Parasites of Fish from the Great Lakes - Great Lakes Fishery ...

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species), Neoechinorhynchus crassus (primarily catostomids), N. cylindratus (several species), Octospinifer macilentus (catostomids), Pomphorhynchus bulbocolli (several species); copepods— Achtheres pimelodi (several species), Ergasilus caeruleus (several species), and E. luciopercarum (several species). Possible reasons why these parasites have been reported from all the lakes are that most parasites, except for Zschokkella sp. and Urocleidus adspectus, infected two or more fish species so they lack strict host specificity; and, if host specificity occurs, the specific fish host is present and has been examined from all the lakes. At least 23 of these parasite species have indirect life cycles, indicating that the necessary intermediate host species are present in all the lakes. All the helminth species listed above are autogenic species, except for two allogenic species, Clinostomum complanatum and Diplostomum spathaceum. Diplostomum spathaceum or unidentified species of Diplostomum infected the most fish species in Lakes Huron, Erie, and Ontario, followed by Echinorhynchus salmonis in Lake Huron, Camallanus oxycephalus in Lake Erie, and E. salmonis in Lake Ontario. Diplostomum spp. are allogenic species as well as generalist parasites in that they can infect a large number of fish species as the second intermediate hosts and several piscivorous bird species as definitive hosts. Thus, they lack host specificity. Echinorhynchus salmonis infected the most fish species in Lakes Michigan and Superior followed by Acanthocephalus dirus in Lake Michigan, and Diplostomum spathaceum in Lake Superior. Echinorhynchus salmonis, an autogenic species, infected the most fish species in these lakes because of the various transmission pathways employed in its life cycle as well as it being a generalist parasite. Also, the first intermediate host, Diporeia affinis of E. salmonis, is probably numerous in these two lakes. Camallanus oxycephalus, an autogenic species, was the second most-common parasite infecting fish species in Lake Erie. Stromberg and Crites (1975b) reported that the prevalence of C. oxycephalus in fish from the western basin of Lake Erie showed little change in fish surveys between 1927 and 1957. However between 1957 and 1972, the prevalence of C. oxycephalus increased in fish, with significant increases in 11 fish species. Stromberg and Crites (1975b) suggested that reasons for this increase were increased numbers of its copepod intermediate host and faster movement of this nematode through the forage fish to the predaceous fish portion of their life cycle. Furthermore, Crites (1976) demonstrated that C. oxycephalus could establish in many fish that ingested the encapsulated larvae. A total of 49 parasite species or distinct genera were reported from four of the five Great Lakes. These parasites by major taxonomic group, fish species infected, and lake where the parasite species was not reported (in parentheses) were protozoans—Ichthyophthirius multifiliis (several fish species, Lake Michigan), Henneguya doori (Perca flavescens, Lake Superior), H. exilis (ictalurids, Lake Superior), Myxobolus bartai (Notropis hudsonius, Lake Superior), M. bibullatum (cyprinids and catostomids, Lake Superior); digenetic trematodes—Acetodextra amiuri (ictalurids, Lake Superior), Azygia angusticauda (several species, Lake Superior), Crepidostomum cornutum (several species, Lake Michigan), C. isostomum (Percopsis omiscomaycus, Etheostoma nigrum, Percina caprodes, Lake Michigan), Crepidostomum lintoni (Acipenser fulvescens, Lake Michigan), Phyllodistomum superbum (several species, Lake Ontario), Proterometra macrostoma (centrarchids, Lake Michigan), Sanguinicola occidentalis 520
(Sander vitreus, Perca flavescens, Aplodinotus grunniens, Lake Michigan), Apophallus brevis (several species, Lake Michigan), Crassiphiala bulboglossa (several species, Lake Michigan), Posthodiplostomum minimum (several species, Lake Michigan), Tylodelphys scheuringi (several species, Lake Michigan), Uvulifer ambloplitis (several species, Lake Michigan); monogeneans— Acolpenteron catostomi (catostomids, Lake Michigan), Anonchohaptor anomalus (catostomids, Lake Michigan), Diclybothrium armatum (A. fulvescens, Lake Michigan), Lyrodiscus rupestris (primarily Ambloplites rupestris, Lake Michigan), Octomacrum lanceatum (catostomids, Lake Michigan), Pseudomurraytrema copulatum (catostomids, Lake Michigan), Tetracleidus banghami (Micropterus dolomieu, Lake Michigan), Tetraonchus monenteron (Esox lucius, Lake Michigan), Urocleidus aculeatus (Sander spp., Lake Michigan); cestodes—Corallobothrium fimbriatum (ictalurids, Lake Michigan), Cyathocephalus truncatus (several species, Lake Erie), Eubothrium salvelini (coregonids and salmonids, Lake Erie), Diphyllobothrium laruei (Coregonus spp., Lake Michigan), Ligula intestinalis (several species, Lake Michigan); nematodes—Capillaria salvelini (coregonids and salmonids, Lake Erie), Cystidicola farionis (coregonids, salmonids, and Osmerus mordax, Lake Erie), Cystidicola stigmatura (coregonids, salmonids, and Osmerus mordax, Lake Ontario), Cystidicoloides ephemeridarum (coregonids and salmonids, Lake Michigan), Hysterothylacium brachyurum (several species, Lake Michigan), Philometroides nodulosa (primarily catostomids, Lake Michigan), Spinitectus carolini (several species, Lake Michigan), Eustrongylides tubifex (several species, Lake Superior), Spiroxys sp. (several species, Lake Michigan); acanthocephalans—Neoechinorhynchus cristatus (catostomids, Lake Michigan), N. rutili (several species, Lake Michigan), N. tenellus (several species, Lake Michigan); leeches—Actinobdella inequiannulata (catostomids, Lake Michigan), Myzobdella lugubris (several species, Lake Michigan), Piscicola punctata (several species, Lake Ontario); and copepods—Ergasilus centrarchidarum (centrarchids and Sander spp., Lake Huron), Salmincola extumescens (coregonids, Lake Erie). Of these 49 parasite species, 33 species (67%) have not been reported in fish from Lake Michigan possibly due to the lack of studies, including extensive surveys on the parasites of fish from this lake. Fish-Transmitted Parasites of Public Health Importance Diphyllobothrium latum Life Cycle and Human Infection Of the larval cestodes found in fish in the Great Lakes area with human health implications, the genus Diphyllobothrium deserves comments. Its life cycle involves copepods that serve as first intermediate hosts when they ingest the coracidium stage (free-swimming stage) in the water that emerges when the egg hatches. The larval parasite moves through the intestinal wall of the copepod to the hemocoel and develops into a stage called a procercoid. The infected copepod is then ingested by a large fish that then serves as a second intermediate host (which is probably not common) that includes several species of freshwater fishes, including fish from the genera Esox, Perca, Sander, and Lota, along with fish in the Salmonidae. When a fish eats an infected copepod, the procercoid is released and moves through the intestinal wall and into the viscera or body muscle and develops into a plerocercoid stage. Large fish also become infected by eating a smaller fish that is infected with the plerocercoid stage when it eats an infected copepod. Mature plerocercoids in fish vary in length (a few millimeters to several centimeters). Plerocercoids are 521
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Parasites of Fish from the Great La
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Parasites of Fish from the Great La
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Table of Contents OVERVIEW ........
Page 7:
PREFACE There has been no comprehen
Page 10 and 11:
fish species examined and parasites
Page 12 and 13:
changed, especially some monogenean
Page 14 and 15:
Table 1, continued. Scientific name
Page 16 and 17:
Table 1, continued. Scientific name
Page 18 and 19:
most similar among fish or fish fam
Page 20 and 21:
Nematodes Ten species of adult nema
Page 22 and 23:
Fish Families—Parasite Species-Ri
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namaycush, and cyprinids. Of the 41
Page 26 and 27:
suitable host and matures. We are n
Page 28 and 29:
Table 2. Overall number, percentage
Page 30 and 31:
Table 3, continued Myxozoa (Myxospo
Page 32 and 33:
Table 3, continued. Myxobolus neuro
Page 34 and 35:
Table 3, continued. Adult Digenea (
Page 36 and 37:
Table 3, continued. Site of Infecti
Page 38 and 39:
Table 3, continued. Strigeidae Rail
Page 40 and 41:
Table 3, continued. Oncorhynchus ts
Page 42 and 43:
Table 3, continued. Diphyllobothrii
Page 44 and 45:
Table 3, continued. Host: Catostomu
Page 46 and 47:
Table 3, continued. Cystidicolidae
Page 48 and 49:
Table 3, continued. Raphidascaris a
Page 50 and 51:
Table 3, continued. Quimperiidae Ba
Page 52 and 53:
Table 3, continued. Osmerus mordax:
Page 54 and 55:
Table 3, continued. Rhadinorhynchid
Page 56 and 57:
Table 3, continued. Host: Coregonus
Page 58 and 59:
Table 3, continued. Host: Oncorhync
Page 60 and 61:
Table 5. Fishes by family and speci
Page 62 and 63:
Table 5, continued. Ictaluridae Ame
Page 64 and 65:
Table 5, continued. Coregonus spp.
Page 66 and 67:
Table 5, continued. Cottus bairdii
Page 68 and 69:
Table 5, continued. Hirudinea: Dess
Page 70 and 71:
Digenetic Trematodes This parasite
Page 72 and 73:
Fish Species—Parasite Analyses Th
Page 74 and 75:
The numbers and percentages of auto
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Cestodes Eubothrium crassum, E. rug
Page 78 and 79:
Most fish species examined for para
Page 80 and 81:
Table 8, continued. Ciliophora (Cil
Page 82 and 83:
Table 8, continued. Myxobolus burti
Page 84 and 85:
Table 8, continued. Coregonus hoyi:
Page 86 and 87:
Table 8, continued. Phyllodistomum
Page 88 and 89:
Table 8, continued. Host: Luxilus c
Page 90 and 91:
Table 8, continued. Tylodelphys sch
Page 92 and 93:
Table 8, continued. Urocleidus acul
Page 94 and 95:
Table 8, continued. Diclybothriidae
Page 96 and 97:
Table 8, continued. Tetraonchus var
Page 98 and 99:
Table 8, continued. Host: Catostomu
Page 100 and 101:
Table 8, continued. Proteocephalus
Page 102 and 103:
Table 8, continued. Host: Coregonus
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Table 8, continued. Triaenophorus n
Page 106 and 107:
Table 8, continued. Truttaedacnitis
Page 108 and 109:
Table 8, continued. Coregonus arted
Page 110 and 111:
Table 8, continued. Philonema oncor
Page 112 and 113:
Table 8, continued. Host Ambloplite
Page 114 and 115:
Table 8, continued. Coregonus arted
Page 116 and 117:
Table 8, continued. Neoechinorhynch
Page 118 and 119:
Table 8, continued. Neoechinorhynch
Page 120 and 121:
Table 8, continued. Ergasilus cotti
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Table 8, continued. Salmincola sisc
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Table 9, continued. Larval/Immature
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Table 9, continued. Esocidae Esox l
Page 128 and 129:
Table 9, continued. Coregonus kiyi
Page 130 and 131:
Table 9, continued. Larval/Immature
Page 132 and 133:
Table 9, continued. Centrarchidae A
Page 134 and 135:
Table 10. Numbers and percentages (
Page 136 and 137:
Fish Species—Parasite Analysis Tw
Page 138 and 139:
Table 12, continued. Crepidostomum
Page 140 and 141:
Table 12, continued. Cryptogonimus
Page 142 and 143:
Page 144 and 145:
Table 12, continued. Host: Esox luc
Page 146 and 147:
Table 12, continued. Spinitectus sp
Page 148 and 149:
Table 12, continued. Pomphorhynchid
Page 150 and 151:
Table 13, continued. Catostomidae C
Page 152 and 153:
Table 13, continued. Lepomis macroc
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Sixteen species of myxozoans repres
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Acanthocephalans Sixteen species of
Page 158 and 159:
The parasite group(s) (in parenthes
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(2), Ergasilus caeruleus (7), E. lu
Page 162 and 163:
Nematodes Hysterothylacium brachyur
Page 164 and 165:
Fish Families—Parasite Communitie
Page 166 and 167:
Table 14, continued. Host: Luxilus
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Table 14, continued. Myxobolus burt
Page 170 and 171:
Table 14, continued. Catostomus com
Page 172 and 173:
Table 14, continued. Host: Luxilus
Page 174 and 175:
Table 14, continued. Lepomis gibbos
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Table 14, continued. Allacanthochas
Page 178 and 179:
Table 14, continued. Phyllodistomum
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Table 14, continued. Plagioporus si
Page 182 and 183:
Table 14, continued. Diplostomidae
Page 184 and 185:
Table 14, continued. Salvelinus nam
Page 186 and 187:
Table 14, continued. Sander canaden
Page 188 and 189:
Table 14, continued. Ambloplites ru
Page 190 and 191:
Table 14, continued. Culaea inconst
Page 192 and 193:
Table 14, continued. Ligictaluridus
Page 194 and 195:
Table 14, continued. Urocleidus ala
Page 196 and 197:
Table 14, continued. Dactylogyrus d
Page 198 and 199:
Table 14, continued. Host: Coregonu
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Table 14, continued. Gyrodactylus g
Page 202 and 203:
Table 14, continued. Etheostoma nig
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Table 14, continued. Eubothrium sal
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Table 14, continued. Cottus bairdii
Page 208 and 209:
Page 210 and 211:
Table 14, continued. Larval/Immatur
Page 212 and 213:
Table 14, continued. Catostomus cat
Page 214 and 215:
Table 14, continued. Triaenophorida
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Table 14, continued. Adult Nematoda
Page 218 and 219:
Table 14, continued. Capillaria cat
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Table 14, continued. Oncorhynchus t
Page 222 and 223:
Table 14, continued. Percopsis omis
Page 224 and 225:
Table 14, continued. Rhabdochona ca
Page 226 and 227:
Table 14, continued. Raphidascaris
Page 228 and 229:
Table 14, continued. Spinitectus gr
Page 230 and 231:
Table 14, continued. Rhabdochonidae
Page 232 and 233:
Table 14, continued. Host: Petromyz
Page 234 and 235:
Table 14, continued. Salvelinus fon
Page 236 and 237:
Table 14, continued. Pungitius pung
Page 238 and 239:
Table 14, continued. Neoechinorhync
Page 240 and 241:
Table 14, continued. Perca flavesce
Page 242 and 243:
Table 14, continued. Hirudinea (Lee
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Table 14, continued. Ergasilidae No
Page 246 and 247:
Table 14, continued. Ergasilus vers
Page 248 and 249:
Table 14, continued. Salmincola ext
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Table 15. Fishes by family from Lak
Page 252 and 253:
Table 15, continued. Cyprinus carpi
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Table 15, continued. Monogenea: Dac
Page 256 and 257:
Table 15, continued. Catostomidae C
Page 258 and 259:
Table 15, continued. Adult Acanthoc
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Table 15, continued. Immature Acant
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Table 15, continued. Oncorhynchus m
Page 264 and 265:
Page 266 and 267:
Table 15, continued. Fundulidae Fun
Page 268 and 269:
Page 270 and 271:
Table 15, continued. Lepomis macroc
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Table 15, continued. Adult Cestoda:
Page 274 and 275:
Table 15, continued. Gobiidae Apoll
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Percina caprodes, Sander vitreus, A
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Table 18, continued. Clinostomidae
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Table 18, continued. LAKE ST CLAIR
Page 282 and 283:
Table 18, continued. Strigeidae Rai
Page 284 and 285:
Table 18, continued. Salvelinus nam
Page 286 and 287:
Table 18, continued. Spiroxys sp. S
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Table 18, continued. DETROIT RIVER
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Table 19, continued. Salmonidae Cor
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Parasite Species—Overview LAKE ER
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Cestodes Twenty-four species of adu
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Parasitological studies have been d
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N. atherinoides, N. buccatus, N. he
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mordax in Lake Erie. Mass mortaliti
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Copepods Copepods (Argulus catostom
Page 304 and 305:
Table 20. Parasites reported in fis
Page 306 and 307:
Table 20, continued. Capriniana sp.
Page 308 and 309:
Table 20, continued. Myxobolus cons
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Table 20, continued. Sphaerosporida
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Table 20, continued. Host: Osmerus
Page 314 and 315:
Page 316 and 317:
Table 20, continued. Azygia longa (
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Table 20, continued. Host: Micropte
Page 320 and 321:
Table 20, continued. Host: Aplodino
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Table 20, continued. Microcreadium
Page 324 and 325:
Table 20, continued. Host: Amia cal
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Table 20, continued. Unknown Family
Page 328 and 329:
Page 330 and 331:
Table 20, continued. Ictalurus punc
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Table 20, continued. Host: Esox luc
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Table 20, continued. Etheostoma exi
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Table 20, continued. Percina copela
Page 338 and 339:
Page 340 and 341:
Table 20, continued. Axinidae Unnit
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Table 20, continued. Dactylogyrus a
Page 344 and 345:
Table 20, continued. Lyrodiscus sem
Page 346 and 347:
Table 20, continued. Tetracleidus c
Page 348 and 349:
Table 20, continued. Gyrodactylidae
Page 350 and 351:
Table 20, continued. Percina caprod
Page 352 and 353:
Table 20, continued. Tetraonchidae
Page 354 and 355:
Table 20, continued. Bothriocephalu
Page 356 and 357:
Page 358 and 359:
Page 360 and 361:
Table 20, continued. Amphicotylidae
Page 362 and 363:
Table 20, continued. Schistocephalu
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Pomoxis nigromaculatus: Bangham 197
Page 366 and 367:
Table 20, continued. Triaenophorus
Page 368 and 369:
Table 20, continued. Cyprinella whi
Page 370 and 371:
Table 20, continued. Etheostoma ble
Page 372 and 373:
Page 374 and 375:
Table 20, continued. Micropterus do
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Table 20, continued. Philometra sp.
Page 378 and 379:
Page 380 and 381:
Table 20, continued. Dioctophymatid
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Table 20, continued. Philometridae
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Table 20, continued. Superfamily Sp
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Table 20, continued. Neoechinorhync
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Table 20, continued. Octospinifer m
Page 390 and 391:
Table 20, continued. Pomoxis annula
Page 392 and 393:
Page 394 and 395:
Table 20, continued. Lepomis cyanel
Page 396 and 397:
Table 20, continued. Sander glaucum
Page 398 and 399:
Table 20, continued. Lernaea crucia
Page 400 and 401:
Table 20, continued. Mollusca (Moll
Page 402 and 403:
Page 404 and 405:
Page 406 and 407:
Table 21, continued. Notemigonus cr
Page 408 and 409:
Table 21, continued. Monogenea: Uni
Page 410 and 411:
Page 412 and 413:
Page 414 and 415:
Page 416 and 417:
Table 21, continued. Umbridae Umbra
Page 418 and 419:
Table 21, continued. Gadidae Lota l
Page 420 and 421:
Page 422 and 423:
Page 424 and 425:
Page 426 and 427:
Table 21, continued. Percidae Ammoc
Page 428 and 429:
Page 430 and 431:
Page 432 and 433:
Table 21, continued. Hirudinea: Act
Page 434 and 435:
Table 23. Jaccard coefficients of p
Page 436 and 437:
Table 25. Fishes by family from the
Page 438 and 439:
Aspidobothreans Cotylogaster occide
Page 440 and 441:
The 49 fish species from Lake Ontar
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Parasite species or a specific genu
Page 444 and 445:
Cestodes Several adult cestodes (Eu
Page 446 and 447:
Parasite Host Specificity—Jaccard
Page 448 and 449:
Table 26, continued. Host: Anguilla
Page 450 and 451:
Table 26, continued. Myxobolus bart
Page 452 and 453:
Table 26, continued. Microspora (Mi
Page 454 and 455:
Table 26, continued. Crepidostomum
Page 456 and 457:
Table 26, continued. Cryptogonimida
Page 458 and 459:
Table 26, continued. Host: Ictaluru
Page 460 and 461:
Table 26, continued. Cryptogonimida
Page 462 and 463:
Table 26, continued. Etheostoma exi
Page 464 and 465:
Table 26, continued. Apophallus ven
Page 466 and 467:
Table 26, continued. Actinocleidus
Page 468 and 469:
Table 26, continued. Cleidodiscus s
Page 470 and 471:
Table 26, continued. Onchocleidus a
Page 472 and 473:
Table 26, continued. Onchocleidus s
Page 474 and 475:
Table 26, continued. Urocleidus ads
Page 476 and 477:
Table 26, continued. Dactylogyrus b
Page 478 and 479: Table 26, continued. Gyrodactylidae
Page 480 and 481: Table 26, continued. Gyrodactylus p
Page 482 and 483: Table 26, continued. Tetraonchidae
Page 484 and 485: Table 26, continued. Proteocephalid
Page 486 and 487: Table 26, continued. Triaenophorida
Page 488 and 489: Table 26, continued. Proteocephalus
Page 490 and 491: Table 26, continued. Camallanidae R
Page 492 and 493: Table 26, continued. Host: Coregonu
Page 494 and 495: Table 26, continued. Rhabdochona sp
Page 496 and 497: Table 26, continued. Cystidicolidae
Page 498 and 499: Table 26, continued. Echinorhynchus
Page 500 and 501: Table 26, continued. Host: Acipense
Page 502 and 503: Table 26, continued. Hirudinea (Lee
Page 504 and 505: Table 26, continued. Perca flavesce
Page 506 and 507: Table 26, continued. Salmincola ext
Page 508 and 509: Table 27. Fishes by family from Lak
Page 510 and 511: Table 27, continued. Monogenea: Dac
Page 512 and 513: Table 27, continued. Catostomidae C
Page 514 and 515: Table 27, continued. Esocidae Esox
Page 516 and 517: Table 27, continued. Coregonus hoyi
Page 518 and 519: Table 27, continued. Gasterosteidae
Page 520 and 521: Table 27, continued. Centrarchidae
Page 522 and 523: Table 27, continued. Larval/Immatur
Page 524 and 525: Table 27, continued. Etheostoma nig
Page 526 and 527: Table 27, continued. Sciaenidae Apl
Page 530 and 531: commonly found unencysted and coile
Page 532 and 533: Exotic Parasite Species Mills et al
Page 534 and 535: that have direct life cycles. Cesto
Page 536 and 537: Table 30. Jaccard coefficients of p
Page 538 and 539: Ambloplites rupestris harbored as f
Page 540 and 541: in composition and numbers between
Page 542 and 543: In Lake Michigan, percids harbored
Page 544 and 545: prevalence of cestodes (tapeworms)
Page 546 and 547: Anderson, R.C. 1992. Nematode paras
Page 548 and 549: Bush, A.O., Fernandez, J.C., Esch,
Page 550 and 551: Dechtiar, A.O. 1967b. Neodiscocotyl
Page 552 and 553: Esch, G.W., Kennedy, C.R., Bush, A.
Page 554 and 555: Hines, R.S. and Spira, D.T. 1974. I
Page 556 and 557: Kennedy, C.R. 2009. The ecology of
Page 558 and 559: Marcogliese, D.J. 2008. First repor
Page 560 and 561: Muzzall, P.M., and Haas, R.C. 1998.
Page 562 and 563: Pronin, N.M., Fleischer, G.W., Bald
Page 564 and 565: Smith, H.D., and Margolis, L. 1970.
Page 566 and 567: Thomas, L.J. 1947. The life cycle o
Page 568: Wisniewski, W.L. 1958. Characteriza
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