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Parasites of Walleyes, Stizostedion vitreum, from Saginaw Bay, Lake Huron, and the Other Great Lakes
J. Great Lakes Res. 24(1):152-158 Internat. Assoc. Great Lakes Res., 1998
NOTE Parasites of Walleyes, Stizostedion vitreum, from Saginaw Bay, Lake Huron, and the Other Great Lakes Patrick M. Muzzall 1* and Robert C. Haas2 1Department
ofZoology Natural Science Building Michigan State University East Lansing, Michigan 48824 2Michigan Department ofNatural Resources Mt. Clemens Fisheries Station 33135 South River Road Mount Clemens, Michigan 48045 ABSTRACT.
A total of 79 walleyes, Stizostedion vitreum (Percidae), was collected from inner and outer Saginaw Bay, Lake Huron, in September 1993 and 1994 and examined for parasites. Nine parasite species (one Monogenea, two Digenea, two Cestoda, one Nematoda, one Copepoda, one Protozoa, one virus) infected walleyes from the bay. The copepod Ergasilus luciopercarum had the highest prevalence and mean intensity followed by the cestode Bothriocephalus cuspidatus. Of the helminth species found, only B. cuspidatus and the monogenean Urocleidus aculeatus were gravid. Walleye parasite faunas were similar between areas. Walleyes from the Great Lakes have had 46 parasites species recorded. Walleye is a definitive host for many parasite species but does not play an important role as an intermediate and transport host for parasites in the Great Lakes.
INDEX WORDS: Walleye, Stizostedion vitreum, Percidae, parasites, Saginaw Bay, Lake Huron.
community of walleyes in Saginaw Bay so that changes brought about by environmental variation and exotic fish and invertebrate introductions can be understood. The objectives of the present study were to provide information on the occurrence and abundance of parasites of walleyes from inner and outer Saginaw Bay, Lake Huron and to summarize and compare the known information about parasites infecting this species in the Great Lakes.
INTRODUCTION
The walleye, Stizostedion vitreum, is an extremely popular fish and a substantial sport fishery has been created in Saginaw Bay, Lake Huron (Mrozinski et al. 1991). Several studies have investigated the parasites of walleyes in the Great Lakes; however, little is known about their parasites in Saginaw Bay. The aquatic environment and prey fish community of Saginaw Bay will undergo major changes following colonization by exotic species such as the white perch (Morone americana), round goby (Neogobius melanostomus), ruffe (Gymnocephalus cernuus), spiny water flea (Bythotrephes cederstroem i), and zebra mussel (Dreissena polymorpha). It is important to document the parasite
METHODS
Walleyes were collected by gill net from Saginaw Bay, which is the southwestern extension of Lake Huron located in east central Michigan. It is a large, shallow, eutrophic bay divided into inner and outer areas. The inner area, with a mean depth of 4.6 m, is shallower and warmer than the outer area, and is enriched with domestic, agricultural, and industrial inputs from the Saginaw River. Haas and Schaeffer
'Corresponding author. E-mail: [email protected]
152
Parasites of Walleyes from the Great Lakes
153
TABLE 1. Mean lengths (mm), weights (kg), ages (ranges), and 95% confidence intervals of Stizostedion vitreum examined from inner and outer areas of Saginaw Bay, Lake Huron, in September 1993 and 1994. (N =number of walleyes examined.)
Mean leanth ± S.D. (range, 95% confidence interval)
Mean weight ± S.D. (range, 95% confidence interval
Mean age ± S.D. (range, 95% confidence interval)
Inner Saginaw Area (N=47)
457 ± 89 (305-599, 431 -483)
1.0 ± 0.6 (0.3-2.2, 0.9-1.2)
3.4 ± 1.8 (1-8,2.8-3.9)
Outer Saginaw Area (N=32)
513 ± 58 (350-622,492-534)
1.3 ± 0.5 (0.3-2.4, 1.1-1.5)
4.8 ± 1.5 (1-8,4.2-5.3)
Location
(1992) described the fish community of Saginaw Bay in detail. Walleyes were examined from two locations in the Inner Saginaw Area: The Black Hole (latitude, longitude; 43°48'06", 83°51'42") and Carreon Reef (43°43'12", 83°43'12") and from two locations in the Outer Saginaw Area: Au Gres (43°58'58", 83°39'37") and Oak Point (43°59'12", 83°18'00"). Fish were measured, weighed, and tagged in the field, put on ice, and then frozen. Skin, fins, gills, eyes, kidney, gonads, heart, spleen, liver, gall bladder, mesentery, esophagus, and gastrointestinal tract were examined. Parasites were collected and processed using routine procedures. Prevalence was calculated as percentage of fish infected and mean intensity as mean number of parasites per infected fish. Prevalence was only calculated for Urocleidus aculeatus and Trichodina sp. Additional information on the parasites of walleyes was obtained from examining published studies performed in the Great Lakes. Data on walleyes from the St. Marys River, which connects Lake Superior and Lake Huron, are included with Lake Huron. Species richness refers to the number of parasite species infecting walleyes from each Great Lake. The Jaccard coefficient of community similarity (CC) was calculated as
where Sl and S2 are the number of parasite species in communities 1 and 2 , respectively, and C is the number of species common to both communities (Brower and Zar 1984). For calculations of the Jaccard coefficient of community similarity and species richness, Diplostomum (present study) and
Diplostomulum in other studies were considered to be a single species.
RESULTS Walleyes from four locations in Saginaw Bay were infected with one or more parasites (Table 1). Fish from the outer area were larger than those from the inner area. Nine parasite species (nine from the inner area and seven from the outer area) infected walleyes from the bay (Table 2). Ergasilus luciopercarum Henderson, 1926 had the highest prevalence and mean intensity in both areas. There were significant negative relationships between walleye length (r = -0.73, P < 0.01), weight (r = -0.64, P < 0.01), and age (r = -0.60, P < 0.01) with the intensities of E. luciopercarum from the inner area. The nonsignificant relationships between E. luciopercarum intensities and host length, weight, and age from the outer area were positive, negative, and negative, respectively. Percentages of E. luciopercarum with egg sacs from the inner and outer areas were 6.3% and 1.1 %, respectively. Bothriocephalus cuspidatus Cooper, 1917 was the next most common parasite of walleyes from both areas. The relationships of B. cuspidatus intensities and host length, weight, and age from the inner area were negative, while these relationships from the outer area were positive; all relationships were nonsignificant. There were no significant differences in the prevalences (Chi-square analyses, P > 0.05) and intensities (Mann-Whitney U test, P > 0.05) of E. luciopercarum and B. cuspidatus between areas. Of the helminth species found, only B. cuspidatus and Urocleidus aculeatus (Van Cleave and Mueller, 1932) Mueller, 1934 were gravid. Urocleidus aculeatus infected a significantly larger percentage of walleyes from the inner
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Muzzall and Haas
TABLE 2. Prevalence (P), mean intensity (MI), and maximum number of parasites (max.) found in Stizostedion vitreumfrom inner (N = 47) and outer (N =32) Saginaw Bay, Lake Huron, in September 1993 and 1994. * denotes larval or immature stages. NC =parasite present but mean intensity not calculated. Dash
=parasite not found.
Parasite Monogenea Urocleidus aculeatus
P(%)
Inner MI ± SD (max.)
Outer MI ± SD (max.) Site
P(%)
62
NC
34
NC
Gills
2 2
4(4) 1(1)
3
1(1)
Lens Stomach
96
84
12.9 ± 19.3 (104)
2
16.1 ± 15.9 (52) 1(1)
2
3(3)
3
2(2)
96
46.2 ± 50.1 (203)
100
42.8 ± 30.2 (115)
Gills
9
NC
19
NC
Gills
11
NC
6
NC
Fins, skin
Digenea
Diplostomum sp. *
Bucephalidae Cestoda Bothriocephalus cuspidatus Proteocephalus sp. *
Anterior intestine, pyloric ceca Encysted in liver
Nematoda Eustrongylides tubifex*
Encysted in mesentery
Copepoda Ergasilus luciopercarum
Protozoa Trichodina sp. Virus Lymphocystis
area than from the outer area (X 2 = 4.25, P < 0.05). Mean lengths ± SD of walleyes infected with U. aculeatus from the inner and outer areas were 455 mm ± 82 and 501 mm ± 31, respectively. Other parasite species infrequently infected walleyes. The two bucephalid trematodes could not be identified beyond family due to their poor condition. The Eustrongylides tubifex found in walleye were in poor condition. There were no significant differences in prevalence (Chi-square analyses, P> 0.05) or intensity (Mann-Whitney U test, P > 0.05) of parasitism between female and male walleyes from each area. Jaccard's coefficient of similarity for the parasite faunas, including lymphocystis, of walleyes from the inner and outer areas was 0.77. Mean parasite species richness ± SD, range, and 95% confidence intervals in walleyes from the inner area (2.8 ± 0.77,1 to 4,2.58 to 3.04) and from the outer area (2.5 ± 0.76, I to 4, 2.23 to 2.78) were not significantly different (Mann-Whitney U test, P > 0.05). Fifty-seven percent (N = 27) of the walleyes from the inner area were concurrently infected with E. luciopercarum, B. cuspidatus, and U. aculeatus; whereas, 22 percent (N = 7) from the
outer area were concurrently infected with these specIes.
DISCUSSION Ergasilus luciopercarum was the most common parasite species infecting walleyes from Saginaw Bay, followed by Bothriocephalus cuspidatus and then Urocleidus aculeatus. The parasite faunas of walleyes from the inner and outer areas were very similar suggesting that these walleyes are not from separate populations. The similar and low mean parasite species richness values in these walleyes from the areas also support this. Furthermore, tagging studies indicate there is some interchange with walleyes from Lake St. Clair and Lake Erie (Mrozinski et a1. 1991). The gill parasites, E. luciopercarum and U. aculeatus, have direct life cycles. The mean intensity of E. luciopercarum and prevalence of U. aculeatus were highest on walleyes from the inner area. This higher mean intensity of E. luciopercarum may be due to smaller, younger fish examined from this area since significant negative relationships occurred between intensities and host size and age.
Parasites of Walleyes from the Great Lakes The difference in the percentage of E. luciopercarum with egg sacs on walleyes between areas may be temperature related with more copepods maturing and retaining their egg sacs on hosts for a longer period of time in the warmer inner area. Bothriocephalus cuspidatus has an indirect life cycle. Essex (1928) reported that larvae of this cestode species develop in the coelom of Cyclops spp. and a second intermediate host was not needed. He suggested small B. cuspidatus infect adults either through infected copepods being strained directly from the water and ingested by walleyes or through the ingestion of small fish that had recently eaten infected copepods. Amin (1992) proposed that infected prey fish species play a role in transmitting B. cuspidatus to walleyes. Four yellow perch, Perca flavescens, from Saginaw Bay were infected with small Bothriocephalus (Muzzall, unpubl. data), supporting the suggestion that it uses a transport host. Haas and Schaeffer (1992) reported that walleyes feed on yellow perch in Saginaw Bay. Wolfert et al. (1967) reported that large numbers of B. cuspidatus caused the ceca of Lake Erie walleyes to become greatly distended, but no inflammation was noted. They noted that the largest number of B. cuspidatus had no detrimental effect on walleye weights and suggested (p. 112) "The greater incidence of worms in the 'fatter' walleyes must have resulted from a greater degree of exposure to infection, i.e., the more successful a fish was in capturing food, the greater numbers of parasitized prey it consumed." The parasite faunas of walleyes and yellow perch, collected in September from different years from the same Saginaw Bay location, differed. Over 10 parasite species infected yellow perch examined by PMM in September 1991, with Eustrongylides tubifex and Proteocephalus plerocercoids being most common. Haas and Schaeffer (1992) reported that walleye and yellow perch differed in their diet in the inner area, with walleyes primarily piscivorous and yellow perch primarily consuming chironomid larvae and zooplankton. The parasite species richness of walleyes from each Great Lake from the literature was: Lake Superior-8 (Dechtiar and Lawrie 1988); Lake Huron11 (Dechtiar et al. 1988), 9 (present study); Lake Erie-19 (Bangham and Hunter 1939), 3 (Wolfert et al. 1967), 15 (Bangham 1972), 22 (Dechtair and Nepszy 1988), and Lake Ontario-21 (Dechtiar and Christie 1988). A total of 46 parasite species (2 Monogenea, 15 Digenea, 8 Cestoda, 7 Nematoda, 6 Acantho-
ISS
cephala, 3 Crustacea, 1 Hirudinea, 1 Mollusca, 2 Protozoa, 1 virus) has been reported from walleyes in the Great Lakes (Table 3). The number of studies and number of fish examined for parasites from each Great Lake vary dramatically. The number of walleyes examined from Lake Erie is represented only by parasite surveys and include Bangham and Hunter (1939), Bangham (1972), Dechtiar (1972), and Dechtiar and Nepszy (1988) (Table 3). Studies on walleye parasites from Lake Michigan have not been published. Eight parasite species have been reported from walleyes in Lake Superior, 24 from Lake Huron including 9 from Saginaw Bay, 23 from Lake Ontario, and 29 from walleyes in Lake Erie. Urocleidus aculeatus, Sanguinicola occidentalis, B. cuspidatus, Neoechinorhynchus teneZlus, E. luciopercarum, and lymphocystis have been reported from walleyes in all these Great Lakes. Of the 37 helminth species reported, 24 (65%) are represented as adults. The distribution and percentage of parasites (where data were provided) by host site were: gastrointestinal tract, 47.5%; gills, 17.5%; mesentery and viscera, 15%; skin and muscle, 12.5%; eye, 5%; and blood, 2.5%. These studies on the parasites of walleyes demonstrate that B. cuspidatus is the most common gastrointestinal parasite of walleyes in each Great Lake. This indicates that one or more of the copepod first intermediate hosts is common and that the piscivorous diet of walleyes exposes them to infected fish transport hosts in each Great Lake. Also, E. luciopercarum or U. aculeatus is consistently the most common external parasite of walleyes in each lake. Ergasilus luciopercarum has been reported from a variety of fish hosts in the Great Lakes (Hudson et al. 1994). Jaccard's coefficient of similarity for the parasite faunas in walleyes from the Great Lakes were lowest in comparisons involving Lake Superior (Table 4). The lowest one involved walleyes from this lake and Lake Erie. Walleyes from Lakes Huron and Ontario had the highest coefficient indicating that they shared the most parasite species. Ergasilus luciopercarum and the virus that causes lymphocystis are considered to be pathogens of Great Lakes walleyes. Dechtiar and Nepszy (1988) and Dechtiar and Christie (1988) reported that feeding and the movements of E. luciopercarum on the gills of walleyes from Lakes Erie and Ontario caused destruction, hemorrhaging, hyperplasia, and hypertrophy of the filaments. The prevalence of lymphocystis on walleyes may be high in some Great Lakes locations and affected fish are com-
156
Muzzall and Haas
TABLE 3. Reported parasites of Stizostedion vitreum from the Great Lakes. Data were taken from the following studies: 1 =Dechtiar and Lawrie (1988); 2 =Dechtiar et al. (1988); 3 =present study, Saginaw Bay; 4 =Muzzall (1984); 5 =Dechtiar and Christie (1988); 6 =Dechtiar and Nepszy (1988); 7 =Dechtiar (1972); 8 = Bangham (1972); 9 = Bangham and Hunter (1939); 10 = Wolfert et al. (1967); 11 = Cooper (1919); 12 = Hunter and Bangham (1933); 13 = Connor (1943); 14 = Stromberg and Crites (1975). * denotes larval or immature stages. A =gills, B =gastrointestinal tract, C =skin and muscle, D = eye, E = blood, F = mesenteries and viscera, ? = unknown. Dash =parasite not found. (N = total number of fish examinedfrom each lake.)
Parasite Monogenea Urocleidus aculeatus Gyrodactyloidea
Site of Infection
Lake Superior (N = 15)
A A
Digenea Azygia angusticauda B Azygia sp. B Centrovarium lobotes B Crassiphalia bulboglossa * C Cryptogonimus chyli B D Diplostomum spathaceum * D Diplostomum sp. * Neascus vancleavi * ? ? Neascus sp. * Prosthorhynchoides pusilla B Bucephalidae B Sanguinicola occidentalis E F Tetracotyle diminuta * F Tetracotyle sp. * Uvulifer ambloplitis * C Cestoda Bothriocephalus claviceps B Bothriocephalus cuspidatus B Proteocephalus ambloplitis * F Proteocephalus stizostethi B Proteocephalus sp. B Triaenophorus nodulosus * ? Triaenophorus stizostedionis B F Triaenophorus sp. * Nematoda Camallanus oxycephalus B Dichelyne cotylophora B C,F Eustrongylides tubifex * Hysterothylacium brachyurum B Hysterothylacium brachyurum * F Spinitectus gracilis ? Unidentified nematode ? Acanthocephala Echinorhynchus salmonis B Leptorhynchoides thecatus B Neoechinorhynchus cylindratus B Neoechinorhynchus rutili B Neoechinorhynchus tene/lus B Unidentified acanthocephala ?
Lake Huron (N = 133)
Lake Ontario (N = 37)
Lake Erie (N:= 193)
2,3
5
6, 7 8
5
9
4 4 2 4 2 3
1 1
2 3 3
4 2,3
9,8,6
5
6 8 9 9, 8 9,8,10
5
7, 8
5 5
6
5
6,8,9,10,11 9,8 9, 8, 6, 12, 13
5 5
2 3,4 4
5
9,8,14
4 3 2,4
8 8 9
5 5 5 5 9 10
4
5 5 6
4
5 5
6, 7 9 Continued
157
Parasites of Walleyes from the Great Lakes TABLE 3.
Continued Site of Infection
Parasite Copepoda Ergasilus caeruleus Ergasilus centrarchidarum Ergasilus luciopercarum Hirudinea Myzobdella moorei Mollusca G10chidia Protozoa Myxobolus sp. Trichodina sp. Virus Lymphocystis
Lake Superior (N = 15)
A A A
1
Lake Ontario (N = 37)
Lake Erie (N = 193)
2
5
2, 3
5
9,8,6 9 6 6, 7
C A
5
F
8
5
A
3
C
1
TABLE 4. Jaccard's index of community similarity based on presence of parasite species reported from Stizostedion vitreum in each lake. (See Table 3 for the parasite species used in these calculations.) No data from Lake Michigan. Lake
Lake Huron (N = 133)
Huron
Erie
Ontario
Superior
0.28
0.19
0.30
Huron
1.00
0.36
0.44
Erie
0.36
1.00
0.38
2, 3
5
8,6
fishes. However, the parasite faunas of walleyes and salmonines are similar in that they harbor a large number (percentage) of helminth species that are autogenic, meaning that they mature in (or on) their respective walleye and salmonine hosts. The dominance of these helminth species is attributable to the position of these fishes in the food web as top predators in their respective habitats in the Great Lakes. ACKNOWLEDGMENTS We thank Jim Johnson, Michigan Department of Natural Resources, Alpena, Michigan, for providing walleyes and Jan VanAmberg for aging them.
monly discarded by anglers. Lesions of this disease are raised nodular masses or wart-like growths of generally light-colored tissue. Mrozinski et aZ. (1991) provided data that suggested lymphocystis had little or no effect on walleye survival and that infected fish may recover in Saginaw Bay. The parasite fauna of walleye is different from the parasite faunas of forage fish, i.e., alewife, AZosa pseudoharengus, (see Muzzall 1994) and emerald shiners, Notropis atherinoides, (see Muzzall and Peebles 1987) in the Great Lakes. Forage fish harbor large numbers of larval and immature helminths that are allogenic, meaning they mature in piscivorous fishes and birds. The parasite fauna of walleye is also different from those of Great Lakes salmonines (Muzzall 1995a, 1995b) in that many parasite species are not shared between these
REFERENCES Amin, o. M. 1992. Cestoda from lake fishes in Wisconsin: the ecology and interspecific relationships of bothriocepha1id cestodes in walleye, Stizostedion vitreum. J. Helminthol. Soc. Wash. 59:76-82. Bangham, R. V. 1972. A resurvey of the fish parasites of western Lake Erie. Bull. Ohio BioI. Surv. 4: 1-23. _ _, and Hunter, G. W., III. 1939. Studies on fish parasites of Lake Erie. Distribution studies. Zoologica 24:385-448. Brower, J. E., and Zar, J. H. 1984. Field and Laboratory Methods for General Ecology, 2 nd ed. William C. Brown Publishers, Dubuque, Iowa. Connor, R. S. 1943. A study of the seasonal cycle of a proteocepha1an cestode, Proteocephalus stizostethi Hunter and Bangham, found in the yellow pikeperch, Stizostedion vitreum (Mitchill). J. Parasitol. 39:621-624.
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Cooper, A. R. 1919. North American Pseudophyllidean cestodes from fishes. Ill. Bioi. Monogr. 4:289-54l. Dechtiar, A. O. 1972. New parasite records for Lake Erie fish. Great Lakes Fish. Comm., Tech. Rep. 17. _ _, and Christie, W. J. 1988. Survey of the parasite fauna of Lake Ontario fishes, 1961 to 1971. Great Lakes Fish. Comm., Tech. Rep. 51:66-106. _ _, and Lawrie, A. H. 1988. Survey of the parasite fauna of Lake Superior fishes, 1969 to 1975. Great Lakes Fish. Comm., Tech. Rep. 51:1-18. ___, and Nepszy, S. J. 1988. Survey of the parasite fauna of selected fish species from Lake Erie, 1970-1975. Great Lakes Fish. Comm., Tech. Rep. 51:49-65. _ _, Collins, J. J., and Reckahn, J. A. 1988. Survey of the parasite fauna of Lake Huron fishes, 1967 to 1971. Great Lakes Fish. Comm., Tech. Rep. 51: 19-48. Essex, H. E. 1928. On the life history of Bothriocephalus cuspidatus Cooper, 1917, a tapeworm of the walleyed pike. Trans. Amer. Microsc. Soc. 47:348-355. Haas, R. c., and Schaeffer, J. S. 1992. Predator-prey and competitive interactions among walleye, yellow perch, and other forage fishes in Saginaw Bay, Lake Huron. Michigan Department of Natural Resources, Fisheries Research Report No. 1984. Hudson, P. L., Bowen, C. A., II, and Stedman, R. A. 1994. New records of Ergasilus (Copepoda: Ergasilidae) in the Laurentian Great Lakes, including a lake wide review of records and host associations. Can. J. Zool.72:1002-1009. Hunter, G. W., III, and Bangham, R. V. 1933. Studies on fish parasites of Lake Erie. II. New Cestoda and Nematoda. J. Parasitol. 19:304-31l. Mrozinski, L. E., Schneider, J. c., Haas, R. c., and
Shepherd, R. E. 1991. Rehabilitation of walleye in Saginaw Bay, Lake Huron, In Status of walleye in the Great Lakes: case studies prepared for the 1989 workshop, pp. 63-84, ed. P.J. Colby, C.A. Lewis, and R.L. Eshenroder, Great Lakes Fisheries Commission, Spec. Pub. No. 91-l. Muzzall, P. M. 1984. Helminths of fishes from the St. Marys River, Michigan. Can. J. Zool. 62:516-519. _ _. 1994. Parasites of alewives, Alosa pseudoharengus, from the Great Lakes. J. Helminthol Soc. Wash. 61:67-72. ___ . 1995a. Parasites of pacific salmon, Oncorhynchus spp., from the Great Lakes. J. Great Lakes Res. 21:248-256. _ _. 1995b. Parasites of lake trout, Salvelinus namaycush, from the Great Lakes. J. Great Lakes Res. 21 :594-598. _ _, and Peebles, C. R. 1987. Parasites of the emerald shiner, Notropis atherinoides, from two localities in the St. Marys River, Michigan, with emphasis on larval trematodes. Proc. Helminthol. Soc. Wash. 54: 105-11 O. Stromberg, P. c., and Crites, J. L. 1975. An analysis of the changes in the prevalence of Camallanus oxycephalus (Nematoda: Camallanidae) in western Lake Erie. Ohio J. Sci. 75: 1-6. Wolfert, D. R., Applegate, V. c., and Allison, L. A. 1967. Infection of the walleye, Stizostedion vitreum, of western Lake Erie with Bothriocephalus cuspidatus (Cooper). Pap. Mich. Acad. Sci., Arts, and Lett. 52:105-114. Submitted: 27 March 1997 Accepted: 2 December 1997 Editorial handling: David J. Jude
NOTE Parasites of Walleyes, Stizostedion vitreum, from Saginaw Bay, Lake Huron, and the Other Great Lakes Patrick M. Muzzall 1* and Robert C. Haas2 1Department
ofZoology Natural Science Building Michigan State University East Lansing, Michigan 48824 2Michigan Department ofNatural Resources Mt. Clemens Fisheries Station 33135 South River Road Mount Clemens, Michigan 48045 ABSTRACT.
A total of 79 walleyes, Stizostedion vitreum (Percidae), was collected from inner and outer Saginaw Bay, Lake Huron, in September 1993 and 1994 and examined for parasites. Nine parasite species (one Monogenea, two Digenea, two Cestoda, one Nematoda, one Copepoda, one Protozoa, one virus) infected walleyes from the bay. The copepod Ergasilus luciopercarum had the highest prevalence and mean intensity followed by the cestode Bothriocephalus cuspidatus. Of the helminth species found, only B. cuspidatus and the monogenean Urocleidus aculeatus were gravid. Walleye parasite faunas were similar between areas. Walleyes from the Great Lakes have had 46 parasites species recorded. Walleye is a definitive host for many parasite species but does not play an important role as an intermediate and transport host for parasites in the Great Lakes.
INDEX WORDS: Walleye, Stizostedion vitreum, Percidae, parasites, Saginaw Bay, Lake Huron.
community of walleyes in Saginaw Bay so that changes brought about by environmental variation and exotic fish and invertebrate introductions can be understood. The objectives of the present study were to provide information on the occurrence and abundance of parasites of walleyes from inner and outer Saginaw Bay, Lake Huron and to summarize and compare the known information about parasites infecting this species in the Great Lakes.
INTRODUCTION
The walleye, Stizostedion vitreum, is an extremely popular fish and a substantial sport fishery has been created in Saginaw Bay, Lake Huron (Mrozinski et al. 1991). Several studies have investigated the parasites of walleyes in the Great Lakes; however, little is known about their parasites in Saginaw Bay. The aquatic environment and prey fish community of Saginaw Bay will undergo major changes following colonization by exotic species such as the white perch (Morone americana), round goby (Neogobius melanostomus), ruffe (Gymnocephalus cernuus), spiny water flea (Bythotrephes cederstroem i), and zebra mussel (Dreissena polymorpha). It is important to document the parasite
METHODS
Walleyes were collected by gill net from Saginaw Bay, which is the southwestern extension of Lake Huron located in east central Michigan. It is a large, shallow, eutrophic bay divided into inner and outer areas. The inner area, with a mean depth of 4.6 m, is shallower and warmer than the outer area, and is enriched with domestic, agricultural, and industrial inputs from the Saginaw River. Haas and Schaeffer
'Corresponding author. E-mail: [email protected]
152
Parasites of Walleyes from the Great Lakes
153
TABLE 1. Mean lengths (mm), weights (kg), ages (ranges), and 95% confidence intervals of Stizostedion vitreum examined from inner and outer areas of Saginaw Bay, Lake Huron, in September 1993 and 1994. (N =number of walleyes examined.)
Mean leanth ± S.D. (range, 95% confidence interval)
Mean weight ± S.D. (range, 95% confidence interval
Mean age ± S.D. (range, 95% confidence interval)
Inner Saginaw Area (N=47)
457 ± 89 (305-599, 431 -483)
1.0 ± 0.6 (0.3-2.2, 0.9-1.2)
3.4 ± 1.8 (1-8,2.8-3.9)
Outer Saginaw Area (N=32)
513 ± 58 (350-622,492-534)
1.3 ± 0.5 (0.3-2.4, 1.1-1.5)
4.8 ± 1.5 (1-8,4.2-5.3)
Location
(1992) described the fish community of Saginaw Bay in detail. Walleyes were examined from two locations in the Inner Saginaw Area: The Black Hole (latitude, longitude; 43°48'06", 83°51'42") and Carreon Reef (43°43'12", 83°43'12") and from two locations in the Outer Saginaw Area: Au Gres (43°58'58", 83°39'37") and Oak Point (43°59'12", 83°18'00"). Fish were measured, weighed, and tagged in the field, put on ice, and then frozen. Skin, fins, gills, eyes, kidney, gonads, heart, spleen, liver, gall bladder, mesentery, esophagus, and gastrointestinal tract were examined. Parasites were collected and processed using routine procedures. Prevalence was calculated as percentage of fish infected and mean intensity as mean number of parasites per infected fish. Prevalence was only calculated for Urocleidus aculeatus and Trichodina sp. Additional information on the parasites of walleyes was obtained from examining published studies performed in the Great Lakes. Data on walleyes from the St. Marys River, which connects Lake Superior and Lake Huron, are included with Lake Huron. Species richness refers to the number of parasite species infecting walleyes from each Great Lake. The Jaccard coefficient of community similarity (CC) was calculated as
where Sl and S2 are the number of parasite species in communities 1 and 2 , respectively, and C is the number of species common to both communities (Brower and Zar 1984). For calculations of the Jaccard coefficient of community similarity and species richness, Diplostomum (present study) and
Diplostomulum in other studies were considered to be a single species.
RESULTS Walleyes from four locations in Saginaw Bay were infected with one or more parasites (Table 1). Fish from the outer area were larger than those from the inner area. Nine parasite species (nine from the inner area and seven from the outer area) infected walleyes from the bay (Table 2). Ergasilus luciopercarum Henderson, 1926 had the highest prevalence and mean intensity in both areas. There were significant negative relationships between walleye length (r = -0.73, P < 0.01), weight (r = -0.64, P < 0.01), and age (r = -0.60, P < 0.01) with the intensities of E. luciopercarum from the inner area. The nonsignificant relationships between E. luciopercarum intensities and host length, weight, and age from the outer area were positive, negative, and negative, respectively. Percentages of E. luciopercarum with egg sacs from the inner and outer areas were 6.3% and 1.1 %, respectively. Bothriocephalus cuspidatus Cooper, 1917 was the next most common parasite of walleyes from both areas. The relationships of B. cuspidatus intensities and host length, weight, and age from the inner area were negative, while these relationships from the outer area were positive; all relationships were nonsignificant. There were no significant differences in the prevalences (Chi-square analyses, P > 0.05) and intensities (Mann-Whitney U test, P > 0.05) of E. luciopercarum and B. cuspidatus between areas. Of the helminth species found, only B. cuspidatus and Urocleidus aculeatus (Van Cleave and Mueller, 1932) Mueller, 1934 were gravid. Urocleidus aculeatus infected a significantly larger percentage of walleyes from the inner
154
Muzzall and Haas
TABLE 2. Prevalence (P), mean intensity (MI), and maximum number of parasites (max.) found in Stizostedion vitreumfrom inner (N = 47) and outer (N =32) Saginaw Bay, Lake Huron, in September 1993 and 1994. * denotes larval or immature stages. NC =parasite present but mean intensity not calculated. Dash
=parasite not found.
Parasite Monogenea Urocleidus aculeatus
P(%)
Inner MI ± SD (max.)
Outer MI ± SD (max.) Site
P(%)
62
NC
34
NC
Gills
2 2
4(4) 1(1)
3
1(1)
Lens Stomach
96
84
12.9 ± 19.3 (104)
2
16.1 ± 15.9 (52) 1(1)
2
3(3)
3
2(2)
96
46.2 ± 50.1 (203)
100
42.8 ± 30.2 (115)
Gills
9
NC
19
NC
Gills
11
NC
6
NC
Fins, skin
Digenea
Diplostomum sp. *
Bucephalidae Cestoda Bothriocephalus cuspidatus Proteocephalus sp. *
Anterior intestine, pyloric ceca Encysted in liver
Nematoda Eustrongylides tubifex*
Encysted in mesentery
Copepoda Ergasilus luciopercarum
Protozoa Trichodina sp. Virus Lymphocystis
area than from the outer area (X 2 = 4.25, P < 0.05). Mean lengths ± SD of walleyes infected with U. aculeatus from the inner and outer areas were 455 mm ± 82 and 501 mm ± 31, respectively. Other parasite species infrequently infected walleyes. The two bucephalid trematodes could not be identified beyond family due to their poor condition. The Eustrongylides tubifex found in walleye were in poor condition. There were no significant differences in prevalence (Chi-square analyses, P> 0.05) or intensity (Mann-Whitney U test, P > 0.05) of parasitism between female and male walleyes from each area. Jaccard's coefficient of similarity for the parasite faunas, including lymphocystis, of walleyes from the inner and outer areas was 0.77. Mean parasite species richness ± SD, range, and 95% confidence intervals in walleyes from the inner area (2.8 ± 0.77,1 to 4,2.58 to 3.04) and from the outer area (2.5 ± 0.76, I to 4, 2.23 to 2.78) were not significantly different (Mann-Whitney U test, P > 0.05). Fifty-seven percent (N = 27) of the walleyes from the inner area were concurrently infected with E. luciopercarum, B. cuspidatus, and U. aculeatus; whereas, 22 percent (N = 7) from the
outer area were concurrently infected with these specIes.
DISCUSSION Ergasilus luciopercarum was the most common parasite species infecting walleyes from Saginaw Bay, followed by Bothriocephalus cuspidatus and then Urocleidus aculeatus. The parasite faunas of walleyes from the inner and outer areas were very similar suggesting that these walleyes are not from separate populations. The similar and low mean parasite species richness values in these walleyes from the areas also support this. Furthermore, tagging studies indicate there is some interchange with walleyes from Lake St. Clair and Lake Erie (Mrozinski et a1. 1991). The gill parasites, E. luciopercarum and U. aculeatus, have direct life cycles. The mean intensity of E. luciopercarum and prevalence of U. aculeatus were highest on walleyes from the inner area. This higher mean intensity of E. luciopercarum may be due to smaller, younger fish examined from this area since significant negative relationships occurred between intensities and host size and age.
Parasites of Walleyes from the Great Lakes The difference in the percentage of E. luciopercarum with egg sacs on walleyes between areas may be temperature related with more copepods maturing and retaining their egg sacs on hosts for a longer period of time in the warmer inner area. Bothriocephalus cuspidatus has an indirect life cycle. Essex (1928) reported that larvae of this cestode species develop in the coelom of Cyclops spp. and a second intermediate host was not needed. He suggested small B. cuspidatus infect adults either through infected copepods being strained directly from the water and ingested by walleyes or through the ingestion of small fish that had recently eaten infected copepods. Amin (1992) proposed that infected prey fish species play a role in transmitting B. cuspidatus to walleyes. Four yellow perch, Perca flavescens, from Saginaw Bay were infected with small Bothriocephalus (Muzzall, unpubl. data), supporting the suggestion that it uses a transport host. Haas and Schaeffer (1992) reported that walleyes feed on yellow perch in Saginaw Bay. Wolfert et al. (1967) reported that large numbers of B. cuspidatus caused the ceca of Lake Erie walleyes to become greatly distended, but no inflammation was noted. They noted that the largest number of B. cuspidatus had no detrimental effect on walleye weights and suggested (p. 112) "The greater incidence of worms in the 'fatter' walleyes must have resulted from a greater degree of exposure to infection, i.e., the more successful a fish was in capturing food, the greater numbers of parasitized prey it consumed." The parasite faunas of walleyes and yellow perch, collected in September from different years from the same Saginaw Bay location, differed. Over 10 parasite species infected yellow perch examined by PMM in September 1991, with Eustrongylides tubifex and Proteocephalus plerocercoids being most common. Haas and Schaeffer (1992) reported that walleye and yellow perch differed in their diet in the inner area, with walleyes primarily piscivorous and yellow perch primarily consuming chironomid larvae and zooplankton. The parasite species richness of walleyes from each Great Lake from the literature was: Lake Superior-8 (Dechtiar and Lawrie 1988); Lake Huron11 (Dechtiar et al. 1988), 9 (present study); Lake Erie-19 (Bangham and Hunter 1939), 3 (Wolfert et al. 1967), 15 (Bangham 1972), 22 (Dechtair and Nepszy 1988), and Lake Ontario-21 (Dechtiar and Christie 1988). A total of 46 parasite species (2 Monogenea, 15 Digenea, 8 Cestoda, 7 Nematoda, 6 Acantho-
ISS
cephala, 3 Crustacea, 1 Hirudinea, 1 Mollusca, 2 Protozoa, 1 virus) has been reported from walleyes in the Great Lakes (Table 3). The number of studies and number of fish examined for parasites from each Great Lake vary dramatically. The number of walleyes examined from Lake Erie is represented only by parasite surveys and include Bangham and Hunter (1939), Bangham (1972), Dechtiar (1972), and Dechtiar and Nepszy (1988) (Table 3). Studies on walleye parasites from Lake Michigan have not been published. Eight parasite species have been reported from walleyes in Lake Superior, 24 from Lake Huron including 9 from Saginaw Bay, 23 from Lake Ontario, and 29 from walleyes in Lake Erie. Urocleidus aculeatus, Sanguinicola occidentalis, B. cuspidatus, Neoechinorhynchus teneZlus, E. luciopercarum, and lymphocystis have been reported from walleyes in all these Great Lakes. Of the 37 helminth species reported, 24 (65%) are represented as adults. The distribution and percentage of parasites (where data were provided) by host site were: gastrointestinal tract, 47.5%; gills, 17.5%; mesentery and viscera, 15%; skin and muscle, 12.5%; eye, 5%; and blood, 2.5%. These studies on the parasites of walleyes demonstrate that B. cuspidatus is the most common gastrointestinal parasite of walleyes in each Great Lake. This indicates that one or more of the copepod first intermediate hosts is common and that the piscivorous diet of walleyes exposes them to infected fish transport hosts in each Great Lake. Also, E. luciopercarum or U. aculeatus is consistently the most common external parasite of walleyes in each lake. Ergasilus luciopercarum has been reported from a variety of fish hosts in the Great Lakes (Hudson et al. 1994). Jaccard's coefficient of similarity for the parasite faunas in walleyes from the Great Lakes were lowest in comparisons involving Lake Superior (Table 4). The lowest one involved walleyes from this lake and Lake Erie. Walleyes from Lakes Huron and Ontario had the highest coefficient indicating that they shared the most parasite species. Ergasilus luciopercarum and the virus that causes lymphocystis are considered to be pathogens of Great Lakes walleyes. Dechtiar and Nepszy (1988) and Dechtiar and Christie (1988) reported that feeding and the movements of E. luciopercarum on the gills of walleyes from Lakes Erie and Ontario caused destruction, hemorrhaging, hyperplasia, and hypertrophy of the filaments. The prevalence of lymphocystis on walleyes may be high in some Great Lakes locations and affected fish are com-
156
Muzzall and Haas
TABLE 3. Reported parasites of Stizostedion vitreum from the Great Lakes. Data were taken from the following studies: 1 =Dechtiar and Lawrie (1988); 2 =Dechtiar et al. (1988); 3 =present study, Saginaw Bay; 4 =Muzzall (1984); 5 =Dechtiar and Christie (1988); 6 =Dechtiar and Nepszy (1988); 7 =Dechtiar (1972); 8 = Bangham (1972); 9 = Bangham and Hunter (1939); 10 = Wolfert et al. (1967); 11 = Cooper (1919); 12 = Hunter and Bangham (1933); 13 = Connor (1943); 14 = Stromberg and Crites (1975). * denotes larval or immature stages. A =gills, B =gastrointestinal tract, C =skin and muscle, D = eye, E = blood, F = mesenteries and viscera, ? = unknown. Dash =parasite not found. (N = total number of fish examinedfrom each lake.)
Parasite Monogenea Urocleidus aculeatus Gyrodactyloidea
Site of Infection
Lake Superior (N = 15)
A A
Digenea Azygia angusticauda B Azygia sp. B Centrovarium lobotes B Crassiphalia bulboglossa * C Cryptogonimus chyli B D Diplostomum spathaceum * D Diplostomum sp. * Neascus vancleavi * ? ? Neascus sp. * Prosthorhynchoides pusilla B Bucephalidae B Sanguinicola occidentalis E F Tetracotyle diminuta * F Tetracotyle sp. * Uvulifer ambloplitis * C Cestoda Bothriocephalus claviceps B Bothriocephalus cuspidatus B Proteocephalus ambloplitis * F Proteocephalus stizostethi B Proteocephalus sp. B Triaenophorus nodulosus * ? Triaenophorus stizostedionis B F Triaenophorus sp. * Nematoda Camallanus oxycephalus B Dichelyne cotylophora B C,F Eustrongylides tubifex * Hysterothylacium brachyurum B Hysterothylacium brachyurum * F Spinitectus gracilis ? Unidentified nematode ? Acanthocephala Echinorhynchus salmonis B Leptorhynchoides thecatus B Neoechinorhynchus cylindratus B Neoechinorhynchus rutili B Neoechinorhynchus tene/lus B Unidentified acanthocephala ?
Lake Huron (N = 133)
Lake Ontario (N = 37)
Lake Erie (N:= 193)
2,3
5
6, 7 8
5
9
4 4 2 4 2 3
1 1
2 3 3
4 2,3
9,8,6
5
6 8 9 9, 8 9,8,10
5
7, 8
5 5
6
5
6,8,9,10,11 9,8 9, 8, 6, 12, 13
5 5
2 3,4 4
5
9,8,14
4 3 2,4
8 8 9
5 5 5 5 9 10
4
5 5 6
4
5 5
6, 7 9 Continued
157
Parasites of Walleyes from the Great Lakes TABLE 3.
Continued Site of Infection
Parasite Copepoda Ergasilus caeruleus Ergasilus centrarchidarum Ergasilus luciopercarum Hirudinea Myzobdella moorei Mollusca G10chidia Protozoa Myxobolus sp. Trichodina sp. Virus Lymphocystis
Lake Superior (N = 15)
A A A
1
Lake Ontario (N = 37)
Lake Erie (N = 193)
2
5
2, 3
5
9,8,6 9 6 6, 7
C A
5
F
8
5
A
3
C
1
TABLE 4. Jaccard's index of community similarity based on presence of parasite species reported from Stizostedion vitreum in each lake. (See Table 3 for the parasite species used in these calculations.) No data from Lake Michigan. Lake
Lake Huron (N = 133)
Huron
Erie
Ontario
Superior
0.28
0.19
0.30
Huron
1.00
0.36
0.44
Erie
0.36
1.00
0.38
2, 3
5
8,6
fishes. However, the parasite faunas of walleyes and salmonines are similar in that they harbor a large number (percentage) of helminth species that are autogenic, meaning that they mature in (or on) their respective walleye and salmonine hosts. The dominance of these helminth species is attributable to the position of these fishes in the food web as top predators in their respective habitats in the Great Lakes. ACKNOWLEDGMENTS We thank Jim Johnson, Michigan Department of Natural Resources, Alpena, Michigan, for providing walleyes and Jan VanAmberg for aging them.
monly discarded by anglers. Lesions of this disease are raised nodular masses or wart-like growths of generally light-colored tissue. Mrozinski et aZ. (1991) provided data that suggested lymphocystis had little or no effect on walleye survival and that infected fish may recover in Saginaw Bay. The parasite fauna of walleye is different from the parasite faunas of forage fish, i.e., alewife, AZosa pseudoharengus, (see Muzzall 1994) and emerald shiners, Notropis atherinoides, (see Muzzall and Peebles 1987) in the Great Lakes. Forage fish harbor large numbers of larval and immature helminths that are allogenic, meaning they mature in piscivorous fishes and birds. The parasite fauna of walleye is also different from those of Great Lakes salmonines (Muzzall 1995a, 1995b) in that many parasite species are not shared between these
REFERENCES Amin, o. M. 1992. Cestoda from lake fishes in Wisconsin: the ecology and interspecific relationships of bothriocepha1id cestodes in walleye, Stizostedion vitreum. J. Helminthol. Soc. Wash. 59:76-82. Bangham, R. V. 1972. A resurvey of the fish parasites of western Lake Erie. Bull. Ohio BioI. Surv. 4: 1-23. _ _, and Hunter, G. W., III. 1939. Studies on fish parasites of Lake Erie. Distribution studies. Zoologica 24:385-448. Brower, J. E., and Zar, J. H. 1984. Field and Laboratory Methods for General Ecology, 2 nd ed. William C. Brown Publishers, Dubuque, Iowa. Connor, R. S. 1943. A study of the seasonal cycle of a proteocepha1an cestode, Proteocephalus stizostethi Hunter and Bangham, found in the yellow pikeperch, Stizostedion vitreum (Mitchill). J. Parasitol. 39:621-624.
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Cooper, A. R. 1919. North American Pseudophyllidean cestodes from fishes. Ill. Bioi. Monogr. 4:289-54l. Dechtiar, A. O. 1972. New parasite records for Lake Erie fish. Great Lakes Fish. Comm., Tech. Rep. 17. _ _, and Christie, W. J. 1988. Survey of the parasite fauna of Lake Ontario fishes, 1961 to 1971. Great Lakes Fish. Comm., Tech. Rep. 51:66-106. _ _, and Lawrie, A. H. 1988. Survey of the parasite fauna of Lake Superior fishes, 1969 to 1975. Great Lakes Fish. Comm., Tech. Rep. 51:1-18. ___, and Nepszy, S. J. 1988. Survey of the parasite fauna of selected fish species from Lake Erie, 1970-1975. Great Lakes Fish. Comm., Tech. Rep. 51:49-65. _ _, Collins, J. J., and Reckahn, J. A. 1988. Survey of the parasite fauna of Lake Huron fishes, 1967 to 1971. Great Lakes Fish. Comm., Tech. Rep. 51: 19-48. Essex, H. E. 1928. On the life history of Bothriocephalus cuspidatus Cooper, 1917, a tapeworm of the walleyed pike. Trans. Amer. Microsc. Soc. 47:348-355. Haas, R. c., and Schaeffer, J. S. 1992. Predator-prey and competitive interactions among walleye, yellow perch, and other forage fishes in Saginaw Bay, Lake Huron. Michigan Department of Natural Resources, Fisheries Research Report No. 1984. Hudson, P. L., Bowen, C. A., II, and Stedman, R. A. 1994. New records of Ergasilus (Copepoda: Ergasilidae) in the Laurentian Great Lakes, including a lake wide review of records and host associations. Can. J. Zool.72:1002-1009. Hunter, G. W., III, and Bangham, R. V. 1933. Studies on fish parasites of Lake Erie. II. New Cestoda and Nematoda. J. Parasitol. 19:304-31l. Mrozinski, L. E., Schneider, J. c., Haas, R. c., and
Shepherd, R. E. 1991. Rehabilitation of walleye in Saginaw Bay, Lake Huron, In Status of walleye in the Great Lakes: case studies prepared for the 1989 workshop, pp. 63-84, ed. P.J. Colby, C.A. Lewis, and R.L. Eshenroder, Great Lakes Fisheries Commission, Spec. Pub. No. 91-l. Muzzall, P. M. 1984. Helminths of fishes from the St. Marys River, Michigan. Can. J. Zool. 62:516-519. _ _. 1994. Parasites of alewives, Alosa pseudoharengus, from the Great Lakes. J. Helminthol Soc. Wash. 61:67-72. ___ . 1995a. Parasites of pacific salmon, Oncorhynchus spp., from the Great Lakes. J. Great Lakes Res. 21:248-256. _ _. 1995b. Parasites of lake trout, Salvelinus namaycush, from the Great Lakes. J. Great Lakes Res. 21 :594-598. _ _, and Peebles, C. R. 1987. Parasites of the emerald shiner, Notropis atherinoides, from two localities in the St. Marys River, Michigan, with emphasis on larval trematodes. Proc. Helminthol. Soc. Wash. 54: 105-11 O. Stromberg, P. c., and Crites, J. L. 1975. An analysis of the changes in the prevalence of Camallanus oxycephalus (Nematoda: Camallanidae) in western Lake Erie. Ohio J. Sci. 75: 1-6. Wolfert, D. R., Applegate, V. c., and Allison, L. A. 1967. Infection of the walleye, Stizostedion vitreum, of western Lake Erie with Bothriocephalus cuspidatus (Cooper). Pap. Mich. Acad. Sci., Arts, and Lett. 52:105-114. Submitted: 27 March 1997 Accepted: 2 December 1997 Editorial handling: David J. Jude