between species (3-Way ANOVA, F = 203.86, d.f. = 1, P < 0.0001). No statistically
significant differences were found between the sexes (3-Way ANOVA, F = 3.2, d.f. = l,
P = 0.0744). Since there was significant interaction between all three main effects (3-
Way ANOVA, F = 6.41, d.f. = 3, P = 0.0003) no further analyses could be done to test

for differences in the mean intensity of P. ambloplitis between the two fish species.

Table 7. The prevalence (P) and mean intensity (Ml) of Proteocephalus ambloplitr’s
in smallmouth bass and largemouth bass examined from Gull Lake Michigan

collected in 2000 — 2001.

 

Smallmouth Bass MM
Microhabitat P (%) MI :t SD P (%) MI :t SD
Parenteric
Gonad 96 26.2 i 18.6 64 3.7 i: 3.0
Liver 100 15.1 d: 13.4 86 8.1 :1: 8.4
Spleen 85 4.5 i 6.7 93 7.9 :1: 7.8
Mesentery 100 20.4 i 15.5 41 2.1 i 1.5
Enteric
Pyloric ceca 50 12.1 :1: 14.1 13 4.4 :1: 3.5
Intestine 18.5 1.7 i 0.82 2 1.0

 

Table 8. The prevalence (P) and mean intensity (MI) of Proteocephalus ambloplia's
from parenteric microhabitats in female smallrnouth and largemouth has examined

from Gull Lake, Michigan, collected in 2000 — 2001.

 

Smallmouth Bass W
Microhabitat P (%) MI :1: SD P (%) M] i SD
Ovaries 94 34.0 i 18.9 70 3.2 i 1.9
Liver 100 14.9 :1: 14.4 86 8.2 i 9.0
Spleen 84 5.5 i: 4.3 41 1.8 :1: 1.5
Mesentery 100 21.5 1: 18.2 87 7.1 :t 6.0

 

36

Table 9. The prevalence (P) and mean intensity (MI) of Proteocephalus ambloplia’s
from parenteric microhabitats in male smallrnouth and largemouth bass examined

from Gull Lake, Michigan, collected in 2000 - 2001.

 

_____Smallmouth Bass Lam—flags
Microhabitat P (%) MI i SD P (%) MI :1: SD
Testes 100 15.5 i 11.8 57 2.4 i 3.7
Liver 100 15.2 i 11.9 86 6.9 i 7.8
Spleen 86 8.1 i 9.0 50 1.9 :t 3.0

Mesentery 100 18.9 i 10.5 98 8.4 i 9.1

37

THE SECOND INTERMEDIATE HOSTS

Rock Bass - Descriptive Statistics

A total of 50 (25 female and 25 male) rock bass was collected in April —
September 2000 and examined for P. ambloplitis fiom Gull Lake. The number of fish
examined, mean lengths and length ranges per month can be found in Appendix D. The
mean length (mm) for all fish was 151.7 i 23.4. The mean length for female and male
fish was 153.4 i 26.2 and 150.2 i 20.7, respectively. There was no significant difference
between the lengths of female and male fish (Paired t-test, t = 0.504, d.f. = 24, P = 0.618).
The mean lengths of rock bass, per month, were significantly different over the 6-month
sampling period (Kruskal-Wallis test, H = 20.4, d.f. = 5, P <0.001), with July and April

having fish with the largest mean lengths.

Proteocephalus ambloplitis in Rock Bass

The overall prevalence and mean intensity of P. ambloplitis in rock bass was 32%
and 3.5 i 3.6, respectively, in 2000. Only the initial plerocercoid II was found in rock
bass. The mean intensity of P. ambloplr‘tis in female and male fish was 5.2 i- 3.7 and 2.8
i 3.4, respectively. There was no statistical difference between the mean intensity of P.
ambloplitis in female and male fish (Mann-Whitney U-test, U = 40, d.f. = 14, P = 0.176).
A total of 57 P. ambloplitis was found in rock bass. A significant correlation did not
exist between fish length and number of P. ambloplitis (Spearman’s correlation, r, =

0.434, P = 0.092). The prevalence, mean intensity, and mean abundance of P.

38

ambloplitis from each microhabitat of combined female and male fish (Table 10) was

calculated.

Table 10. The prevalence, mean intensity, mean abundance, and range of

Proteocephalus ambloplitis from 4 microhabitats in rock bass collected in 2000.

 

Microhabitat Prevalence Mean Intensity i SD Mean Abundance :t SD Range
Parenteric
Gonad 4 2.0 :1: 1.4 0.08 :1: 0.44 0 - 3
Liver 22 2.0 :1: 1.2 0.44 :1: 1.0 0 - 4
Mesentery 10 5.4 :1: 2.5 0.54 :1: 1.7 0 - 8
Spleen 4 1.0 0.04 :1: 0.19 0 - l

 

Bluegill - Descriptive Statistics

A total of 50 (24 female and 26 male) bluegill was collected in May - September
2000 and examined for P. ambloplitis fi'orn Gull Lake. The number of fish examined,
mean lengths and length ranges per month can be found in Appendix E. The mean length
(mm) for all fish was 122.4 i 24.0. The mean length for female and male fish was 115.2
1 25.8 and 129.1 :1: 20.5, respectively. There was a significant difference between the
lengths of female and male fish (Unpaired t-test, t = 2.11, d.f. = 48, P = 0.039). The
mean lengths of bluegill, per month, were significantly different over the 5-month
sampling period (Kruskal-Wallis test, H = 17.2, d.f. = 3, P < 0.001), with May and

August having fish with the largest mean lengths.

Proteocephalus ambloplitr’s in Bluegill

The overall prevalence and mean intensity of P. ambloplitis in bluegill was 44%

39

and 1.8 i 1.9, respectively, in 2000. Only the initial plerocercoid H was found in
bluegill. The mean intensity of P. ambloplitis in female and male fish was 2.2 i 2.4 and
1.3 i: 0.5, respectively. There was no statistical difference between the mean intensity of
P. ambloplitis in female and male fish (Mann-Whitney U-test, U = 70.5, d.f. = 20, P =
0.446). A total of 40 P. ambloplitis was found in bluegill. A significant correlation did
not exist between fish length and number of P. ambloplitis (Spearman’s correlation, r, =
0.584, P = 0.565). The prevalence, mean intensity, and mean abundance of P.
ambloplitis from the two microhabitats of combined female and male fish (Table 11) was
calculated. Only the liver and mesentery were found infected and no statistical difference
in the mean intensity of P. ambloplitis was found between these microhabitats (Mann-
Whitney U-test, U = 38, d.f. = 20, P = 0.900). There was no statistically significant
difference in the mean intensity of P. ambloplitis when compared between rock bass and
bluegill (Mann-Whitney U-test, U = 206, d.f. = 36, P = 0.385). There was no statistically
significant difference in the number of worms when compared between rock bass and

bluegill (x2 = 2.58, d.f. = 1, P > 0.05).

Table 11. The prevalence, mean intensity, mean abundance, and range of
Proteocephalus ambloplitis from 2 microhabitats in bluegill collected in 2000.

Microhabitat Prevalence (%) Mean Intensity i SD Mean Abundance 1: SD Range—

 

Parenteric
Liver 36 1.7 i: 1.6 0.64 :1: 1.3 0 - 8
Mesentery 8 1.5 :1: 0.57 0.12 i 0.43 0 - 2

 

40

DISCUSSION

Esch et al. (1975) suggested that as water temperature rose from 4° C to 7° C in
Gull Lake, parenteric plerocercoids moved from the viscera to the digestive tract of
smallrnouth bass, thus showing a seasonal pattern in movement. In the present study a
seasonal pattern would indicate that in spring (April and May) the worms begin to move
from the viscera into the digestive tract, as summer progresses (June — August) the
prevalence of worms in the digestive tract increases, and as fall (September) approaches
the number of worms in the digestive tract decreases. In the year 2000 the prevalence (P)
of adult and gravid worms in June was (P = 63%), then peaked in July (P = 67%), and
declined in August (P = 23%) with no enteric worms found in September. While these
data generated in the present study do indicate a seasonal pattern, a relationship to water
temperature cannot be made. In 2000 and 2001, the water temperature reached 10° C in
late March before sampling was done.

Esch (1971) reported that the prevalence of adult P. ambloplitis in smallmouth
bass and largemouth bass was 43% and 12%, respectively, from Gull Lake. In the
present study adult and gravid P. ambloplitis were never reported from the digestive tract
of largemouth bass. However, the terminal plerocercoid II was found in the digestive
tract of largemouth bass in the present study. It is believed that these worms would have
developed into adult worms if the fish had not been caught. Similar to what I found,
Esch (1971) did not find adult or gravid P. ambloplitis in the digestive tract of rock bass.
Esch (1971) found plerocercoids in all 4 fish species examined in this study, but did not
give prevalences.

Esch (1971) reported that the prevalence of adult P. ambloplitis was 43% during

41

the summer months. Esch et al. (1975) demonstrated that the prevalence of adult P.
ambloplitis reached a maximum of 50% during the summer. In the present study I report
the prevalence of adult and gravid P. ambloplitis reached a maximum of 51% in the
summer of 2000 (this is the average prevalence for June, July, and August 2000).
Interestingly, the prevalence of adult and gravid P. ambloplitis has decreased in the
largemouth bass to zero. Esch et al. (1975) reported that adult and gravid worms were
never found in smallrnouth bass less than 200 millimeters (mm). Adult and gravid
worms occurred in fish less than 200 mm in the present study. One male fish (181 mm)
from June 2000 had 6 adult worms and 5 gravid worms. Another male fish (175 mm)
from August 2000 harbored 6 gravid worms.

It is not known why largemouth bass have lower mean intensities of P.
ambloplitis compared to smallmouth bass; a possible reason may have to do with where
each fish species spawns. This author speculates that worm recruitment may be highest
during the fishes mating season (April — May), because the two bass species do not mate
in similar habitats. However, this is merely speculation since so few fish were collected
during the actual spawning times for both fish species. Smallmouth bass will nest in
areas of sand, gravel or rubble while largemouth bass usually prefer soft bottoms with
vegetation and other woody debris (Hubbs and Bailey, 193 8). Perhaps, it is during
mating time when smallmouth bass are eating more second intermediate hosts.

Neither rock bass nor bluegill was ever found in the stomachs of smallrnouth and
largemouth bass. The diet of smallrnouth and largemouth bass was comprised primarily
of crayfish, Orconectes propinquus, which was common in the lake (personal

observation). F ingerling basses and minnows were also found in the stomach of the two

42

definitive host species, but much less frequently as crayfish. Since rock bass are ofien
found in weedy, benthic habitats one might expect not to find them too often in the guts
of smallrnouth and largemouth bass. One would expect that open water bluegill would
make up a portion of smallrnouth and largemouth bass diets.

It is not known what proportion of the bass diet is comprised of other centrarchids
in Gull Lake (J arnes Dexter, personal communication). In the present study crayfish
were the primary food item found in the stomach and digestive tract of basses,
comprising approximately 95% of their diet. Since crayfish were abundant in the bass
diet it was speculated that they may be a second intermediate host for P. ambloplitis.
However, cestodes have never been reported as utilizing crayfish or other decapods as a
second intermediate host. Twenty-two crayfish, 0. propinquus, were collected in July
2001 from KBS-l and examined for P. ambloplitis plerocercoids. None of the crayfish
examined were infected with P. ambloplitis. Minnows were also found in the stomachs
of the basses. Likewise, cyprinids have never been reported as a second intermediate
host for P. ambloplitis (Hoffman, 1999 and Amin, 1990). It may be possible that
minnows are involved in the transmission of P. ambloplitis to the bass definitive host.
Fingerling smallrnouth and largemouth bass were also found in the stomachs, but they
were found even less frequently then minnows. Fingerling basses have been shown to be
a potential second intermediate host through cannibalism (Szalai and Dick, 1990).
Further study should be performed to examine what part fingerling bass, minnows, and
crayfish play in the transmission of P. ambloplitis.

The mean intensity and prevalence of P. ambloplitis in smallrnouth and

largemouth bass have been reported from several locations in North America. It would

43

seem that infections of P. ambloplitis vary from each system studied, in regards to which
fish host has higher mean intensities and prevalences. Amin (1990) reported, that of the
22 smallrnouth and 116 largemouth bass examined in Wisconsin, prevalences were 18%
and 43%, respectively. Amin and Cowen (1990) also reported that plerocercoids of P.
ambloplitis in smallrnouth and largemouth bass from Silver Lake, Wisconsin, had
prevalences of 50% and 56%, respectively, and from Tichigan Lake, Wisconsin,
prevalences of zero and 14%, respectively. Similar to the present study, Ingham and
Dronen (1982) and Szalai and Dick (1990), from Texas and Saskatchewan, respectively,
reported only finding plerocercoids of P. ambloplitis in largemouth bass and never any
adult worms. Ingham and Dronen (1982) demonstrated that the prevalence of P.
ambloplitis plerocercoids was as high as 50%. Szalai and Dick (1990) reported the
prevalence of P. ambloplitis plerocercoids was highest (91%) in 2 - 4 year old
largemouth bass. Eure (1976) reported finding adult worms in largemouth bass from
South Carolina with the mean number of worms ranging from 0.5 — 3.0. Not similar to
the present study, Joy and Madan (1989) concluded, based upon the mean intensity of P.
ambloplitis plerocercoids, largemouth bass are the favored host species in Beech Fork
Lake, Wisconsin. The prevalence of P. ambloplitis plerocercoids in the present study for
smallrnouth and largemouth bass was 100% and are the highest reported to date in North
America.

Rock bass and bluegill have been shown in many studies to serve as second
intermediate hosts for P. ambloplitis. Amin (1990) reported that P. ambloplitis was
found to be common in rock bass from Wisconsin, and had prevalences ranging from 12

— 100% in spring, summer and fall. Harley and Keefe (1970) indicated that 11 encysted

P. ambloplitr’s were recovered in 60 bluegill from Kentucky. Cloutman (1975) reported
that the mean abundance of P. ambloplitis ranged from 0.1 — 6.0 in bluegill from
Arkansas. Jilek and Crites (1980) found P. ambloplitis in bluegill from five different
inland lakes from Ohio, and had prevalences ranging from 7.4 — 84.8%. Fischer and
Kelso (1990) showed that P. ambloplitis in bluegill captured from the littoral zone in a
Louisiana Pond had a prevalence and mean intensity (:1: SD) of 20.7% and 4.0 :1: 6.2,
respectively. Amin (1990) reported the prevalence of P. ambloplitis in bluegill from
Wisconsin ranged from 36 — 66% in the spring, smnmer and fall. Wilson et al. (1996)
demonstrated that the prevalence and mean intensity (i SD) of P. ambloplitr’s in bluegill
fiom Holcomb Lake, Michigan, was 83% and 15.3 i 24.5, respectively. The results of
the present study are similar to what other studies have reported in regards to the mean
intensity and prevalence of P. ambloplitis plerocercoids from rock bass and bluegill in
North America.

The fact that smallmouth bass had higher mean intensities of P. ambloplitis in the
ovaries compared to other microhabitats may indicate that this cestode is contributing to a
decline in this fish population from Gull Lake. Female smallrnouth bass harbor more
worms in the ovaries than any other organ when compared to male smallmouth bass and
to male and female largemouth bass. The damage done to the ovaries was often so severe
it was difficult to differentiate an ovary fiom the mass of fibrotic and necrotic tissues that
surrounded and infiltrated it. This gross pathology is consistent with the histopathology
reported by Esch and Huffines (1973 ), and observations made by McCormick and Stokes
(1982). Amin (1990) reported that the unilateral hypertrophy of the ovaries could result

in the destruction of many eggs. In the present study, infected female smallrnouth bass

45

very often (> 60%) exhibited severe unilateral hypertrophy of the ovaries. This usually
was identified by one ovary being 2 - 3 times as large as the other.

The infected ovaries of smallmouth bass were characterized by being white in
color, poorly vascularized, and having the appearance of a deflated balloon; the
uninfected ovaries were much larger, robust, and yellow in color. In contrast, infected
and uninfected ovaries of largemouth bass were similar in appearance, pink and red in
color, highly vascularized, and robust in appearance. The ovaries of smallmouth bass had
the appearance of strands or threads that were made up of the plerocercoids, fibrotic
tissue, and necrotic tissues, thus giving the ovary an appearance likened to a ball of yarn.
This stranded appearance was also described by Bailey (1984) fiom the liver of bluegill.
It is hard for this author to believe that the ovaries could function properly, if at all.
Furthermore, I observed the damage to the gonads worsened as the fish became larger
and older. A significant positive correlation was found between fish length and the
number of P. ambloplitis only in the smallmouth bass. This indicates that as the fish
becomes larger they acquire more worms and this too would cause increased damage to
the gonads. However, not significant, the number of P. ambloplitis decreased as length
increased in largemouth bass. It is not known why there is a trend of decreasing worms
with increasing length in largemouth bass.

The ovaries of smallmouth bass had significantly higher mean intensities of P.
ambloplitis compared to any other visceral organ within the female fish. McCormick and
Stokes (1982) indicated that the nutlient rich yolk of the eggs is often absorbed by the
plerocercoids. Perhaps these plerocercoids are attracted to the ovary because of this

nutrient rich yolk. It is also possible that the ovaries have higher mean intensities of P.

46

ambloplitis because of the large surface area compared to the smaller surface area of the
testes. The ovary becomes very large, especially during the mating season of the fish; it
may be that the large surface area makes the ovaries more susceptible to colonization by
the invading plerocercoids. In female largemouth bass it is not the ovaries that have
higher mean intensities of P. ambloplitis but the liver and mesentery.

The mean intensity of P. ambloplitis in the testes of smallrnouth bass was not
significantly different from those of the liver and mesentery. In fact, the mesentery had
higher mean intensities of P. ambloplitis, although not significant. Within smallrnouth
bass the ovaries harbored more worms than the testes. This demonstrates that if the
reproductive potential of smallrnouth bass is decreasing it may be happening because of
the high mean intensity of P. ambloplitl's in female fish. Esch and Hufiines (1973)
reported the damage caused by P. ambloplitis is usually more severe in young males and
that they may suffer from a decline in sperm producing tissue. Similarly, Esch et al.
(1975) found the most extreme pathology in the testes of young male smallrnouth bass.
Neither of these two studies reported the mean intensity of P. ambloplitis, but is based on
histopathology. It may be possible that even though the mean intensity of P. ambloplitis
is lower in male smallmouth bass than female smallrnouth bass that the pathology caused
by this worm is also severe in males. Male smallrnouth bass have higher worm burdens
than do male largemouth bass. Clearly, this indicates that overall the gonads of the
smallrnouth bass have much higher mean intensities of P. ambloplitis than those of
largemouth bass.

The gonads of largemouth bass had fewer worms than that of the liver and

mesentery. This may indicate that P. ambloplitis is not affecting the reproductive

47

potential of largemouth bass as drastically as it may be in the smallrnouth bass. In both
the female and male largemouth bass it was the other visceral organs that had higher
mean intensities of P. ambloplitis.

Proteocephalus ambloplitis has a significantly higher overall mean intensity in
smallrnouth bass when compared to largemouth bass. This clearly indicates that P.
ambloplitis infections are worse in smallmouth bass. It is also evident that the gonads,
especially the ovaries, of smallmouth bass may be damaged so severely as to impair
proper filnction. Impaired function of the gonads could cause a decline in the
reproductive potential of smallmouth bass and ultimately contribute to their declining

numbers.

48

CONCLUSION

It would seem that smallrnouth bass are experiencing an increase in the mean
intensity of Proteocephalus ambloplitis through the life span of the fish. As the fish ages,
the infections become more severe, with increasing scar tissue formation (fibrous
adhesions and necrotic tissue) and the recurring penetration of worms over time. Several
residents and avid fishermen of Gull Lake were interviewed over the course of this study.
These interviews indicated that a common fishing practice is to only keep fish between
355 — 432 millimeters, and to release the larger fish (> 441 millimeters). If this is a
common fishing practice then this might be contributing to a decrease in smallrnouth bass
numbers. As fish become larger the pathology caused by P. ambloplitis becomes worse.
If the smaller, younger, reproductively viable fish were taken from the breeding stock,
then the larger fish should be present in higher numbers. If these larger fish are rendered
sterile, but still go through spawning behaviors they could be contributing to an overall
decline in the abundance of smallmouth bass from Gull Lake. It is the suggestion of this
author that the larger fish are caught and removed fi-om the breeding population. This
may allow for the smaller fish, which have less severe infections, to spawn and
reproduce.

More research is warranted to investigate if smallmouth bass are producing fewer
offspring than largemouth bass. To test this in a lake system, experiments could be
designed to count the number of smallrnouth bass nesting and quantify the number of
eggs produced and compare these findings to that of largemouth bass. This would give
more support to the hypothesis that smallmouth bass are experiencing a decline in their

numbers due to bass tapeworm interaction.

49

F ingerling bass are known to acquire P. amblopliris by eating infected
zooplankton. It is not known how long the bass tapeworm can persist or survive in the
fish host. Further study should investigate bass tapeworm infections in fingerling bass
and attempt to understand how long worms can survive in fish when the infections are
acquired as fingerlings. Further study should be done to investigate what role, if any,
crayfish play in the transmission of P. ambloplitis. Orconectes propinquus is known to
raid the nests of smallmouth bass and consume the fish eggs. Even though decapods
have never been reported as second intermediate hosts for cestodes a study is still
warranted, based upon the large amount of crayfish that are eaten by smallmouth bass

and largemouth bass.

50

APPENDIX A

51

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8.5

0
came»:

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:9 er

 

 

 

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/00/00/00 000000%u000%00%%00%%000%0%0000
- p1- . lb! 1 ..-|rl.-|l. ll..- e _. o

1m

T:
.3
Tom
imm

 

ion

52

0

(3 ) umuedural

APPENDIX B

53

Table B.1. Number of smallmouth bass examined, mean length, and length range

per month sampled from Gull Lake, Michigan in 2000 and 2001.

 

Month Number Examined Mean Le_ngth (mm) i SD Range (mm)
June 2000 16 224.5 i 42.7 181 — 274
July 2000 12 265 i 56.4 225 - 303
August 2000 13 219.7 i 40.1 166 — 263
September 2000 10 166.2 d: 14.5 137 - 186
May 2001 1 230 230

June 2001 2 257.5 i 10.6 255 - 265

 

54

APPENDIX C

55

Table C. 1. Number of largemouth bass examined, mean length, and length range

per month sampled from Gull Lake, Michigan in 2000 and 2001.

 

Month Number Examined Mean Lenjth (mm) -_1- SD Range (mm)
April 2000 6 239. 3 1 34.6 192 — 280
June 2000 16 191.3 1 20.5 148 — 221
July 2000 7 193.412l.6 160—219
August 2000 15 198.1 1 23.0 155 — 240
September 2000 2 187.5 1 10.6 180 - 195
April 2001 15 275.1130.8 217—315
May 2001 15 209.8 1 29.1 131 — 248

July 2001 12 202.5 :1: 31.7 150 — 248

56

APPENDIX D

57

Table D. 1. Number of rock bass examined, mean length, and length range per

month sampled from Gull Lake, Michigan in 2000.

 

Month Number Examined Mean Length (mm) 1 SD Range (mm)
April 2000 3 164.6 1 8.38 155 - 170
May 2000 4 157.0 1 30.1 123 - 196
June 2000 15 145.6 1 17.8 126 — 197
July 2000 7 165.5 1 20.7 135 — 204
August 2000 15 153.5 111.6 138— 170

September 2000 6 120.8 1 24.8 72 — 141

 

58

APPENDIX E

59

Table E. 1. Number of bluegill examined, mean length, and length range per month

sampled from Gull Lake, Michigan in 2000.

 

Month Number Examined Mean Leigth (mm) 1 SD Range (mm)
May 2000 2 132.0 1 12.7 123 - 141
June 2000 12 116.3 121.7 89— 145
July 2000 12 112.61 14.1 86— 132
August 2000 15 14381191 108— 175

September 2000 9 106.1 1 24.2 68 - 136

 

60

LITERATURE CITED

Amin, O. M. 1990. Cestoda fi'om lake fishes in Wisconsin: The ecology and pathology
of Proteocephalus ambloplitis plerocercoids in their fish intermediate hosts.
Journal of the Helminthological Society of Washington 57:113-119.

------- , and M. Boarini. 1992. Cestoda from lake fishes in Wisconsin: The
morphological identity of plerocercoids of Proteocephalus ambloplitis.
Transactions of the American Microscopical Society 111:193-198.

-------, and M Cowen. 1990. Cestoda from lake fishes in Wisconsin: The ecology of
Proteocephalus ambloplitis and Haplobothrium globuliforme in bass and bowfin.
Journal of the Helminthological Society of Washington 57:120-131.

Anderson, R. C. 1992. Nematode Parasites of Vertebrates Their Development and
Transmission. University Press, Cambridge.

Bailey, W. C. 1984. Epizootiology of Posthodiplostomum minimum (MacCallum) and
Proteocephalus ambloplitis (Leidy) in bluegill (Lepomr's macrochirus
Rafinesque). Canadian Journal of Zoology 62:1363-1366.

Bangham, R. H. 1927. Life history of bass cestode Proteocephalus ambloplitis.
Transactions of the American Fisheries Society 57:206-208.

Becker, C. D., and W. D. Brunson. 1968. The bass tapeworm: A problem in northwest
trout management. The Progressive Fish-Culturist 30:76-83.

Cloutman, D. G. 1975. Parasite community structure of largemouth bass, warmouth, and
bluegill in Lake Fort Smith, Arkansas. Transactions of the American Fisheries
Society 104:277-283.

Cooper, A. R. 1915. Contributions to the life history of Proteocephalus ambloplitis
Leidy, a parasite of black bass. Fascicle 2: 1 77-194.

Dexter, J. L. 1996. Michigan Department of Natural Resources, Gull Lake, Status of
Fishery Resource Report 96-7, Plainwell, 14 pgs.

Esch, G. W. 1971. Impact of ecological succession on the parasite fauna in centrarchids
fi'om oligotrophic and eutrophic ecosystems. American Midland Naturalist
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