Download UNIVERSITY OF WISCONSIN-LA CROSSE Graduate Studies FISH

UNIVERSITY OF WISCONSIN-LA CROSSE
Graduate Studies
FISH HEALTH ASSESMENTS OF GREAT LAKES COREGONIDS
A Manuscript Style Thesis Submitted in Partial Fulfillment of the Requirements for the
Degree of Master of Science in Biology
Christopher M. Olds
College of Science and Health
Aquatic Science Concentration
May, 2012
FISH HEALTH ASSESSMENTS OF GREAT LAKES COREGONIDS
By Christopher M. Olds
We recommend acceptance of this thesis in partial fulfillment of the candidate's
requirements for the degree of Master of Science in Biology (Aquatic Sciences
Concentration)
The candidate has completed the oral defense of the thesis.
A-
r-1;)_
Date
Gregory Sanclt n , Ph.D.
Thesis Committee Co-Chairperson
Roger H ro, P .D.
Thesis Committee Member
( - f--ZVIZ...
Date
.x IJ(..;{. 6 / 2
I
ate
'd.--+ -J.o 12
Date
Thesis Committee Member
Thesis accepted
2
Robert H. Hoar, Ph.D.
Associate Vice Chancellor for Academic Affairs
-"1~ -.?a/~
Date
ABSTRACT
Olds, C. M. Fish health assessments of Great Lakes Coregonids. MS in Biology, May
2012, 70pp. (B. Lasee and G. Sandland)
Health of Great Lakes coregonids is continuously monitored for the spread of pathogens
because of their economic importance. An infectious disease and parasite survey was
conducted to build on previous data collected in the past but to also examine other factors
that may affect distribution of pathogens in Great Lakes lake whitefish, round whitefish, ·
and bloater populations. Coregonids (n=394) were collected from 3-4 regions in Lake
Michigan, Lake Huron and Lake Superior and screened for target pathogens according to
the procedures outlined in the AFS Blue Book Fish Health Section Inspection Manual.
Parasite and age data were collected from a sub-sample (n = 2-30) of each fish species
from each region sampled. No target viral pathogens were detected and one bacterial
pathogen was detected in a lake whitefish from Western Lake Superior. A total of7,404
parasites were recovered representing 12 genera. Prevalence of infection ranged from
50% to 90% in each host species. Results indicate that host age and condition factor do
not appear to influence the presence or absence of parasite communities of coregonids in
the Great Lakes.
iii
ACKNOWLEDMENTS
I would like to thank everyone at the United States Fish and Wildlife Service, La
Crosse Fish Health Center for their patience and time as I learned a new part of the
Region 3 Fisheries Program and for funding my research. Thank you Becky Lasee for
bringing me into your facility and sharing your knowledge and passion for health of the
Great Lakes and its fish species. I have learned so much from my experience with you
and your office.
I would like to thank all of my committee me.mbers: Dr. Becky Lasee, Dr.
Gregory Sandland, Dr. Roger Haro, and Dr. Michael Hoffman for their time and patience
as we worked through this process. Your encouragement and guidance is greatly
appreciated. Thank you for sharing the passion you have in your subject areas and
sharing it with me.
I would like to thank Dr. Gregory Sandland and Dr. Sherwin Toribio for their
patience and time explaining new statistical concepts to me.
I would like to thank all the collecting agencies that took the time to individually
package each fish and get the samples to me quickly. These agencies include: Alpena
FWCO, Michigan Department ofNatural Resources (Marquette and Charlevoix Research
Stations), Ontario Department ofNatural Resources, Chippewa Ottawa Resource
Authority, Mackinaw Fish Company, Wilcox Fish Company, Wisconsin Department of
Natural Resources, United States Geological Survey (Ashland Office).
I would like to thank my friends and family for their guidance, support, and
patience throughout my college career. I want to thank God for giving me the guidance
and direction that I needed as I made big decisions for school and family. Lastly, I would
lV
like to thank my loving wife Jade for all her support and patience throughout my college
career.
v
TABLE OF CONTENTS
PAGE
viii
..............
.
..
LIST OF TABLES ................. ............ . ...... ...... ........... . ..........
LIST OF FIGURES ... ......... .. . ................ .......... ......... .. .... .. ....... . ... . ......... .. .x
LIST OF APPENDICES .... ..... .................... ... .................................. ..... .... xiii
INTRODUCTION ............... ...... .. . .. .............. .... ..... .................................. . 1
Morphology and Habitat Preferences ........ . ..... ... .. . ..... . .. .. .. . .......... .. .... .... 2
Great Lakes Whitefish Status ................. ................... ... .... ................... 3
Great Lakes Bloater Status ............... .......................... ........................ .4
Coregonid Population Management Objectives ....... .... ........... . ................... 4
Great Lakes Viral Pathogens .......... . ..... ...................... ... .. .. . ...... .. ......... 5
Great Lakes Bacterial Pathogens .... ........... : ............. .... ... .. .................... 7
Great Lakes Parasite Fauna .............. . .......... ........... ............................ 8
Large-Scale Fish Parasite Sampling .... . ...... ... ... . ......................... .... :.. ... .. 9
Study Objectives ................ : ............. ..... ..... .............. . .. .. .. ... ... ......... 10
METHODS ......... . ........ .. ............... .... .. .. .... .... ............................ . .......... 11
Site Selection ............ .......... .................... ....... . . ... ..... ............ .... ... .11
Fish Collection .. ............ .............. ............... .......... .. ... ........... ....... 12
Virology ........... ...... ... ............. ...................... ........ ..... .......... ...... 14
Bacteriology .... .......... . .......... ..... ... .... .. .... ........ .. . ........................... 14
Parasitology . .. .... ................ . ..... . .. .. ........ .. ... ...... ... ....... ..... ........... . 15
Statistical Analysis .................. ...................... ...................... . .. ....... 15
Vl
PAGE
RESULTS ......... .. ......................................... . ........................ .. ............. 17
Bacteriology and Virology ...... . .. .. .......................... ........... .. ...... . .... ... 17
Parasitology ........................... ..... . ..... ........ .... .. ............ .... ...... .... ... 17
Lake Whitefish ......................................... . ........ . ............. . ... :22
· Round Whitefish ......... ................ ... ... ..... ....... .. .... . ................. 26
Bloater. ..... .... ..... .. ..... .............. .......... . .... .. . ... .... . .. ... . ........... 31
Parasite abundances between host species .......... ... .............. . .. ...... .36
DISCUSSION .. ............... .. ...... ............................ . . ....... ........................ . 39
REFERENCES .... ......................................... .. ........................ ............... 45
APPENDICES .................... . ............ .... . ...... . .... .. ............... ................ ..... 52
Vll
LIST OF TABLES
PAGE
TABLE
1.
Lake, sampling region, and collection dates of lake whitefish,
round whitefish, and bloater collected from the Upper Great Lakes.
Plus, the number of fish examined for target pathogens and the
number of individuals examined for parasites with the mean length,
weight, and depth of fish sampled from each region ...... ..... .... .. .............. ..... .13
2.
Infection prevalence, mean intensity(± S.D.) and the range of
intensities for parasites found in lake whitefish (Coregonus clupeaformis)
from sampling sites in Lake Superior. ................................... ................ .. 20
3.
Infection prevalence, mean intensity (±S.D.) and range of intensities
for parasites found in lake whitefish from sampling sites in Lake Michigan
and Lake Huron ................ ...... .................. .... .... .. ... ........ ... ...... ..... .. .21
4.
Gender-based estimates of parasites and their abundances of lake whitefish
using the Mann-Whitney U Test for significance ................................. ..... 26
5.
Infection prevalence, mean intensity (± S.D.) and range of intensities
found in round whitefish (Prosopium cylindraceum) from sampling
sites in Lake Superior, Lake Michigan, and Lake Huron ...... ...................... ..28
6.
Gender-based estimates of parasites and their abundances of round whitefish
using the Mann-Whitney U Test for significance ................................. . ....31
7.
Infection prevalence, mean intensity(± S.D.) and range of intensities found
in bloater (Coregonus hoyi) from sampling sites in Lake Michigan and Lake
Superior. ................................. ................................. .................... 33
Vlll
PAGE
TABLE
8.
Gender-based estimates of parasites and their abundances of bloater using
the Mann-Whitney U Test for significance ................. ..... ........... .. .......... 36
lX
LIST OF FIGURES
PAGE
FIGURE
1.
Sampling regions of A. Lake Michigan, B. Lake Huron, and
C. Lake Superior using the Whitefish Management Units established
by the U.S. vs. Michigan Consent Decree. Yellow rectangles
indicating sampling regions within each of the three Great Lakes
sampled ........... .. ............................. ............... .. .. .. . . .... . . ............ . .. 11
2.
Photomicrograph of the posterior end of the nematode
Cystidicolafarionis at 40x magnification. Nematode preserved in
glycerin alcohol. . ... . . .. . ..... . ... ..... . ... .. .... .......... .. .. .... .. ..... ... .. .. . ... ... .... 18
3.
Photomicrograph of the acanthocephalan Acanthocephalus dirus
with a protracted proboscis (Semi chon's acetic-carmine stain) at 1Ox
magnification .. . .. .. .. ... ....... .. . . ....... ..... .. .. .. . ..... ... ... .. .. ........ . .. .. ... ..... . 18
4.
Photomicrograph ofthe cestoda Cyathocephalus truncatus scolex.
(Semichon' s acetic-carmine stain) at 1Ox magnification .... .................. .. ..... . 19
5.
Distribution of the number of parasite taxa infecting lake whitefish in
the Great Lakes ... ... ... .......... .... . . ... .. ....... .. ...... .. . . .. . .. . .. . .. . .... ....... .. ... 23
6.
Mean parasite abundance(± 1 standard error) infecting lake whitefish
in Lake Michigan (LM), Lake Huron (LH), Lake Superior East (LS-E),
West (LS-W), Middle (LS-M), and North (LS-N) sampling regions.
A. All parasite species; B. Cystidicolafarionis;
C. Cyathocephalus truncatus; D. Acanthocephalus dirus ................ .. . .. .. .. .... 24
X
PAGE
FIGURE
7.
Fulton's K (condition factor) of lake whitefish examined
for parasites from all sampling regions in the Great Lakes .................... .. . ....24
8.
Age distribution of lake whitefish sampled from Lakes Michigan,
Huron, and Superior. ............ .. ........... ... .. ............ .. ....... .. . ... .. ..... .. ..... 25
9.
Distribution of the number of parasite taxa infecting round whitefish
in the Great Lakes ............ . ... ... ..... ........ .. ................ .. .......... .......... .. 27
10.
Parasite abundance(± standard error) infecting round whitefish from
Lake Huron (LH), Lake Michigan (LM), and Lake Superior West (LS-W).
A. All parasite species; B. Acanthocephalus dirus; C. Salmincola
thymalli ............. ..... .. .... .. . ..... .. . .. ...... .... ... ... .. ....... ..... .... ... .... ...... .. 29
11.
Mean Fulton's K (condition factor) of round whitefish examined
for parasites from all sampling locations in the Great Lakes .......... .. ............. 30
12.
Age distribution of round whitefish sampled from Lakes Michigan,
Huron and Superior................. .. . .... . .. .. ................................. .......... 30
13.
Distribution of the number of parasite taxa infecting bloater from
Lake Michigan and Lake Superior ..... . .... ...... .............. .. ... ... .... ........... .. 32
14.
Parasite abundance(± 1 standard error) infecting bloater from Lake Michigan
(LM) and Lake Superior North (LS-N) and West (LS-W) sampling regions.
A. All parasite species; B. Cystidicola farionis; C. Acanthocephalus dirus ...... .. 34
15.
Mean Faulton's K (condition factor) of bloater examined for parasites
from Lake Michigan and Lake Superior North and West sampling regions ....... 35
16.
Age distribution of bloater in Lake Superior and Lake Michigan ................... 36
XI
PAGE
FIGURE
17.
Parasite abundance(± 1 standard error) infecting lake whitefish and
bloater of Lake Michigan (LM) and Lake Superior North (LS-N)
and West (LS-W) sampling regions. A. All parasite species;
B. Cystidicolafarionis; C. Acanthocephalus dirus ....................... . ... .. . ....... 37
18.
Parasite abundance (± 1 standard error) infecting lake whitefish and
round whitefish from Lake Huron (LH), Lake Michigan (LM) and
Lake Superior West (LS-W) sampling regions. A. All parasite species;
B. Acanthocephalus dirus ... ... .......... .. ........ . ....... ... ... .. .. . ... . ...... ..... .. ... 38
Xll
LIST OF APPENDICES
PAGE
APPENDIX
A.
List of Target pathogens screened for by fish health methods ............ ....... ... .. 52
B.
Species affected by viral hemoragic septicemia (VHS) federal order ... ... .......... 54
C.
Inner ear bone (Otolith) for ageing before and after being cracked
and burned ...... .. ..... .... .. ... .... ...... ...... ... .... ..... ......... .... .. ...... .. ........ ... 56
Xlll
Introduction
Great Lakes commercial fishing is a multi-million dollar industry, with whitefish
being the primary source of revenue (DeBmyne et al. 2008; Pothoven and Medenjian
2008). Between the 1930s and 1950s, thousands of commercial operations targeted
whitefish and lake trout (Salvelinus namaycush) in Lake Superior (Ebener 2007).
Subsequent reductions in stocks led to fewer fishing operations in the region. Now, there
are fewer than 200 commercial operators remaining (Ebener 2007). Due to reductions in
fishing pressure, whitefish abundance in Lake Superior has increased dramatically over
the past 40 years, but populations are still threatened by new diseases, invasive species,
and environmental change (Ebener 2007; Wagner et al. 201 0).
Fish management agencies in states and provinces surrmmding the Great Lakes are
encouraged to manage each fishery to promote abundant healthy populations (Pothoven
et al. 2006; Wagner et al. 2009). Due to recent changes in fish populations, feeding·
grounds, and spawning habitat, fishery managers have been required to manage each
species differently based on their specific biologies. This has not been an issue for
managing many fish species because much is known about their morphologies,
behaviors, and genetics. However, less is known about whitefish and bloaters
(Coregonidae: Salmonifmmes).
One of the few studies to investigate coregonid stocks found that individual lake
whitefish tend to stay within 16 kilometers of their spawning reef (Smith and Oosten
1940; Dryer 1963). Movement of whitefish within these areas can be food related as they
are generalist benthivores that feed on energy-rich invertebrates such as Diporeia sp.
(Ihssen et al. 1981). Unfortunately, native prey species like Diporeia sp. have declined
in abundance which has con-elated with a decline in the condition and growth of Lake
Huron and Lake Michigan whitefish (Pothoven et al. 2001 ). Because of a decline in
native prey, whitefish health in the Great Lakes is continuously assessed with the goal of
monitoring responses to perturbations from pathogens, parasites, malnutrition,
management actions, and environmental change (Wagner et al. 2009).
The deepwater chub or bloater (Coregonus hoyi) is also a coregonid of concern in
the Great Lakes. Bloaters are the smallest of the coregonids and inhabit deep pelagic
waters (Brown et al. 1985). They are an impmiant ecological link in the Great Lakes
food web where they primarily forage on invetiebrates such as Mysis relicta and
Diporeia sp. (Moeffet 1957). Bloaters also have experienced population reductions in the
Great Lakes. From the late 1800s until the 1950s, the commercial fishing industry
overharvested top predators. Reductions of top predators and increased abundance of
bloaters led the Great Lakes commercial fishetmen to target bloaters to boost their
commercial harvest (Brown et al. 1985; Ebener et al. 2005). Commercial fishing of
bloater was shmi-lived but had a negative impact on the populations.
Morphology and Habitat Preferences
Lake whitefish (Coregonu_s clupeiformis) and round whitefish (Prosopium
cylindraceum) are found near the bottom of lakes at a depth of 15-50 meters. Lake
whitefish are silver in color with a black edging around their scales, whereas the round
whitefish are smaller and have different scale color patterns.
2
Bloaters are a much deeper dwelling fish species that tend to inhabit depths of 60160 meters. Unlike whitefish, bloaters are pelagic and differ morphologically. They
have a terminal mouth, larger eyes, and longer fins proportional to their body size.
Great Lakes Whitefish Status
In lakes Michigan and Huron, harvest limitations facilitated whitefish population
peaks in the early 1990s. Unfortunately, this timing corresponded with the introduction
of invasive mussel species (Pothoven et al. 2001; Bence et al. 2004; Schneeberger et al.
2005). In 1989, zebra mussels (Dreissena polymorpha) were introduced and quickly
established throughout the Great Lakes. A second invasive mollusk, the quagga mussel
(Dreissena bugensis), followed shortly after and established in the deeper waters of the
Great Lakes (Nalepa et al. 2001). After establishment of dreissenid mussels, a decline in
Diporeia sp., the primary nutrient-rich food source for whitefish, was observed (Nalepa
et al. 1998; DeBrunye et al. 2008). Currently Lake Superior has the greatest abundance of
native prey and the lowest abundance of dreissenid mussels. This has maintained healthy
coregonid populations across Lake Superior (Ebener et al. 2004). The decline in growth
and condition of whitefish in lakes Michigan and Huron may have been due in part to
nutritional stress (Ebener et al. 2004). With the absence of an important food source,
whitefish switched prey sources from Diporeia sp. to dreissenid mussels (Pothoven et al.
2008; Tillit et al. 2009). Current research has shown that dreissenid mussels contain high
levels of thiaminase which, when ingested by fish in large numbers, can lead to thiamine
deficiency and affect future offspring. Thiamine deficiency is a lack of vitamin B 1 in fish
eggs and fry and is called early mortality syndrome (EMS). This leads to poor
development and high fry mortality in a number offish species. This condition has been
3
observed in whitefish from both Lakes Michigan and Huron (Pothoven and Nalepa 2006;
Pothoven and Medenjian 2008; Tillitt et al. 2009).
Great Lakes Bloater Status
Commercial fishing has played an important role in supporting the economy of
local ports around the Great Lakes basin, but has led to overfishing of many important
species (Lawrie and Rahrer 1973; Clapp and Horns 2008). Bloater fishing began when
lake trout populations declined during the early 1950s, and commercial fishing shifted
focus to the increasingly abundant bloater populations. The decline oflake trout allowed
bloater growth rates and habitat ranges to increase throughout the region (Smith 1964;
Dryer and Beil1968). Overfishing ofbloaters in the late 1950s and 60s led to the
species' decline. As a result, fisheries agencies in the 1960s had to change their
management strategy from unrestricted commercial fishing to limited harvest for
commercial and recreational fishing (Brown et al. 1999). These actions were designed to
protect small populations of bloaters (and whitefish) throughout the Great Lakes. EMS
has not been identified in Great Lakes bloater populations.
Coregonid Population Management Objectives
The Great Lakes Fishery Commission is an agency formed by members of
academic, state, federal, and tribal fishery agencies of the United States and Canada. It is
designed to protect the Great Lakes and eradicate the sea lamprey. The commission has
distinct lake committees for each ofthe Great Lakes (e.g., Lake Michigan Committee)
that create management objectives for the fish communities within that lake.
Management objectives addressing bloater and whitefish species have been created for
Lake Michigan, Lake Huron, and Lake Superior.
4
Management objectives for all coregonids include maintaining present coregonid
populations while restoring certain threatened or endangered species. Maintaining selfsustaining stocks of lake whitefish, round whitefish, and bloater for commercial harvest is
also goal of the commission (Busiahn 1990; DesJardine et al. 1995; Eshenroder et al.
1995). Managing important fish species is a difficult task when current populations face
many challenges. Rehabilitation of native planktivores through stocking by fish
hatcheries is one example of how to increase the biological integrity and diversity of
planktivore populations (Busiahn 1990; DesJardine et al. 1995; Eshenroder et al. 1995).
This approach has recently been combined with modeling to enhance restocking success.
For example, Zimmerman and Krueger (2009) created a conceptual model on how to reestablish native deepwater fish communities. The model uses an ecosystem approach
that incorporated exotic species, parasites, environmental changes and challenges, to reestablishing extirpated or depleted stocks of deepwater fish species. The model
examined the individual life cycle within the context of the population, metapopulation,
community, and ecosystem level processes of coregonids.
In addition to overfishing and diet-related factors, micro- and macroparasites may
also influence coregonid populations in the Great Lakes. Parasites can influence the
foraging ability, spawning success, and predator avoidance oftheir host. Factors
influencing parasite communities that establish within these species are fish habitat,
range, food preference, gender, size, and age (Wagner et al. 2010).
Great Lakes Viral Pathogens
Viral pathogens have been shown to cause large die offs of fish in water bodies
around the world. In the Great Lakes, the loss of important commercial fish species to a
5
viral pathogen could be devastating to local economies. Viral pathogens of recent
concern to Great Lakes biologist include Viral Hemorrhagic Septicemia (VHSv), Spring
Viremia of Carp Virus (SVCV), and Largemouth Bass Virus (LMBV). These viruses
have been detected within the Great Lakes basin and have been associated with fish kills
(G-rizzle and Brunner 2003; Elsayed et al. 2006; Goodwin 2011). SVCV and LMBV both
tend to infect a narrow range of hosts (Grizzle and Brunner 2003; Goodwin 2011)
whereas VHSV has broad host specificity (Grizzle and Brunner 2003). Viral
Hemorrhagic Septicemia (VHS) was originally reported to cause high mortality rates in
rainbow trout (Oncorhyncus mykiss) and other salmonids in Europe (Elsayed et al. 2006;
Bergmann and Fichtner 2008). The first outbreak in the Great Lakes was recorded in
muskellunge (Esox musquinongy) in southern Lake St. Clair in 2003, but was not
identified as VHS until2005. Since then, it has been identified in 28 different fish
species and has caused large fish kills around the Great Lakes region (Appendix B). It is
unknown how VHS was introduced into the Great Lakes or how long it has been present.
The genotype of VHS found in the Great Lakes is VHS IVb has been shown to be a
different genotype than those from other parts of the country, such as the West Coast
strain of VHS IVa that infects marine fish species (Hope et al. 201 0). Fish infected with
VHS may appear to be normal or may exhibit some external clinical signs of disease such
as bulging eyes, bloated abdomens, inactive or over active behavior, and hemorrhages in
the eyes, skin, gills, and at the base of the fins (http://www.aphis.usda.gov/animal_healthl
emergingissues/downloads/vhsgreatlakes.pdf). Some fish will have lesions that can
resemble other viral pathogens, which makes it important to test the fish to confirm the
presence ofVHS. Recently, VHS has been confirmed in lake whitefish in the Great
6
Lakes (http://www.aphis.usda.gov/animal_healthlemergingissues/
downloads/vhsgreatlakes.pdf). Due to the importance oflake whitefish for commercial
fishing it is necessary to monitor the spread ofVHSV to other species and regions.
Great Lakes Bacterial Pathogens
Bacterial Kidney Disease (BKD) is a serious, and often fatal, disease among wild
and hatchery reared salmonids worldwide (Fryer and Sanders 1981 ). BKD is caused by
infections of Renibacterium salmoninarum, which appear to become virulent when fish
are stressed or experience a drastic environmental change. Renibacterium salmoninarum
has been found in whitefish and bloaters from Lakes Michigan and Huron by serological
and molecular assays (Jonas et al. 2002; Faisal et al. 2010a). Feeding and swimming
behaviors of infected juveniles may become erratic, making them more susceptible to
predation (Mesa et al. 1998). Infected adults may lack clinical signs ofthe disease and
may feed and behave normally. Over time, destruction of kidney tissue by the bacteria
leads to mortality in these adults. Recent research has shown a higher prevalence of
BKD in coregonids sampled from the Great Lakes in 2009 compared to previous
sampling (Faisal et al. 2010a).
Faisal et al. (2010a) sampled 1,284lake whitefish in northern Lakes Huron and
Michigan over a three-year period; 62.31% of the whitefish tested positive for R.
salmoninarum. The high prevalence of BKD may indicate that the fish are stressed which
could result in lower reproductive success (Ebener et al. 2004). BKD is less prevalent in
Lake Superior compared to Lakes Michigan and Huron (Faisal et al 201 Oa).
Another group of bacterial pathogens that causes fish disease are the motile
Aeromonas species. Motile aeromonad species cause Motile Aeromonad Septicemia
7
(MAS). MAS can cause an aiTay of disease signs in fish such as lesions, gastroenteritis,
and extra-intestinal infections. MAS often is associated with stressors such as spawning,
handling, temperature fluctuations, and poor nutrition (Austin and Adams 1996; Aoki
1999). MAS could pose problems to a fish population that is already experiencing a
decline in growth and condition (Pothoven et al. 2001). Loch and Faisal (2010) sampled
443 lake whitefish from Lakes Huron and Michigan over a 11 month span and 63 tested
positive for Aeromonas species. MAS is significant because of the economic losses it has
caused in salmonids worldwide (Austin and Austin 2007).
Many of the salmonids introduced into the Great Lakes are known to be infected
with A. salmonicida (Cipriano and Bullock 2001) and they may serve as a source of
infection for lake whitefish. In addition, Wagner et al. (2009) reported that bacterial
infections might be a secondary infection caused by the swim bladder nematode
Cystidicolafarionis (Wagner et al. 2009; Faisal et al2010a).
Great Lakes Parasite Fauna
Coregonids are distributed throughout North America with species overlap among
lakes (Hanzelova and Scholz 1999; Baldwin and Goater 2003). In inter-connected lakes
of Alberta, Canada, lake whitefish were shown to have higher parasite diversity than any
other fish species sampled (Baldwin and Goater 2003). Karvonen and Valtonen (2004)
examined parasite similarities in whitefish of interconnected lakes in Finland and found
whitefish to have similiar parasite species across lakes. However, in the Great Lakes
little is known about the parasite communities of coregonids. Understanding parasite
species overlap among these hosts could allow researchers to also understand the spread
of secondary bacterial and/or viral pathogens. Cystidicola farionis is one parasite species
8
that has been documented to overlap in many coregonids found in Lakes Michigan,
Huron, and Superior (Sutherland et al. 1985; Faisal et al. 2010b).
Distribution of parasites across fish species and bodies of water can be altered
with the introduction of exotic species (Matitsky et al. 201 0). An invasive parasite
species introduced into the United States is the Asian fish tapeworm (Bothriocephalus
acheilognathi). It was most likely brought into North America in 1975 with the
importation of Asian carp species (Hoffman 1999). To date, it has been reported in the
Great Lakes region but not in any coregonid species in the Great Lakes.
Large-Scale Fish Parasite Sampling
Historically, fish parasite surveys have only examined one host species from one
sampling location or a single body of water. Few studies have assessed multiple species
from different sites (Muzzall1995). In rare instances where multiple sites and lakes were
taken into account, sampling was not consistent across lakes or season, and focused on
specific parasite taxa (Bangham 1955, Muzzall et al. 1995). For example, Karvonen and
Valtonen (2004) examined the influence of geographical separation on helminth
infections of whitefish in Finland, but only examined one parasite. Cone et al. (2004)
assessed spatial dynamics of parasites in spottail shiner (Notropis hudsonius) from the
Great Lakes, but studied the myxozoan fauna.
There is a need for large multi-lake, site, and host species assessments to fill in
the information gap for parasite distributions across multiple species within the Great
Lakes (Brenden et al. 2010). This information would not only be useful for monitoring
parasite distribution over time, but also to monitor parasite community changes across
species of fish.
9
Study Objectives
Research examining and comparing the parasite community structure of multiple
fish species across multiple areas of each upper Great Lake (Lake Michigan, Lake Huron,
Lake Superior) are lacking. Specifically, there has been little or no comparative work on
the parasite-communit{' structure of whitefish and bloater populations. The four main
objectives of this study are to: 1) screen for viral or bacterial pathogens that may be
present in coregonids (lake whitefish, round whitefish and bloaters); 2) examine and
compare the parasite communities from coregonids in Lake Michigan, Lake Huron, and
Lake Superior; 3) determine differences in parasite community structure among fish
species, sampling sites and lakes; and 4) investigate the influence of age and gender on
parasite abundance and composition. Lake whitefish from Lake Superior would probably
have the greatest diversity of parasites because their native prey is more abundant than
Lakes Michigan and Huron. Furthermore, I predicted that fish from Lake Michigan and
Lake Huron would have similar parasite communities due to declining prey abundance
and close proximity of sampled spawning reefs. My research findings can be used as a
tool for future comparisons of coregonid parasite communities that aid in identifying
spatial and temporal differences.
10
Methods
Site Selection
Collection sites were selected using the Whitefish Management Units (Figure 1)
from the U.S. vs. Michigan Consent Decree of 1836. Based on this document, Lake
Michigan was separated into northern, middle and southern sampling regions (Figure 1a).
Lake Huron was divided into a northern and middle sampling region (Figure 1b), and
Lake Superior divided into four sampling regions (western, middle, eastern, and northern
zones) (Figure 1c).
+_..
..._
. .... _..-=i _ _ _
....... _.__..,_
....,
FIGURE 1. Sampling regions of A. Lake Michigan, B. Lake Huron, and C. Lake
Superior. Regions were determined using the Whitefish Management Units established
by the U.S. vs. Michigan Consent Decree. Yellow rectangles indicate sampling regions
within each of the three Great Lakes sampled.
11
Fish Collection
Up to 60 whitefish and bloaters were collected from each of the 9 sites by
trawling, gill netting, and/or trap netting from late July to late November 2009 (Table 1).
Collections were made with assistance from the United States Fish and Wildlife Service,
United States Geological Service, Michigan Department ofNatural Resources, Wisconsin
Department ofNatural Resources, Chippewa Ottawa Resource Authority, and Ontario
Ministry ofNatural Resources. All fish were held on ice until processing, and when
possible, fi~h were examined within 48 h of collection to prevent breakdown of parasites
and reductions of viral titers. In the laboratory, each fish was measured for total length
(rnrn), weighed (g), and then opened with a longitudinal incision along the abdomen to
note gender and maturity. After the initial incision, the viral and bacterial samples were
acquired as noted below.
12
TABLE 1. Lake, sampling region, and collection dates of lake whitefish, round whitefish, and bloater collected from the Upper Great
Lakes. Plus, the number offish examined for target pathogens and the number of individuals examined for parasites with the mean
length, weight, and depth of fish sampled from each region.
Depth(m)
Mean Weight (g .±SD)
Mean Length (mm .±SD)
No. of Fish Examined for
Date Collected
Location
Target Pathogens
Lake Whitefish
Lake Michigan
North
Middle
Lake Huron
North
Lake Superior
North
West
Middle
East
Parasites
-
October 2009
November 2009
20
31
0
31
479.4 ±36.2
514.9 ±35.5
1463.1 ±317.5
60-100
50-100
October 2009
40
30
487.3 ±18.5
1015.4 ±134.3
80-100
November 2009
July 2009
August 2009
October 2009
9
35
32
36
9
21
32
30
388.8 ±74.3
385.1 ±123.2
381.5 ±184.7
520.8 ±44.7
558.9 ±329.4
677.5 ±482.9
516.3 ±330.8
1319.3 ±368.3
50-100
50-100
105-200
60-100
August 2009
23
23
434.0 ±20.5
905.0 ±176.4
60-100
August 2009
32
32
387.8 ±34.7
483.3 ±144.7
100
July 2009
August 2009
17
2
17
2
246.7 ±150.3
354.5 ±17.7
263.2 ±280.7
342.5 ±88.4
20-50
115-200
November 2009
60
30
249.1 ±23.0
164.3 ±41.1
288-318·
November 2009
July 2009
Totals
30
27
30
22
212.3 ±16.7
228.0 ±45.5
96.2 .±22.5
80.8 ±48.4
250-300
100-200
394
309
~
w
Round Whitefish
Lake Michigan
Middle
Lake Huron
Middle
Lake Superior
West
Middle
Bloater
Lake Michigan
South
Lake Superior
North
West
Virology
Virology assays were conducted on individual fish or pooled samples of up to five
fish. Approximately 0.2 g ofkidney and spleen tissues was removed and diluted 1:10 in
Hank's Balanced Salt Solution (HBSS). Samples were homogenized with a stomacher
(Stomacher 80 Biomaster-Seward) and centrifuged at 2,800 rpm for 5 minutes at a
temperature of 4°C. Once centrifuged, samples were diluted 1:1 (1ml of sample to 1ml
HBSS) and incubated at either 4°C overnight or at 15°C for 2 hours, and centrifuged at
2,800 rpm for 5 minutes to pellet any large material left in the sample. Duplicate wells of
Bluegill Fry Cells (BF -2), Epithelioma Papulosum Cyprini (EPC), and Chinook Salmon
Embryo cells (CHSE) in 24-well cell culture plates were inoculated with 0.2 ml of
sample per well. The EPC and BF -2 are acceptable cell lines that facilitate growth of
such vimses such as VHSV and SVCV (USFWS and AFS-FHS 2010; Hope et al. 2011).
The CHSE cell line facilitates growth of vimses such as Infectious Pancreatic Necrosis
(IPNV) and VHSV. The inoculated EPC and CHSE cell lines were incubated at 15°C
and BF-2 cells at 30°C for 14 days. Culture plates were examined twice per week for
cytopathic effect (CPE) caused by target pathogens (Appendix A) (USFWS and AFSFHS 2010).
Bacteriology
The kidney of each whitefish and bloater was stabbed with a 1 ~1 sterile
disposable loop and inoculated onto a brain-herui infusion agar (BHIA) slant tube. The
samples were then incubated for 5 to 7 days at 20°C. After incubation, bacteria was
removed from the original tube and streaked onto a BHIA plate to isolate individual
bacterial colonies. Isolated colonies were then identified following the procedures
14
outlined in the USFWS and AFS-FHS (2010). Kidney tissue samples were also collected
for Enzyme-linked Immunosorbent Assay (ELISA) analysis for the presence of
Renibacterium salmoninarum following the sampling protocol outlined in the National
Wild Fish Health Survey Laboratory Procedures Manual
(http://www.fws.gov/wildfishsurvey/manuall NWFHS _Lab_ Manual_5.0_ Editiqn.pdf).
Parasitology
When possible, fish were examined immediately after collection. However, when
this was not possible, fish were flash frozen by pouring super cooled ethanol (-80°C) over
the whole fish and stored in a freezer (-20°C) for later necropsy. Whitefish and bloaters
were examined for external and internal parasites using a stereomicroscope. Parasites
were removed from the fins, gills, stomach, gastro-intestinal tract, pyloric caecae, eyes,
and swim bladder. Nematodes and copepods were preserved in glycerin alcohol for later
identification. All other parasites were stored in Alcohol-fonnol-acetic Fixative (AF A).
Staining and identification of parasites was completed by following the steps outlined by
Daily (1996), Hoffman (1999) and Beverly-Burton (1984). While performing the
necropsies, the otoliths were removed and stored in a coin envelope. Otoliths were aged
using the crack and bum method (Claramunt 2005). Using the otolith for aging has been
proven to be more accurate than using other hard structures such as fin rays and scales
(Isermann et al. 2003).
Statistical Analysis
For all three fish species, parasite prevalence (number of infected fish/ number
examined x 100), mean intensity (average number of parasites/ number of infected fish),
range (minimum-maximum), and mean abundance (average number of parasites/ all hosts
15
examined) were calculated across all three lakes (Margolis et al. 1982). SPSS (Statistical
Package for Social Sciences) software was used for statistical analysis of parasite data
using non-parametric tests. The Mann-Whitney U test was used to test gender
differences and parasite abundance difference between two sites. Pearsons Correlation
Coefficient was used to examine the relationship between age and parasite abundance
across fish hosts. Lastly, the Kruskal-Wallis Tests were used to compare fish from
multiple sites and to compare multiple fish and parasite species at a single time point.
All tests were run using an alpha of 0.05 and results were considered significant at P <
0.05.
16
Results
Bacteriology and Virology
No target viral pathogens were detected in the 394 whitefish and bloaters
examined from Lake Michigan, Lake Huron, and Lake Superior. Only one sample tested
positive for Renibacterium salmoninarum in western Lake Superior. Target bacterial
pathogens were not detected in any other samples from any of the lakes sampled.
Parasitology
Of the 309 fish examined for parasites, 7,404 parasites were recovered,
representing 11 genera. Parasites collected represented the following taxa: Crustacea
(Sa/mineola sp.), Monogenea (Discocotyle sagittata), Digenea (Diplostomum
spathaceum), Nematoda (Cystidicolafarionis (Figure 2) Acanthocephala
(Metechinorhynchus sp., Neochinorhynchus sp., Acanthocephalus dirus (Fig. 3), Cestoda
(Cyathocephalus truncatus (Figure 4), larval and adult Eubothrium salvelini, and
Proteocephalus exiguus), Myxozoa (Henneguya zschokkei) (Tables 2,3,5,7). None ofthe
parasites identified were considered invasive species.
17
FIGURE 2. Photomicrograph ofthe posterior end of the nematode Cystidicolafarionis.
Nematode preserved in glycerin alcohol.
FIGURE 3. Photomicrograph ofthe acanthocephalanAcanthocephalus dirus with a
protracted proboscis (Semichon's acetic-carmine stain).
18
FIGURE 4. Photomicrograph of the cestode Cyathocephalus truncatus scolex.
(Semichon's acetic-carmine stain).
19
TABLE 2. Infection prevalence(%), mean intensity(± S.D.) and the range of intensities for parasites found in lake whitefish
(Coregon.us clupeaformis) from sampling sites in Lake Supe1ior.
N
0
Parasite
Protozoa
Henneguya sp.
Mongenea
Disc:ocotyle sagittata
Digenea
Diplostomum spathacewn
Cestoda
Cyathocephalus truncatus
Eubothrium salvelini
Proteocephalus exiguus
Proteocephalus sp."
Acanthocephala
Acanthocephalus dirus
Metechinorhynchus salmonis
Neochinorhynchus
tumidus
salmon is
rutlii
Nematoda
Cystidicola farionis
North (n=9)
West (n=21)
Middle (n=32)
East (n=30)
31.3,3 ±.2.1 (1-9)
30.0,2.7 ±.1.4 (1-7)
3.1,4 ±.0.7 (1-4)
30.0,2.3 ±.1.2 (1-6)
62.5, - b(3-tntc)
3.1,8 ±._undc (8)
56.3,14.1 ±.)2.5(1-50)
10.0,9.5 ±.4.9 (1-29)
4. 76,8±. undc (8)
11.1, 1 ±.undc (1)
9.5,4 ±.undc (4)
44.4,120.3 ±134.0 (4-408) 14.3,6.7 ±2.8 (3-12)
9.5,2 ±. undc (2)
55.6,7.6 ±.8.2 (6-25)
100,12.2 ±.11.2 (2-35)
44.4,21.8 ±16.8 (4-41)
33.3,10 ±.6.1 (4-18)
4.8,2 ±.0.4 (1-2)
4.8,1 ±.und' (1)
9 .5,4 ±.1.5 ( 1-7)
4.8,6 ±. undc (6)
4.8,3 8 ±. undc (3 8)
" Larval parasite
n Could not be determined because parasites were too numerous to count (tntc ).
37.5,18.3 ±.21.0 (2-115)
25.0,5.25 ±.3.0 (3-13)
22 .2,36.3 ±.6.6 (1-27)
8.3, - b(l-tntc)
44.4,23.6±.19.0 (1-80)
15.6,7.6 ±.3.4 (2-13)
3.0,3 ±.0.6 (2-3)
3 .1, 118 ±. undc ( 118)
33.3,2.5 ±.1.6 (1-6)
~ Mathematical operation cannot be defined. (und =undefined)
TABLE 3. Infection prevalence(%), mean intensity (±S.D.) and range of intensities for parasites found in lake whitefish from
sampling sites in Lake Michigan and Lake Huron.
Parasite
Digenea
Diplostomum spathaceum
Lake Michigan (n=31)
Lake Huron (n=30)
22.6,1.4 ±0.7 (1-3)
10.0,2.5 ±0.7 (1-4)
9.7,10 ±3.7 (5-20)
29.0,- "(1-tntc)
12.5,111.2 .±57.6 (39-306)
85.0,13.6 .±14.8 (1-70)
5.0,70 ±11.1 (2-70)
25.8,1.9 +1.0 (1-4)
70.0,18.1_±19 (1-95)
b
5.0,1 + und (1)
b
15.0,2 ±und (2)
Cestoda
N
Cyathocephalus truncatus
Proteocephalus exiguus
Proteocephalus .sp.
Acanthocephala
Acanthocepha/us dirus
Metechinorhynchus salmonis
Neoch inorhynchus tumidus
Nematoda
22.6,2 +1.2 (1-6)
"Could not be determined because parasites were too numerous to count (tntc)
b Mathematical operation cannot be defined. (und =undefined)
Cystidicolafarionis
40.0,7.2 ±6.7 (1-39)
Lake Whitefish.- Lake whitefish were infected with 0-6 parasite species, with 72%
offish being infected with at least one parasite species across all lakes (Fig. 5).
Cystidicolafarionis, A. dirus, C. truncatus, and P. exiguus were the more common
parasite species recovered. Lake Superior had >75% offish infected with one or more
parasite species. Whereas, Lake Michigan and Lake Huron had < 70% of fish infected
with one or more parasite species. Common parasite species such as C. farionis had a
mean prevalence of 22%, with a mean intensity of 8.5 parasites/fish and a range of 0-118
parasites across Lake Superior (Fig. 2). Lake Superior-East had the highest prevalence
of C. farionis (33%), whereas Lake Superior-Middle had the lowest prevalence (3.1 %)
(Table 2). Lake Huron C. farionis prevalence ( 40%) was much greater than Lake
Michigan C. farionis (22.6%) (Table 3).
A second common parasite, Acanthocephalus dirus had a mean prevalence of36%,
with a mean intensity of 16.7 parasites per fish and a range of 1-115. In Lake SuperiorNorth A. dirus had a prevalence of 100%, which is more than double the second highest
prevalence found in Lake Superior-East (44.4%) (Table 2). Prevalence ofLake Huron A.
dirus was 70.0%, which is greater than Lake Michigan at 25.8% (Table 3).
Cyathocepalus truncatus had the highest prevalence (62.5%) in Lake Superior-Middle
(Tables 2). Lake Michigan had the lowest prevalence of C. truncatus (9.7%).
22
18
ISJLake Huron
16
D Lake Michigan
12 Lake Superior-North
14
12
.....=
~
~
II-<
10
Q
8
z
6
4
2
0
.
• Lake Superior-East
~
~
~~
0
raLake Superior-Middle
~
~
rl}
DLake Superior-West
§
~
~
~
~
~
~~
~
~
~
~
~
~
§
~
~
~
~
0
~
n
~
2
l
~
~~
3
~
~
=
~
~
~
~ ~~
~
~~
==
~
4
§
~~
5
~~
6
No. of Parasite Species
FIGURE 5. Distribution ofthe number of parasite species infecting lake whitefish in the
Great Lakes.
Total parasite abundance in lake whitefish was significantly different in Lake
Superior, Lake Michigan and Lake Huron (Kruskal-Wallis Test, df=2, p = 0.001) (Fig.
6a). Of the parasites recovered from lake whitefish, only P. exiguus had the same
distribution across the three lakes sampled. The dominant parasite species C. farionis, C.
truncatus, and A. dirus differed significantly in abundance among lakes (All KruskalWallis Test, df= 2, p < 0.001) (Fig. 6b,c,d). Cystidicolafarionis had the lowest mean
abundance in Lake Michigan fish and Lake Huron had the highest overall abundance
(Fig. 6b). Cyathocephalus truncatus had the greatest abundance in Lake Superior, while
Lake Michigan had the lowest abundance (Fig. 6c ). Lake Superior and Lake Huron had
similar abundances of A. dirus while Lake Michigan had the lowest abundance (Fig. 6d).
The condition factor of lake whitefish, which could be influenced by parasite infection
23
was also compared across the three lakes and was not significantly different (KruskalWallis Test, df= 2, p > 0.05) (Fig. 7).
50
45
40
·~
"'a
4.,
'0
ci
z
.,"'c
::E
4
B
3.5
3
35
30
25
20
2.5
2
1.5
IS
10
5
0.5
0
0
70
12
c
D
60
10
50
8
40
6
JO
4
20
2
10
0
0
LM
LII
LII
LS
LM
LS
FIGURE 6. Mean parasite abundance(± 1 standard error) infecting lake whitefish in
Lake Huron (LH), Lake Michigan (LM), and Lake Superior (LS) sampling regions. A.
All parasite species; B. Cystidicolafarionis; C. Cyathocephalus truncatus; D.
Acanthocephalus dirus.
L2
::..::
""
·~::
0.8
Q
;::
:I
011
'"1:011"'
..
0.6
0.4
:E
0.2
0
Lll
LM
LS
FIGURE 7. Fulton's K (condition factor) oflake whitefish examined for parasites from
all Lakes.
24
Whitefish movement has been documented to be within 40 miles of spawning
reefs (Dryer 1963). The two sampling regions, Lake Superior-East and Lake Huron are
within that range. Total parasite abundance of lake whitefish between the sampling
regions was not significantly different (Mann-Whitney U Test, df= 1, p = 0.37).
However, individual parasite abundance of C. farionis between Lake Huron and Lake
Superior-East was significantly different (Mann-Whitney U Test, df= 1, p = 0.048).
Lake whitefish ranged in age from 2 to 31 years across lakes (Fig. 8). Lake
whitefish parasite abundance had no correlation with age
fo~
any parasite species
identified (Pearson Correlation Coefficient, r < 0.25). Parasite abundance was examined
in relation to host age at different sampling points in Lake Superior because a sufficient
range offish sizes were collected (and they represented the necessary year classes).
There was no correlation between host age and parasite abundance for the North, Middle
and East sampling regions of Lake Superior (Pearson Correlation Coefficient, r < 0.30).
There was a weak negative relationship for parasite abundance and host age from Lake
Superior-West (Pearson Correlation Coefficient, r = -0.603).
10
9
....-=
<ll
~
._
8
7
-
6
5
=
0 4
z
3
2
I
0
-
I'
I
II
-.-
I
0 1 2 3 4 56 7 8 9101112131415161718192 0212223242526272829303 1
Age (years)
FIGURE 8. Age distribution of lake whitefish sampled from Lakes Michigan, Huron, and
Superior.
25
Lake whitefish pooled across all lakes showed no significant difference in overall
parasite abundance between host sexes (Table 4). Abundance of C. farionis was
significantly lower in male than in female lake whitefish. Abundance of C. truncatus was
also significantly different between sexes of lake whitefish. Males had a higher
abundance of C. truncatus than females. Acanthocephalus dirus and P. exiguus had
similar parasite abundances between sexes of lake whitefish pooled across all lakes.
Lake Huron samples only included females, therefore a comparison between male and
female fish was not possible.
TABLE 4. Gender-based estimates of parasites and their abundances oflake whitefish using Lhe
_Mann-Whitney U Test for significance.
Abundance
Sample Size
Parasite Species
Male/Female
Male (±SD)
Female (±SD)
p-value
0.396
All Parasites
68/89
31.5 (±3.2)
21.8 (+80.5)
Cystidicola farionis
68/89
0.2 (±0.8)
1.6 (±4.7)
Cyathocephalus truncatus
68/89
40.3 (±29.3)
Acanthocephauls dirus
68/89
7.6 (±1.5)
9.4 (±0.3)
0.979
Proteocephauls exiguus
68/89
4.5 (±7.9)
4.1 (±22.7)
0.258
10.8 (±57.1)
<0.001
0.003
Round Whitefish.- The number of parasite species infecting round whitefish from
Lakes Michigan, Huron and Superior ranged from 0 to 3, with >50% of the hosts infected
with at least one parasite species (Fig. 9). The most common parasite species was the
acanthocephalan, A. dirus. Round whitefish from Lake Superior had an 11% infection
rate of at least one parasite species, whereas 60% of round whitefish from Lake Michigan
26
and 59% of Lake Huron round whitefish were infected with at least one parasite (Table
5).
20
•Lake Huron
DLake Michigan
u Lake Superior-West
IR
16
14
-=
.~
""'~
z0
12
10
8
6
4
2
0
2
0
3
No. of Parasite Species
FIGURE 9. Distribution of the number of parasite species infecting round whitefish in the
Great Lakes.
27
TABLE 5. Infection prevalence(%), mean intensity(± S.D.) and range of intensities found in round whitefish (Prosopium
cylindraceum) from sampling sites in Lake Superior, Lake Michigan, and Lake Huron.
N
00
Lake Michigan (n=23)
Parasite
Protozoa
Henneguya sp.
Digenea
13 .0,5.3 ±2.1 (2-9)
Diplostomum spathaceum
Cestoda
34.8,3.8 ±2.5 (1-10)
Eubothrium salvelini
Proteocephalus exiguus
Acanthocephala
52.2,1.3 ±0.8 (1-3)
Acanthocephalus dints
Crustacea
Sa/mineola thymalli
" Mathematical operation cannot be defined. (und =undefined)
Lake Huron (n=32)
Lake Superior
West (n=17)
Middle (n=2)
5.9,8.0±. und"(8)
18.8,0.3 ±4.3 (10-18)
3.1,0.1 ±. und" (3)
3.1,0.01 ±und" (1)
11.8,2.5 ± und" (4)
50.0,5.0 ± unda (5)
34.4,0.2 ±4.2 (1-22)
5.9,2.0 ± unda (2)
50.0,13 ±und" (13)
Overall parasite abundance was not significantly different among round whitefish
from Lake Michigan, Lake Huron and Lake Superior (Kruskal-Wallis Test, df= 2, p =
0.055) (Fig. lOa). However, the abundances of more common parasite species including
A. dirus and S. thymalli were significantly different between lakes (All Kruskal-Wallis
Test, df= 2, p < 0.004) (Fig. lOb,c). Lake Michigan round whitefish had the highest
abundance of A. dirus, whereas Lake Huron had the lowest value (Fig. 1Ob). However,
the greatest abundance of S. thymalli was found in fish in Lake Huron whereas fish from
Lake Michigan where not infected by this parasite (Fig. 1Oc). The condition factor of
round whitefish sampled was not significantly different between lakes (Kruskal-Wallis
Test, df= 2, p = 0.354) (Fig. 11)
5
4.5
4
3.5
3
2.5
2
1.5
·~.,
a
c..
'0
0
;z_
c:
"'
~
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0. 1
0
I
0.5
0
LH
LM
LS-W
2.5
B
LH
LM
LS-W
~c-----------.,
2
1.5
0.5
0
LH
LM
LS-W
FIGURE 10. Parasite abundance (± standard error) infecting round whitefish from Lake
Huron (LH), Lake Michigan (LM), and Lake Superior West (LS-W). A. All parasite
species; B. Acanthocephalus dirus; C. Sa/mineola thymalli.
29
1.4
l.2
~
~"'
.s=0.8
';
~
=0.6
~
~
~ 0.4
0.2
0
LS-W
LM
LH
FIGURE 11. Mean Fulton's K (condition factor) (±1 standard error) of round whitefish
examined for parasites from all sampling locations in the Great Lakes.
Round whitefish ranged in age from 1 to 19 years (Fig. 12). Round whitefish
parasite abundance was not correlated with host age using total parasite abundance, or
correlated with any parasite species (all Pearson Correlation Coefficients, r < 0.20).
16
14
12
..r:l
"'
ii:
....
10
0
8
c
z;
6
4
..II I
2
0
I
0
2
3
4
5
6
7
8
9
I0
II
12
13
14 15
F
I
16
*"i
17
18
19 20
Age (years)
FIGURE 12. Age distribution of round whitefish sampled from Lakes Michigan, Huron
and Superior.
Total parasite abundance was not significantly different between sexes of round
whitefish across all lakes (Table 6). There was no significant difference in total parasite
abundance between male and female round whitefish from either Lake Huron or Lake
30
Superior (Table 6). However, male and female fish from Lake Michigan did show a
significant difference in total parasite abundance. However, female round whitefish had a
greater parasite abundance than male round whitefish from Lake Michigan. No
significant difference was observed in abundance ofthe most common parasite species
between male and female round whitefish across all lakes.
TABLE 6. Gender-based estimates of parasites and their abundances of round whitefish using
the Mann-Whitney U Test for significance.
Abundance
Parasite Species/
Sample Size
Location
Male/Female
Male (±SD)
Female (±SD)
23/44
3.2 (±4.8)
2.7 (±4.8)
0.798
Lake Michigan
5/15
0.4(±0.5)
3.4 (±4.4)
0.39
Lake Huron
14/17
4.1 (±5.5)
3.1 (±5.8)
0.325
3.07 (±52.2)
31.5 (±77.9)
All Parasites
Lake Superior
4/9
p-value
<0.001
Diplostomum spathaceum
23/44
1.8 (±4.7)
0.7 (±2.2)
0.340
Acanthocephalus dirus
23/44
0.3 (±0.9)
0.4 (±0.7)
0.139
Eubothrium salvellini
23/44
0 (±0)
0.7 (±1.9)
0.790
Salmincola thymalli
23/44
0.6 (±1.5)
0.8 (±3.5)
0.500
Bloater.- The number of parasite taxa in bloaters collected from Lake Michigan
and Lake Superior ranged from 0-5, with 90% of fish with at least one parasite species
(Table 7). Bloaters were not collected from Lake Huron because their population is
considered to be extirpated in most areas. The infection rate in Lake Superior-North
(81%) was lower than the Lake Superior-West (91% ). All of the bloaters from Lake
Michigan were infected. The most common parasite species in Lake Michigan were C.
farionis and A. dirus. Prevalence of C. farionis was 90% in Lake Michigan with a mean
31
intensity of 27.1 parasites and a range of 1-112. Lake Michigan had a lower prevalence
and mean intensity (24.8 with range 0-76) of C. farionis (9%) compared to Lake
Superior. Prevalence of E. salmonis was 45%, with a mean intensity of 11.6 parasites
(range of 1-76) (Fig. 13).
16
• Lake Superior-North
14
DLake Superior-West
12
• Lake Michigan
~10
~
~
Q
z
8
6
4
2
0
0
3
2
4
5
No. of Parasite Species
FIGURE 13. Distribution of the number of parasite taxa infecting bloater from Lake
Michigan and Lake Superior.
32
TABLE 7. Infection prevalence(%), mean intensity(± S.D.) and range of intensities found in bloater (Coregonus hoyi) from sampling
sites in Lake Michigan and Lake Superior.
Lake Superior
w
w
Lake Michigan (n=30)
Parasite
Protozoa
Henneguya sp.
Mongenea
Discocotyle sagittata
Digenea
6.7,1 ±. und" (1)
Diplostornurn spathaceum
Cestoda
33 .3,2.7 ±1.8 (1-8)
Cyathocephalus truncatus
13 .3,6 ±.2.9 (1-15)
Eubotltrium salvelini
Proteocephalus exiguus
Proteocephalus sp.
Acanthocephala
83.3,13.8 ±16.1 (1-76)
Acanthocephalus dints
Metechinorhynchus salmonis
3.3,1 ±und"(l)
Neochinorhynchus tumidus
Nematoda
90.0,27.1 ±.30.9 (2-112)
Cystidicolafarionis
Crustacea
Salmineola
thymali
16.7,1.2 ±0.5 (1-2)
corpulentus
• Mathematical operation cannot be defined. (und =undefined)
North (n=30)
19.4,7.3 ±.3.5 (2-16)
West (n=22)
22.7,3 ±(1-10)
6.5,1.5 ±0.4 (1-2)
19 .4,3 ±.1.7 ( 1-8)
9.1,7.5 ±2.8 (2-13)
35.5,10.5 ±6.5 (3-25)
40.9,19.9 ±.3.5 (1-11)
22.7,46 ±36.3 (3-169)
19.4,5 ±.2.3 (1 -9)
45.1,5.8 ±.3.8 (2-12)
9.7,3.3 ±.1.3 (1 -7)
27.3,8.8 ±.8.1 (1-36)
38.7,24.8 ±.21.8 (2-95)
40.9,21.3 ±.19.5 ( 10-78)
9.7,1 ± und" (1)
12.9,1 ±und" (1)
4.6, 1 :!:. und' (I)
Overall parasite abundance was significantly different between Lake Superior and
Lake Michigan bloaters (Mann-Whitney U Test, df= 1, p = 0.011) (Fig. 14a). Lake
Michigan had a greater abundance of parasites than Lake Superior. In terms of the most
common parasite, abundance of C. farionis was significantly different between lakes
(Mann-Whitney U Test, df= 1, p < 0.05) (Fig. 14b). The less abundant parasite C.
truncatus did not significantly differ between the two lakes (Mann-Whitney U Test, df =
1, p > 0.05).
Bloater parasite abundance was also compared between two regions of Lake
Superior that were close in distance. Cystidicola farionis abundance was not
significantly different between the North and West sampling regions (Mann-Whitney U
Test, df= 1, p = 0.935) (Fig. 14b). Moreover, the mean abundance ofCyathocephalus
truncatus, P. exiguus, and A. dirus were not significantly different between sites (MannWhitney U Test, df= 1, p > 0.229). The condition factor ofbloaters between the two
regions was significantly different (Mann-Whitney U Test, df= 1, p < 0.001) (Fig. 15).
50
45
35
A
....~"' 40
35
~
j,
25
~ 30
.....
Q
20
25
~ 20
15
; 15
10
~
~
B
30
10
5
5
0
0
LM
LM
LS
LS
FIGURE 14. Parasite abundance (± 1 standard error) infecting bloater from Lake
Michigan (LM) and Lake Superior (LS). A. All parasite species; B. Cystidicolafarionis.
34
1_-1
I__:>
~
Jl
-=
=
0
().X
('l
;.,..,
=
('l
~
;::
(l_h
fl_~
(} __2
n
LS
L:'vl
FIGURE 15. Mean Faulton's K (condition factor)(± 1 standard error) of bloater
examined for parasites from Lake Michigan (LM) and Lake Superior (LS).
There was no correlation with host age and total parasite abundance or with that
of individual parasite species (Pearson Correlation Coefficient, r < 0.25). Bloater age
ranged from 8 to 28 years (Fig. 16).
14
12
..c 10
"'
~
8
=
0
6
......
z
4
2
II
0
I
I
0 1 2 3 4 56 7 8 9101112131415161718192021222324252627282930
Age (years)
FIGURE 16. Age distribution of bloater in Lake Superior and Lake Michigan.
There was a significant difference in total parasite abundance between sexes in
bloaters sampled in Lakes Michigan and Superior (Table 8). Female bloaters had a
higher abundance of parasites than the male bloaters sampled from all lakes. Bloaters
sampled in Lake Superior-North did not have significantly different parasite abundance
35
between males and females (Mann-Whitney U Test, df=l, p=0.068). In Lake SuperiorWest, parasite abundance between the two sexes was not significantly different. Lake
Michigan-South bloater parasite abundance did significantly differ between sexes.
Female bloater had a much greater parasite abundance compared to males.
Abundance of C. farionis was significantly different between sexes in bloaters
sampled from all lakes (Table 8). Conversely, C. truncatus, A. dirus, and P. exiguus had
similar parasite abundances between sexes from all lakes.
TABLER . Gender-based estimates of parasites and their abundance of bloater using the MannWhitney U Test for significance.
Abundance
Parasite Species/
Sample Size
Location
Male/Female
Male (±SD)
Female (±SO)
p-value
All Parasites
24/40
18.7 (±38.3)
31.5 (±32.2)
0.004
Lake Superior-W
10/12
23.8 (±51.5)
26.75 (±29.7)
0.275
Lake Superior-N
11/20
I 4.5 (±30.5)
21.H (±20.3)
0.06H
Lake Michigan-S
3/27
13.0 (+4.4)
40.7 (+38.3)
0.25
Cystidicola farionis
24/40
5.7 (±19.5)
11.6 (±27.2)
0.042
Cyathocephalus truncates
24/40
0.1 (±1.1)
0.9 (±2.3)
0.328
Acathocephalus dirus
24/40
0
0
0.201
Proteocephauls exiguus
24/40
3.5 (±5.8)
2.8 (±4.0)
0.594
Parasite abundances between host species.- Bloater and lake whitefish had
significantly different parasite abundances when data from Lake Michigan and Lake
Superior were combined (Mann-Whitney U Test, df = 1, p = 0.002) (Fig. 17a). Bloaters
had significantly higher abundances of C. farionis compared to lake whitefish (MannWhitney U Test, df= 1, p < 0.001) (Fig. 17b).
36
Parasite abundance of round whitefish, lake whitefish and bloater were compared
across regions in Lake Superior because it was the only lake to have all three species
present in samples. Parasite abundance was significantly different between the three
species (Kruskal-Wallis Test, df= 2, p < 0.001). Lake whitefish had the greatest parasite
abundance whereas round whitefish had the lowest. The abundance of dominant parasite
species, such as C. farionis was significantly different between fish species (KruskalWallis Test, df= 2, p < 0.001). Bloater was found to have the greatest abundance of C.
farionis and round whitefish had the lowest abundance. However, less abundant parasites
such as N tumidus and N rutlii did not differ between fish species (Kruskal-Wallis Test,
df= 2, p > 0.328).
....."'
2
3.5
~
A
·;;.;
~
!.
1.5
3
~
2.5
0
1.5
c..
.....Q
z
=
•LWF
B
BLO
2
0.5
~
~
~
T
0.5
0
0
LM
LS-W
LS-N
FIGURE 17. Parasite abundance (± 1 standard error) infecting lake whitefish (L WF) and
bloater (BLO) ofLake Michigan (LM), Lake Superior West (LS-W) and North (LS-N)
sampling regions. A. All parasite species; B. Cystidicolafarionis.
Parasite abundance was significantly different between round whitefish and lake
whitefish species across all sites (Mann-Whitney U Test, df= 1, p = 0.033) (Fig. 18a).
Lake whitefish sampled had a significantly higher abundance of C. farionis, A. dirus, and
P. exiguus compared to round whitefish (all Mann-Whitney U Tests, df= 1, p < 0.001).
Lake Huron lake whitefish had significantly higher total parasite abundance, and a higher
37
abundance of A. dirus compared to round whitefish (Mann-Whitney U Test, df= 1, p <
0.033) (Fig. 18a,b). In Lake Michigan overall parasite abundance did not differ between
the two whitefish species (Mann-Whitney U Test, df = 1, p = 0.836) (Fig. 18a).
Abundance of more common parasite species found in Lake Michigan was only
significantly different for C. farionis (Mann-Whitney U Test, df= 1, p = 0.016). For A.
dirus, abundance was similar between species (Mann-Whitney U Test, df= 1, p = 0.101)
(Fig. 18b). Overall parasite abundance did not differ between the two whitefish species
in Lake Superior (Mann-Whitney U Test, df= 1, p= 0. 352) (Fig. 18a). More common
parasite species were not significantly different between round whitefish and lake
whitefish (Mann-Whitney U Test, df= 1, p > 0.091) (Fig. 18b).
12
A
!JO
~
LWI'
I
·~
;
. RWF
8
p..
'1:; 6
Q
z4
=
_l
~
<l.l
~ 2
0
-~
LH
LM
45
40
35
30
25
20
B
l
15
10
5
0 .
LS-W
LH
LM
LS-W
FIGURE 18. Parasite abundance (± 1 standard error) infecting lake whitefish (L WF) and
round whitefish (RWF) from Lake Huron (LH), Lake Michigan (LM) and Lake Superior
West (LS-W) sampling regions. A. All parasite species; B. Acanthocephalus dirus.
38
Discussion
Coregonid fish populations have been negatively impacted as the Great Lakes
undergo environmental changes. Despite fewer numbers, whitefish are the most
important commercially harvested fish species and a key biological indicator of health for
the Great Lakes. Because of the current decline in condition factor of coregonids due to
the switching from native prey to exotic prey species, I predicted to find a higher
incidence of microbial pathogens than previously reported, and an altered parasite
community than previously documented.
No target bacterial pathogens other than Renibacterium salmoninarum were
detected from the coregonids sampled and even Renibacterium salmoninarum was found
at a very low incidence (one positive fish) in lake whitefish from western Lake Superior
using ELISA. Moreover, the single infected whitefish did not exhibit any visible signs of
bacterial kidney disease such as white granulomatous lesions in the kidney. Conversely,
Faisal et al. (2010a) detected R. salmoninarum in 305 of371 (82%) lake whitefish
sampled from northern Lakes Michigan and Huron between the years 2003 and 2006.
One explanation for this large discrepancy in R. salmoninarum incidence between studies
may lie in the different techniques employed to detect these pathogens. In the work by
Faisal et al. (2010a) bacteria were cultured on Modified Kidney Disease Medium
(MKDM), which is highly selective for R. salmoninarum from the kidney (White et al.
1995). Furthermore, Faisal et al. (2010a) also used q-ELISA which detects a protein
secreted by the bacteria. The standard ELISA used in my work was not as sensitive as
39
those of the above study (White et al. 1995) suggesting that infected fish may have not
have been detected as readily in my study.
Unlike this study, Loch and Faisal (2010) foundAeromonas salmonicida in four
lake whitefish from northern Lake Huron (n= 1,286 fish) during the course of three years
(fall2003-summer 2006). This was a very low infection incidence (0.3%) given the
number of hosts examined. The sample size (n=20) used in my work was much less than
that of Loch and Faisal (2010). Because of this, I may not have detected this pathogen
given its potentially low incidence in the fish population in combination with my small
sample size.
Even though no viral target pathogens were detected in this study, they have been
reported in previous work. For example, VHS has been documented in Great Lakes lake
whitefish and in lake herring (Coregonus artedi) from the Apostle Islands of Lake
Superior (www.wisconsin.dnr.gov/fish/vhs). Interestingly the infected lake herring were
collected in close proximity to where my Lake Superior-West samples were taken, but at
different time points. Seasonal variability in the transmission of this virus may help to
explain why previous work detected VHS, yet it was absent in my study. Although viral
pathogens were not detected in fish from my collections, reduced condition factor and
increased consumption of exotic prey species in coregonids may eventually lead to
increases in the incidence of viral pathogens, such as VHS, in these Great Lakes fish
(Wagner et al. 2010)
Recent switches in diet could have altered the parasite species present in the three
coregonid species in Lakes Michigan, Huron, and Superior. Lake Superior has a stable
forage base and was found to have a higher abundance of parasites and a greater diversity
40
of parasites species. However, in Lakes Michigan and Huron, where the forage base has
declined, parasite abundance and parasite species diversity is lower. The native forage
base ofmacroinvertebrates (Diporeia sp.) has been reduced in Lakes Michigan and
Huron, causing bottom-up limitations in the food web (Wells and Beeton 1963; Pothoven
and Madenjin 2008; Strayer 2009). When native prey abundance declines, predators
switch to different prey sources. Recently, coregonids have switched to consuming the
exotic dreissenid mussels and spiny water fleas could explain the differences in parasite
abundances between Lake Superior and Lakes Michigan and Huron (Pothoven and
Madenjin 2008; Strayer 2009). This idea is also supported by patterns seen in C. farionis
which was at its highest prevalence and abundance in Lake Superior. The intermediate
hosts of C. farionis are the amphipods Gammarus sp. and Diporeia sp. Declines in
amphipods in Lakes Huron and Michigan versus stable populations in Lake Superior
(Scharold et al. 2004) could account for the differences in C. farionis infections from
hosts collected from these different waterbodies.
Overall prevalence of C. farionis in lake whitefish in this study varied compared
to past work. For example, previous investigations of lake whitefish from Lake Superior
(Sutherland et al1985; Nepszy 1988) reported relatively high prevalence values (2087%) for C. farionis relative to this study (14%). Conversely, Faisal et al. (2009; 2010b)
found lower prevalence values of C. farionis in whitefish from Lakes Michigan (3 .310%) and Huron (12-33%) compared to this work (Lake Michigan- 22.6%; Lake Huron
- 40%). Seasonal variation in fish sampling could account for differences in C.farionis
prevalence (Faisal et al. 2010a). The relatively short sampling window employed in this
study likely provided a snapshot in the overall seasonal and annual patterns exhibited by
41
this parasite species. Collecting over a longer time scale would capture more of the
temporal variation in C. farionis infection dynamics potentially leading to a broader
estimate of nematode infections. Thus the longer collection periods employed in
previous studies (Sutherland et al. 1985) may help to explain differences between this
work and previous studies.
In past studies Cystidicola farionis has been identified in round whitefish;
however none were present in this study. Nepszy (1988) and Sutherland et al. (1985)
reported prevalences of C.farionis ranging from 7-59%. The absence of C. farionis may
be due to a loss of prey species that are intermediate hosts for C. farionis or an increase in
the consumption of exotic prey (Pothoven et al. 2006; Carlsson et al. 2009; Faisal et al.
2010b). Also in many sampling locations few round whitefish were collected in this
study providing limited representation of parasites present. Thus larger sample sizes of
round whitefish like in previous studies (Nepzy 1988; Sutherland et al. 1985) could
enhance the probability of capturing this nematode.
Prevalence of C. farionis in bloaters was also observed to differ between this
work and previous research. For instance, C. farionis prevalence from Lake Michigan
was 90% in this study compared to work by Sutherland et al. (1985) who reported a value
of6.7%. In Lake Superior, Nepszy (1988) reported C.farionis prevalence at 75%
compared to 40% in this study. As alluded to above, seasonal variation in sampling
could account for differences in prevalence of C. farionis because coregonids have been
shown to have a lower prevalence in the fall compared to other seasons (Faisal et al.
201 Oa). The lower prevalence of C. farionis in Lake Superior bloaters could be due to
bloaters inhabiting deeper waters. The deep waters of the Great Lakes are limited by
42
light and food therefore reducing the number of intermediate hosts that could survive
reducing the parasite distribution and exchange between deeper dwelling hosts (Wells
and Beeton 1963; Scharold et al. 2004; Pothoven and Madenjin 2008).
No relationship between mean parasite intensity and host age was identified for
any of the host species examined in this study. This was somewhat unexpected, as
correlations between parasite intensity and host age have been documented in other
studies (Hanek and Fernando 1978; Watson and Dick 1979). Hanek and Fernando (1978)
examined rock bass infected with three species of monogeneans and found rock bass
older than four years of age have a greater parasite load than younger fish (Hanek and
Fernando 1978). Coregonids are a long lived fish species which could allow for parasite
load to increase with age (Dryer and Beil 1968; DeBryune 2008). However, a lack of
individuals making up each age ~lass may have provided a very limited representation of
parasite intensity in young versus old fish.
There was little overlap of parasite species between lake and round whitefish in
this study. This was surprising, given that the species overlap in feeding habits,
movement, and spawning areas. Diplostomum spathaceum was one species where there
was overlap, but it exhibits broad host specificity and is ubiquitous in Great Lakes fishes
(Nepszy 1988). Similarly, lake whitefish and bloater shared few parasite species. Two
uncommon parasites, D. sagittata and E. salmonis had similar parasite abundances in
these hosts. Nepszy (1988) also reported overlap ofthese species in coregonids from the
Great Lakes. Climate change and alterations in food web dynamics may create
competition for habitat and prey among these species, and in turn, may disrupt parasite
life cycles leading to variation in parasite distributions.
43
Prior to European settlement, the Great Lakes were maintained by a balanced
diverse fish assemblage. Now, stocking of native and exotic fish species such as pacific
salmon and rainbow trout.( Onchorhynchus mykiss) has resulted in predatory fish species
becoming dominant in the Great Lakes. Prior to the 1930s, the planktivore: piscivore fish
ratio was 16:2 (lake trout, burbot). Today the ratio is 1.3:1 (Eby et al. 2006). This trophic
cascade over time could have influenced parasite dispersal and intermediate hosts across
the Great Lakes due to changing behavioral patterns of native fish species in competition
with exotic species (Eby et al. 2006).
Parasite communities of lake whitefish, round whitefish, and bloater were
different between water bodies and sampling regions in Lakes Michigan, Huron, and
Superior. Hudson et al. (2006) described an ecosystem rich in parasite species to
generally be a healthy community. Based on parasite analysis, the three coregonid
species in Lake Superior from this study reside in what could be considered a healthy fish
community and harbored a diverse fauna of parasites. As the sampling gradient went
from North to South (northern Lake Superior to southern Lake Michigan), parasite
diversity decreased. This could be due to habitat and food web degradation found in
Lakes Michigan and Huron and stable in Lake Superior. This was the first study to
examine parasite communities of coregonid species from multiple lakes and regions
within the Great Lakes. Previous work has documented parasites recorded in these
species; however, parasite data did not include a viral and bacterial component.
Continued monitoring of climate change and changing food web dynamics on the effects
of microbial and viral pathogens and parasites in Great Lakes coregonids would assist in
management of these important fish species.
44
References
Aoki, T. 1999. Motile aeromonads (Aeromonas hydrophila). Fish Diseases and
Disorders. Wallingford:CABI Publishing 427-453.
Austin, B., and C. Adams. 1996. The Genus Aeromonas. Fish Pathogens.
John Wiley & Sons, Inc .. Chichester, UK.
Austin, B., and D. A. Austin. 2007. Bacterial pathogens. Disease offarmed and wild fish.
Chichister: Praxis Publishing Ltd. Chichester, UK.
Baldwin, R. E., and C. P. Goater. 2003. Circulation of parasites among fishes from lakes
in the Caribou Mountains, Alberta, Canada. The Journal of Parasitology 89:215225.
Bangham, R. V. 1955. Studies offish parasites of Lake Huron and Manitoulin Island.
American Midland Naturalist 53:184-194.
Bence, J. R., and L. C. Mohr. 2004. The state of Lake Huron in 2004. Great Lakes
Fishery Commision. Special Report 08-01. www.glfc.org/pubs_out/commun/.
(August 2008).
Bergmann, S. M., and D. Fichtner. 2008. Diseases caused by virus: viral diseases in
salmonids. Fish Disease: Volume 1. Science Publishers, Enfield, New Hampshire.
Beverley-Burton, M. 1984. Monogenea and turbellaria. Pages 5-209 in L.
Margolis and Z. Kabata, editors. Guide to the parasites of fishes of Canada. Part I.
Canadian Special Publication of Fisheries and Aquatic Sciences 74. Monograph
Pulishing Program, Ottawa, ONT.
Brenden, T. 0., M.P. Ebener, T. M. Sutton, M. L. Jones, M. T. Arts, T. B. Johnson,
G. M. Wright, and M. Faisal. 2010. Assessing the health oflake whitefish
populations in the Laurentian Great Lakes: lessons learned and research
recommendations. Journal of Great Lakes Research 36:135-139.
Brown, R. W., M.P. Ebener, and T. Gorenflo. 1999. Great Lakes commercial fisheries:
historical overview and prognosis for the future. Great Lakes fisheries policy and
management. Michigan State University Press, East Lansing, MI
Brown, E. H., R. W. Rybicki, and R. J. Poff. 1985. Population dynamics an
45
interagency management of the bloater (Coregonus hoyi) in Lake Michigan,
1967-1982. Great Lakes Fishery Commission, Ann Arbor, MI. Available:
www.glfc.org/pubs out/communi/. (March 1985).
Busiahn, T. R. 1990. Fish community objectives for Lake Superior. Great Lakes Fishery
Commission, Ann Arbor, MI. Available: www.glfc.org/pubs out/communi/.
(January 1990).
Carlsson, N. 0., 0. Samelle, and D. L. Strayer. 2009. Native predators and exotic preyan aquired taste? Frontier Ecology and Environment 10:525-532.
Chappell, L. H. 1969. The parasites of the three-spined Stickleback Gasterosteus
aculeatus L. from a Yorkshire pond. II Variation of the parasite fauna with sex
and size offish. Journal ofFish Biology 1:339-347.
Cipriano, C. R., L.A. Ford, D. R. Smith, J. H. Schachte, and C. J. Petrie. 1997.
Differences in detection of Aeromonas salmonicida in covertly infected salmonid
fishes by the sress-inducible furunculosis test and culture-based assays. Journal
of Aquatic Animal Health 9:108-113.
Cipriano, R. C., and G. L. Bullock. 2001. Furunculosis and other diseases caused by
Aeromonas salmonicida. U.S. Fish and Wildlife Service, U.S. Geological Survey,
Kerneysville. Fish Disease Leaflet:66.
Clapp, D. F., and W. Horns. 2008. The state of Lake Michigan in 2005. Great Lakes
Fishery Commission, Ann Arbor, MI. Available:
www.glfc.org/pubs out/communi/ (October 2008).
Claramunt, R. M., and D. F. Clapp. 2005. Image analysis procedures for aging calcified
structures: an example with Lake Michigan lake whitefish. Michigan DNR Fish
Technical Report 2005-2.
Cone, D., D. J. Marcogliese, and R. Russell. 2004. The myxozoan fauna of spottail shiner
in the Great Lakes Basin: membership, richness, and geographical distribution.
The Journal ofParasitology 90:921-932.
Dailey, M.D., and G. D. Schmidt. 1996. Meyer, Olsen, and Schmidt's Essentials of
Parasitology, sixth edition. WCB Publishers, Dubuque, Iowa.
DeBryune, R. L., T. L. Galarowicz, R. M. Claramunt, and D. F. Clapp. 2008. Lake
whitefish relative abundance, length-at-age, and condition in Lake Michigan as
indicated by fishery-independent surveys. Journal of Great Lakes Research
34:235-244.
DesJardine, R. L., T. K. Gorenflo, R.N. Payne, and J.D. Schrouder. 1995.
46
Fish-community objectives for Lake Huron. Great Lakes Fishery Commission,
Ann Arbor, MI. Available: www.glfc.org/pubs out/communi/. (April 1995).
Dryer, W. R. 1963. Age and growth of the whitefish in Lake Superior. U.S. Fish and
Wildlife Service. Fisheries Bulletin. 63:77-85.
Dryer, W. R. and W. W. Beil. 1968. Growth changes in the bloater (Coregonus hoyi) of
the Apostle Islands region of Lake Superior. Transactions of American Fisheries
Society 97:146-148.
Ebener, M.P. 2007. The state of Lake Superior in 2000. Great Lakes Fishery
Commission, Ann Arbor, MI. Available: www.glfc.org/pubs out/communi/. (July
2007).
Ebener, M.P., L. C. Mohr, S. Riley, E. F. Roseman, and D. G. Fielder. 2004. Status of
Lake Huron. Great Lakes Fishery Commission. Special Report. 08-01.
Ebener, M.P., G. M. Wright, P. J. Schneeberger, and R. M. Claramunt. 2005. Status of
Lake Michigan. Great Lakes Fishery Commission, Ann Arbor, MI. Available:
www.glfc.org/pubs out/communi/. (March 2005).
Eby, L. A., J. J. Roach, L. B. Crowder, and J. A. Stanford. 2006. Effects of stocking-up
freshwater food webs. Trends in Ecology and Evolution 21:576-584.
Elsayed, E., M. Faisal, M. Thomas, G. Whelan, W. Batts, and J. Winton. 2006.
Isolation of viral haemorrhagic septicaemia virus from muskellunge, Esox
masquinongy (Mitchill), in Lake St. Clair, Michigan, USA reveals a new
sublineage of the North American genotype. Journal ofFish Diseases 29:611619.
Eshemoder, R. L., M. E. Holey, T. K. Gorenflo, and R. D. Clark, Jr. 1995. Fish
community objectives for Lake Michigan. Great Lakes Fishery Commission, Ann
Arbor, MI. Available: www.glfc.org/pubs_out/communi/. (November 1995).
Faisal, M., T. P. Loch, T. 0. Brenden, A. E. Eissa, M.P. Ebener, G. M. Wright, and M.
L. Jones. 2010a. Assessment of Renibacterium salmoninarum infections in four
lake whitefish (Coregonus clupeaformis) stocks from northern Lakes Huron and
Michigan. Journal of Great Lakes Research 1:95-102.
Faisal, M., W. Fayed, T. 0. Brenden, A. Noor, M.P. Ebener, G. M. Wright, and M. L.
Jones. 2010b. Widespread infection oflake whitefish Coregonus clupeaformis
with the swimbladder nematode Cystidicola farionis in northern lakes Michigan
and Huron. Journal of Great Lakes Research 36:18-28.
Fryer, J. L., and J. E., Sanders. 1981. Bacterial kidney disease of salmonid fish. Annual
Review of Microbiology 35:273-298.
47
Goodwin, A. E. 2011. First report of spring viremia of carp virus (SVCV) in North
America. Journal of Aquatic Animal Health 14:161-164.
Grizzle, J. M. and C. J. Brunner. 2003. Review of largemouth bass virus. Fisheries
28:10-14.
Hanek, G., and C. H. Fernando. 1978. The role of season, habitat, host age, and sex on
gill parasites of Ambloplites rupestris. Canadian Journal of Zoology 56:12511253.
Hanzelova, V., and T. Scholz. 1999. Species of Proteocephalus Weinland, 1858
(Cestoda: Proteocephalidae), parasites of coregonid and salmonid fishes from
North America: Taxonomic Reappraisal. The Journal of Parasitology 85:94-101.
Hoffman, G. L. 1999. Parasites ofNorth American freshwater fishes. Comstock
Publishing Associates, Ithaca, New York.
Hope, K. M., R.N. Casey, G. H. Groocock, R.G. Getchell, P.R. Bowser, and J. W.
Casey. 2010. Comparision of quantitative RT-PCR with cell culture to detect viral
hemorrhagic septicemia virus (VHSV) IVb infections in the Great Lakes. Journal
of Aquatic Animal Health 22:50-61.
Horns, W. H., C. R. Bronte, T. R. Busiahn, M.P. Ebener, R. L. Eshenroder, T. Gorenflo,
N. Kmiecik, W. Mattes, J. W. Peck, M. Petzold, and D. R. Schreiner. 2003. Fishcommunity objectives for Lake Superior. Great Lakes Fishery Commission, Ann
Arbor, MI. Available: www.glfc.org/pubs out/communi/. (March 2003).
Hudson, P. J., A. P. Dobson, and K. D. Lafferty. 2006. Is a healthy ecosystem one that is
rich in parasites? Trends in Ecology and Evolution 21:381-385.
Ihssen, P.E., D.O. Evans, W.J. Christie, J.A. Reckahn, and R.L. DesJardine. 1981. Life
history, morphology, and electrophoretic characteristics of five allopatric stocks
of lake whitefish (Coregonus clupeaiformis) in the Great Lakes region. Canadian
Journal of Fish and Aquatic Science 3 8: 1790-1807.
Isermann, D. A., J. R. Meerbeek, G. D. Scholten, and D. W. Willis. 2003. Evaluation of
three different structures used for walleye age estimation with emphasis on
removal and processing times. North American Journal of Fisheries Management
23:625-631.
Jonas, J. L., P. J. Schneeberger, D. F. Clapp, M. Wolgamood, G.Wright, and B. Lasee.
2002. Presence of the BKD-causing bacterium Renibacterium salmoninarum in
lake whitefish and bloaters in the Laurentian Great Lakes. Hydrobiologia.
Special Issues, Advancing Limnology 57:447-452.
48
Karvonen, A., and E. T. Valtonen. 2004. Helminth assemblages of whitefish
(Coregonus lavaretus) in interconnected lakes: Similarity as a function of species
specific parasites and geographical .separation. The J oumal of Parasitology
90:471-476.
Lafferty, K. D., J. W. Porter, S. E. Ford. 2004. Are diseases increasing in the
ocean? Annual Record in Ecology Evolution Systems 35:31-54.
Lawrie, A. H., and J. F. Rahrer. 1973. Lake Superior: A case history ofthe lake and its
fisheries. Great Lakes Fishery Commission, Ann Arbor, MI. Available:
www.glfc.org/pubs out/communi (January 1973).
Loch, T. P., and M. Faisal. 2010. Isolation of Aeromonas salmonicida subspecies
salmonicida from lake whitefish (Coregonus Clupeaformis) inhabiting Lakes
Michigan and Huron. Journal of Great Lakes Research 36:13-17.
Matitsky, S. E., A.Y. Karatayev, L. E. Burlakova, and D.P. Molloy. 2010. Parasites of
exotive species in invaded areas: does lower diversity mean lower epizootic
impact? Diversity and Distribution 16:798-803.
Margolis, L., G. W. Esch, J. C. Holmes, A.M. Kuris, and G. A. Schad. 1982. The use
of ecological terms in parasitology (Report of an ad hoc committee of the
American society of parasitologists). The Journal ofParasitology 68:131-133.
Mesa, M.G., T. P. Poe, A. G. Maule, arid C. B. Schreck. 1998. Vulnerability to predation
and physiological stress response in juvenile Chinook salmon (Onchorynchus
tshawytscha) experimentally infected with Renibacterium salmoninarum.
Canadian Journal ofFish and Aquatic Science 55:1599-1606.
Muzzall, P.M. 1995. Parasites oflake trout, Salvelinus namaycush, from the Great
Lakes: a review of the literature 1874-1994. Journal of Great Lakes Research
21:549-598.
Nalepa, T. F., D. J. Hartson, D. L. Fanslow, G. A. Lang, and S. J. Lozano. 1998.
Declines in benthic macroinvertebrate populations in southern Lake Michigan,
1980-1993. Canadian Journal ofFish and Aquatic Science 55:2402-2413.
Nalepa, T. F., D. W. Schloesser, S. A. Pothoven, D. W. Hondorp, D. L. Fanslow,
M. L. Tuchman, and G. W. Fleischer. 2001. First finding ofthe amphipod
Echinogam marus ischnus and the mussel Dreissena burgensis in Lake Michigan.
Journal of Great Lakes Research 27:384-391.
Nepszy, S. J. 1988. Parasites offishes in the Canadian waters ofthe Great Lakes. Great
Lakes Fishery Commission, Ann Arbor, MI. Available:
www.glfc.org/pubs out/communi/. (January 1988).
49
Pothoven, S. A., and T. F. Nalepa. 2006. Feeding ecology oflake whitefish in Lake
Huron. Journal of Great Lakes Research 32:489-501.
Pothoven, S. A., and C. P. Medenjian. 2008. Changes in consumption by alewives and
lake whitefish after dreissenid mussel invasions in Lake Michigan and Lake
Huron. North American Journal of Fisheries Management 28:308-320.
Pothoven, S. A., T. F. Nalepa, P. J. Schneeberger, and S. B. Brandt. 2001. Changes in
diet and body condition of lake whitefish in southern Lake Michigan associated
with changes in benthos. North American Journal of Fisheries Management
21:876-883.
Pothoven, S. A., T. F. Nalepa, C. P. Madenjian, R. R. Rediske, P. J. Schneeberger, and J.
X. He. 2006. Energy density of lake whitefish Core go nus clupeaformis in Lakes
Huron and Michigan. Environmental Biology ofFish 76:151-158.
Scharlod, J. V., S. L. Lozano, and T. D. Corry. 2004. Status of the amphipod Diporeia
spp. in Lake Superior, 1994-2000. Journal of Great Lakes Research 30:360-368.
Schneeberger, P. J., M.P. Ebener, M. L. Toneys, and P. J. Peters. 2005. Status oflake
whitefish (Coregonus clupeaformis) in Lake Michigan. In Proceedings of a
workshop on the dynamics of lake whitefish (Coregonus clupeaformis) and the
amphipod Diporeia spp. in the Great Lakes. Great Lakes Fishery Commission,
Ann Arbor, MI. Available: www.glfc.org/pubs out/communi/. (March 2005).
Smith, S. H. 1964. Status ofthe deepwater cisco population of Lake Michigan.
Transactions of American Fisheries Society 93:155-163.
Smith, 0. H., and J. V. Oosten. 1940. Tagging experiments with lake trout, whitefish, and
other species of fish from Lake Michigan. Transactions of American Fisheries
Society 69:63-84.
Strayer, D. L. 2009. Twenty years of zebra mussels: lessons from the mollusk that made
headlines. Frontier Ecology and Environment 3:135-141.
Sutherland, D. R., M. Moubry, R. L. Calentine, and B. A. Lasee. 1985. Fish parasite
communities as indicators of predator-prey relationships in Lakes Michigan and
Superior. Wisconsin Sea Grant. Madison, WI.
USFWS and AFS-FHS (U.S. Fish and Wildlife Service and American Fisheries Society
Fish Health Section). 2007. Standard procedures for aquatic animal health
inspections. In AFS-FHS. FHS blue book: suggested procedures for the detection
and identification of certain finfish and shellfish pathogens, 201 0 edition. AFSFHS, Bethesda, Maryland.
Valtonen, E. T., and T. Valtonen. 1978. Cystidicolafarnionis as a swimbladder parasite
50
ofthe whitefish in the Bothinian Bay. Journal ofFish Biology 13:557-561.
Wagner, T., M. L. Jones, M.P. Ebener, M. T. Arts, T. 0. Brenden, D. C. Honeyfield,
G. M. Wright, and M. Faisal. 2010. Spatial and temporal dynamics of lake
whitefish (Coregonus clupeaformis) health indicators: Linking individual based
indicators to a management-relevant endpoint. Journal of Great Lakes Research
36:121-134.
Watson, R. A., and T. A. Dick. 1979. Metazoan parasites of whitefish Coregonus
clupeaformis (Mitchill) and cisco C. Artedii Lesueur from Southern Indian Lake,
Manitoba. Journal ofFish Biology 15:579-587.
Wells, L., and A.M. Beeton. 1963. Food ofbloater, Coregonus hoyi, in Lake Michigan.
Transactions of American Fisheries Society 92:245-255.
White, M. R., C. C. Wu, and S. R. Albregts. 1995. Comparison of diagnostic tests for
bacterial kidney disease in juvenile steelhead trout (Oncorhynchus mykiss).
Journal ofVetrinary Diagnostic Investigation 7:494-499.
Willers, W. B., R. R. Dubielzig, and L. Miller. 1991. Histopathology ofthe swim bladder
ofthe cisco due to the presence of the nematode Cystidicola farionis Fischer.
Journal of Aquatic Animal Health 3:130-133.
Zimmerman, M.S., and C. C. Krueger. 2009. An ecosystem perspective on re
establishing native deepwater fishes in the Laurentian Great Lakes. North
American Journal of Fisheries Management 29:1352-1371.
51
APPENDIX A
LIST OF TARGET PATHOGENS SCREENED FOR BY FISH HEALTH METHODS
Viral Target Pathogens
Viral Hemorrhagic Septicemia
Infectious Pancreatic Necrosis
Infectious Hematopoietic Necrosis
Spring Viremia of Carp Virus
Largemouth Bass Virus
Bacterial Target Pathogens
Aeromonas spp.
Edwardsiella ictaluri
Edwardsiella tarda
Yersinia ruckeri
Renebacterium salmoninarum
53
APPENDIXB
SPECIES AFFECTED BY VIRAL HEMORAGIC SEPTICEMIA (VHS) FEDERAL
ORDER
(http://www.aphis. usda. gov/animal_health/emergingissues/downloads/vhsgreatlakes. pdf)
Black crappie
Bluegill
Bluntnose minnow
Brown bullhead
Brown trout
Burbot
Channel catfish
Chinook salmon
Emerald shiner
Freshwater drum
Gizzard shad
Lake whitefish
Largemouth bass
Muskellunge
Shorthead redhorse
Northern pike
Pumpkinseed
Rainbow trout
Rock bass
Round goby
Silver redhorse
Smallmouth bass
Spottail shiner
Trout-Perch
Walleye
White bass
White perch
Yell ow perch
Poxomis nigromaculatus
Lepomis macrochirus
Pimphales notatus
Ictalurus nebulosus
Salmo trutta
Lota Iota
Ictalurus punctatus
Oncorhynchus tshawytscha
Notropis atherinoides
Aplodinotus grunniens
Dorosoma cepedianum
Coregonus clupeaformis
Micropterus salmoides
Esox musquinongy
Moxostoma macrolepidotum
Exos lucius
Lepomis gibbosus
Onchorhynchus mykiss
Ambloplites rupestris
Meogobius melanstomus
Moxostona anisurum
Micropterus dolomieu
Notropis hudsonius
Percopsis omiscomaycus
Sander vitreus
Marone chrysops
Marone americana
P erca jlavescens
55
APPENDIXC
INNER EAR BONE (OTOLITH) FOR AGEING (BEFORE AND AFTER BEING
CRAC;KED AND BURNED)
BEFORE
AFTER
57