sign in sign up
<<
Home , Anisakis, Balaena, Bowhead whale, Whale louse

Great Basin Naturalist

Volume 47 Number 3 Article 2

7-31-1987

Parasites of the bowhead , mysticetus

Richard A. Heckmann Brigham Young University

Lauritz A. Jensen University of Health Sciences, Kansas City, Missouri

Robert G. Warnock Westminster College, Lake City, Utah

Bruce Coleman Brigham Young University

Follow this and additional works at: https://scholarsarchive.byu.edu/gbn

Recommended Citation Heckmann, Richard A.; Jensen, Lauritz A.; Warnock, Robert G.; and Coleman, Bruce (1987) "Parasites of the , Balaena mysticetus," Great Basin Naturalist: Vol. 47 : No. 3 , Article 2. Available at: https://scholarsarchive.byu.edu/gbn/vol47/iss3/2

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. PARASITES OF THE BOWHEAD WHALE, BALAENA MYSTICETUS

Richard A. Heckmann', Lauritz A. Jensen', Robert G. VVarnock^ and Bruce Coleman'

Abstract —Blood, tissue, and samples from five bowhead were examined for ecto- and endoparasites. Two of protozoans, four genera of diatoms, one species of , two species of nematoda, and one species of "" were found. No blood parasites were recovered. The larval anisakid , found in the submucosa of the forestomach of one whale, generated a prominent inflammatory response. Protozoans found in contents of the colon included a flagellate and a sarcodinan. The sarcodinan, which was common in the colon contents of one whale, belongs to the Entamoeba and probabK- represents an undescribed species. Ogomogaster plicatus, a trematode, was also identified. The data from this study are compared with previous lists of parasites for the bowhead whale and two other species ofbaleen whales. From the results presented, the previous list of parasites for the bowhead whale has been expanded to include eight additional genera and species.

Cetaceans throughout the world are known The primary objective of this study was to to be infested and infected with parasites estimate the parasite burden of the bowhead (Dailey and Brownell 1972). This does not whale, Balaena mysticetus, through the ex- necessarily mean that the hosts are seriously amination of the selected specimen materials affected or damaged by the symbionts. If, in obtained from subsistence harvested whales. addition to the parasite load, stress and/or nutritional imbalances occur, the may Methods become weak and possibly die. Stroud and Roffe 1979, Dailey and Walker 1978, Martin Specimen materials were obtained from et al. 1970, Ridgway and Dailey 1972 have five bowhead whales taken off Barrow, , indicated that helminths were a possible fac- in 1980 by Eskimo hunters. Tissue samples, tor for cetacean strandings. Stranded including colon contents, were collected on- exhibited disoriented behavior with an obvi- site (Albert 1981), fixed in 10% formaUn, and ous loss of equilibrium. Necropsy results of shipped by air freight to the parasitology labo- these animals showed that the central nervous ratory at Brigham Young University. Blood system was infected with trematodes of the smears from whales were air dried and sent genus Nasitrema, thus providing at least a with the above samples. The samples were partial explanation for the whale strandings. processed as follows; The nematode Sternurus, located in the ears Tissues and organs,—After the code num- of cetaceans, is also a potential factor for ber for the whale was recorded, each speci- cetacean strandings. The brains of these men was weighed, measured, and then dis- stranded animals showed lesions induced by sected to determine the presence of parasites. trematode eggs. Intestinal segments were cut lengthwise, af- Activities associated with offshore oil and ter which the lumen was examined for macro- gas development, such as those in the Beau- scopic parasites. Samples of lumen contents fort Sea, may increase the stress to bowhead were placed on glass slides and examined with whales and thereby allow an increase in para- a light microscope. Slides of lumen contents site burden. It would be advantageous to de- from the intestine were also fixed and stained termine the types of parasites harbored by with iron haemotoxylin, trichrome, or bowhead whales for such knowledge would Giemsa-Wrights stains to enhance parasite help in understanding what effect contact presence. After the staining procedure was with spilled oil may have on cetaceans. completed, each slide was examined for para-

Department of zooiog\-. Brigham Young University, Provo, Utah 84602. ^Department of MicrobiologN-, University of Health Sciences. Kansas Cit\', Missouri 64124. Department of Biolog)-, Westminster College, Salt Lake City, Utah 84101,

355 356 July 1987 Heckmann etal: Whale Pamsites 357

Table 2. Results of examining bowhead whale, Balacna mysticetus. tissue samples, with process procedi summarized, for parasites.

Whale 358 Great Basin Naturalist Vol. 47, No. 3

*/ \ Jul

1

a Fig. 1. Photomicrographs and hne drawings of an amoeboid parasite (Entamoeba sp.) from the colon contents of bowhead whale, Balaena mysticetus. Note the pseudopod (P) characteristic of this protozoan group, both single (n) and

multinucleate (mn) cells, vacuoles (v), granular cytoplasm (g), and chromatoid body (c) (1,000X for photomicrographs).

spheroid to ovoid, nuclei randomly dis- located in uninucleate forms, nucleus occu- tributed for multinucleate forms and centrally pies approximately 10% of the cell volume, July 1987 Heckmann etal: Whale Parasites 359

chromatoidlike bodies in cytoplasm, periph-

eral nonchromatic granules, it was common in the intestinal contents of one bowhead whale. Based on these observations and the similarity of characteristics (Kudo 1966), we consider this amoeba a species of Entamoeba Casagrandi & Barbagallo, 1895. Thus, based on Levine et al. (1980), the classification for this amoeba would be:

Phylum:

Fig. 2. Photomicrographs and Hne drawing of a flagel- lated protozoan found in the colon contents of Balaena mysticetus. Flagella (f) and a single nucleus (n) are visible, both characteristic of flagellated protozoa (1,000X for pho- tomicrographs). pseudopodia observed, vacuoles vary in num- ber, both and water vacuoles present Great Basin Naturalist Vol. 47, No. 3

Fig. 3. Scanning electron microscope (SEM) micrographs (3a, 3b) and light microscope micrograph (3c) of one of the most common diatoms, Cocconeis (arrowheads), observed during this study. Fig. 3b shows the extent to which Cocconeis extends into the epidermis of whale . The micron bar at the bottom of each micrograph (SEM) is used to measure object size. Filamentous bacteria (b) and whale red blood cells (r) are present on one micrograph (3a). The light microscope micrograph (3c) is magnified 400X.

Fig. 3b. July 1987 Heckmann etal.: Whale Parasites 361

Fig. 3c.

I 362 Great Basin Naturalist Vol. 47, No. 3

Fig. 5. SEM micrograph of a diatom (n) Navicula sp. Note micron bar at bottom of micrograph.

Fig. 6. The diatom (g) Gomphonema sp. on the surface of bowhead whale skin(s). Note filamentous bacteria (b) and a biconcave erythrocyte (r) (220X). July 1987 Heckmann etal; Whale Parasites 363

Fig. 7. SEM micrograph of bowhead whale epidermis from an area without prominent erosions of the epidermis. Note filamentous bacteria (b) and diatoms (d) such as Gomphonema and Cocconeis on the surface of the skin (220X).

Fig. 8. Bowhead whale epidermis: 8a, the free surface of the skin with initial erosion (lOOX); 8b (lOOX) and 8c (400X), the erosion (e) process continuing and the presence of bacteria (b) and diatoms (d) in the eroded area. gitudinal ridges on the ventral surface. Og- Anisakid-type Larvae mogaster plicatus is characterized by 19-28 Phylum Nematoda(The Aschelminthes, Barnes 1980) ridges with an average of 23 (Rausch and Fay Order: Ascaridata 1966). Figure 10 represents the dorsal and Family: ventral surfaces of O. plicatus collected dur- The piece of bowhead forestomach ing this study. The life cycle is unknown for mounted in paraffin contained larval ne- this species. matodes that appeared to be an anisakid-type 364 Great Basin Naturalist Vol. 47, No. 3

Fig. 9. SEM micrograph representing erosions (e) in the epidermis of whale skin, which usually contains numerous diatoms and bacteria (llOX).

(Schmidt and Roberts 1984, Migaki et al. remains present, trilobed lips, dentigerous 1982) (Fig. 11). No adult stages of this round- ridge on anterior end, no terminal enlarge- worm were observed in examined samples. A ment for the esophagus, no alae, and overlap- description of the life cycle of is ping annulations on the surface. The ne- found in parasitology texts (Faust et al. 1975, matode is apparently a species o( Anisakis. Schmidt and Roberts 1984) and in recent pub- Because we lacked adult worms, which are hcations (Smith 1971, Wootten and Waddell required for a definitive taxonomic assign- 1977, Smith and Wootten 1978, Wootten ment (Smith and Wootten 1978), and because 1978, Heckmann and Otto 1985). Adult stages of the taxonomic confusion of the family An- of this nematode are characteristically found isakidae, the larval nematode will be referred in stomachs of carnivorous marine to as "anisakid-type' (Schmidt and Roberts (Smith and Wootten 1978). The examined ne- 1984). Yokogawa and Yoshimura (1967) re- matode was in the migratory larval phase of its ported larval anisakiasis in the gastrointestinal life cycle. Larval characteristics for species of tract of Japanese people. Recently, cases of Anisakis include: esophagus with a ven- anisakiasis have been reported in the United triculus that ends obliquely at its junction States (Schmidt and Roberts 1984), and larval

with the intestine (Hadidjaja et al. 1978), no stages of this roundworm, obtained from ventricular appendage nor intestinal caecum, harvested at Barrow, Alaska (Heck-

the tail is blunt and terminates in a distinct mann and Otto 1984), were sent to this labora- mucron (Smith and Wootten 1978, Shiraki tory. 1974, Oshima 1972), a prominent boring tooth Anisakid Roundworm (mucron) present (Smith and Wootten 1978). Phylum: Nematoda For the life cycle of Anisakis sp., euphausiids Order: Ascaridata (Crustacea) are probably the most important intermediate host (Smith 1971, Smith and One worm found free in the stomach of Wootten 1978). Euphausiids are a source of animal (80B1) was too poor to evaluate prop-

food for the bowhead whale (Lowry and Burns erly; therefore, it is impossible to obtain a 1979, Lowry and Burns 1980, Lowry and complete taxonomic description. This round- Frost 1984). After examining serial sections of worm appears to be Anisakis or Contracae- the larval nematode, we noted the following ciun. Members of these genera are among the characteristics: no bursa or prominent teeth, most common parasites in the stomachs of blunt tail with mucron (Dailey and Brownell 1972). July 1987 Heckmann et al.; Whale Parasites 365

Jk 366 Great Basin Naturalist Vol. 47, No. 3

whale), and physalus () (Dailey and Brownell 1972). Trematode.—Lecithodesmus goliath is a fluke that parasitizes bile ducts of . Lecithodesmus goliath produces large eggs that are triangular in cross-section. MoUus- cans are intermediate hosts, and metacercar- iae can be ingested with the moUuscan inter- mediate host (Dailey and Brownell 1972). Small clams (bivalves), which are members of the phylum mollusca, have been reported from the colon of a bowhead whale (Lowry and Burns 1979). Ki'Ji Acanthocephala.—Bolhosoma halaenae

is an acanthocephalan that is found in the Fig. 11. The larval anisakid-type roundworm (arrow- intestine of marine mammals including B. heads) found encysted (c) in the suhmucosa (sm) of the mysticetus (Dailev and Brownell 1972, Nei- howhead whale forestomach. Note the inflammatory (i) response around the nematode (lOOX). land 1962). The parasites observed during this study and all those reported for the bowhead whale found on gray whales. The species Cyamus are listed in Table 3. The parasites reported ceti is one of the most common parasites ob- for the bowhead whale are compared with served during this and a previous study those reported for two other cetaceans, the (Heckmann et al. 1980, Heckmann 1981). [Eschrichtus rohustus) and the Figure 12 represents the ventral surface of a {Balaenoptera ??i».scu/j/.s)(Table 4). whale louse. Note the enlarged appendages with numerous hooks. The mouthparts, as Discussion well as the appendages, are highly modified for the ectoparasitic mode of life. The cyamids Samples of bowhead whale tissue were sent have a direct life history with the young whale to our laboratory during 1980 to be examined lice being released from the broodpouch of for parasites. From samples of five bowhead the female. The amphipods have no free- whales, two protozoans, four genera of di- swimming stage. Subsequent moultings pro- atoms, and a nematode have been added to duce sexually mature adults. the existing list of parasites (Table 3). With additional samples, the hst would most likely Other Reported Balaena inysticetus Parasites be expanded, especially the protozoan forms.

Nematode.—Crassicauda crassicauda is a Data from this study confirmed the presence nematode parasitizing the urogenital system of Cyamus ceti, a whale louse, as well as the and sometimes other parts of the body. Al- presence of an Ogmogaster, which had been though the life cycle of C. crassicauda has not described in a bowhead whale in 1979 (Shults been determined, members of the order in 1979). Samples of blood from four whales which this genus belongs reproduce were negative for parasites. viviparously or ovoviparously and parasitize Because of its currently known dietary the body cavity, blood sinus, air bladder, or habits, the bowhead whale is not subject to other tissues of aquatic vertebrates. Cope- many of the internal parasites found in marine pods are considered intermediate hosts for C. mammals that feed on fish, large , crassicauda. For cetaceans, the nematode has and mollusks. Fish, large crustaceans, and been reported from Tiirsiops truncatus mollusks are common intermediate hosts for (bottlenosed ), Balaenoptera mus- helminths of marine mammals (Ridgway and culus (blue whale), Megaptera novaengjiae Dailey 1972). (), Balaen mysticetus (bow- The bases for placing the protozoan, found head whale), Ziphius cavirostris (Cuvier's in the colon contents of one whale, in the ), Balaenoptera acutorostrata family Endamoebidae are its small size and (), Balaenoptera horealis (sei location, the presence ofone to four nuclei per July 1987 Heckmann etal: Whale Parasites 367

Fig. 12. SEM of the ventral surface of the whale "louse," Cyamns ceti (8X). Cijamus ceti is not a louse but a highly modified amphipod infesting the skin of whales. The anterior (a) and posterior (p) parts of C. ceti are labeled. , and numerous food vacuoles in the cyto- moeba are common entocommensals and par- plasm. Members of the Endamoebidae are asites of the digestive system of vertebrate typically parasites or commensals of the diges- and invertebrate hosts. The present study is tive systems of and vertebrates the first record of a protozoan parasite for the (Schmidt and Roberts 1984). Species of Enta- bowhead whale. Additional material must be 368 Great Basin Naturalist Vol. 47, No. 3

Table 3. A consolidated list of parasites for Balaena mysticetus, bowhead whale.

Parasite July 1987 Heckmann etal.: Whale Parasites 369

Table 4. Comparison of parasites observed in three species of whales.

Parasite group with listed species Protozoa Acanthocephala * Trematoda* Nematoda Amphipoda** (host) EFD B1B2B3B4C P1P2P3T OiOoOaL AAiCiC.P C Eschrichfiis robusttis O O O oooop oppo oppo 00000 O Gray whale

Balaenoptera mtiscultis' O O O PPPPO OPOP PPOO POPOP P Blue whale

Balaena mysticetus^ P P P POOOO POOO PPOP OPPPO P O^Not observed P=Obsened in host *Phyluni: Plat\helminthes ** Phylum: Arthropoda ' 'Daile\ and Brownell 1972 *rhis study and Daile\- and Browniell 1972

Codes for parasites: Protozoa Cestoda Nematoda E =^ Amoeboid form [Entamodeba] Pi - Phyllobothrium detphuu A = Anisakis F = Flagellate Po ^ Pi'iapocephahis sp Ai = Anisakis-type larvae - D Diatoms; 4 species P3 ^ Pseudophyllidae sp. Ci = Crassicauda crassicauda T ^ Tetrabothrius affinis C2 = sp. P = Porrocaecum decipiens

Acanthocephala Trematoda Amphipoda = - Bi Bolboscmm balaenae Oi O^mogaster plicatus C = Cyamus ceti B2 - Bolbosoma brevicolle Oa^ Ogtnogaster antarcticus B3 = Bolbosonia hamiltoni O3 ^ Ogmogaster pentcdineatus B4 = Bolbosoma turbinella L ^ Lecithudesmus gotiath C = Corynosoma sp

roldT. Haldiman, Louisiana State University, Dailey, M D , L Jensen, and B. Westerhof Hill 1981. provided Figures 3a, 5, and 14 for this report. Larval anisakine roundworms of marine fishes This study was supported by Bureau of Land from southern and central California, with com- ments on public health significance. California Management Contract AA851-CT0-22 to the Fish and Game 67: 240-245. University of Maryland, College Park, Mary- Faust, E C . P. C. Beaver, and R. C. Jung. 1975. Animal land. agents and vectors of human disease. Lea and Febiger.

Fuller. H J , and O Tippo 1960. College botany. Holt, LiTER.\TURE Cited Rinehart and Winston, Co.

Hadidj.ma. P , E I Herry, H Mahfudin-Burhanuddin, Albert. T F 1981. Listing of collected bowhead whale AND M Hutomo 1978. Larvae of anisakidae in marine fish of coastal waters specimens with observations made during initial near Jakarta, Indone- sia. 51-.54. examination. Pages 84.5-916 in T. F. Albert, ed.. J. Trop. Med. and Hygiene 27:

Tissue structural studies and other investigations Haldiman, J. T., Y. Z. Abdelbaki, F K. Al-Bagdadi, D. on the biology of endangered whales in the Beau- W DuFFiELD, W. G. Henk, andR B. Henry 1981. fort Sea. Report to the Bureau of Land Manage- Determination of the gross and microscopic struc- ment from the Department of Veterinar> Science, ture of the lung, kidney, brain and skin of the bowhead whale, University of Maryland, College Park. 9.5.3 pp. Balaena mysticetus. Pages 305-662 in T. F. Albert, ed.. Tissue structural Barnes, R D 1980. Pages 263-312 in Invertebrate zool- studies and other investigations on the biology of ogy. VV. B. Saunders Company, Philadelphia. endangered whales in the . Report to Beverly-Burton. M 1978. Helminths of the alimentary the Bureau of Land Management from the De- tract from a stranded herd of the Atlantic white- partment of Veterinar}' Science, University of sided dolphin, acuttis. J. Fish Maryland, College Park. 953 pp. Res. Board Canada: 35: 1356-13.59. Heckmann. R 1981. Parasitological study of the bowhead

Dailey. M D . AND R L Brownell 1972. A checklist of whale, Balaena mysticetus. Pages 27.5-.304 in T. marine parasites. Pages 528-589 in S. F. Albert, ed. , Tissue structural studies and other Ridgway, ed.. Mammals of the sea, biology and investigations on the biology of endangered medicine. Charles C. Thomas Co. whales in the Beaufort Sea. Report to the Bureau

Dailey, M D , and W A Walker 1978. as a of Land Management from the Department of factor (?) in single strandings of southern California Veterinary Science, University of Maryland, Col- cetaceans. J. Parasitol. 64: .593-.596. lege Park. 9.53 pp. 370 Great Basin Naturalist Vol. 47, No. 3

Fig. 13. Micrographs representing the presence of: 13a, protozoa (P); 13b, bacteria (b); and 13c, diatoms (d) in the eroded areas of bowhead whale epidermis (1,000X).

Par- Heckmann, R. a., and T. Otto. 19S.5. Occurrence of an- Heckmann, R. A., R Warnock. and L Jensen 1980. isakid larvae (Nematoda: Ascardidia) in fishes from asites (RU-979). Pages .517-.538 in]. Kelley and G. of the occurrence and Alaska and Idaho. Great Basin Nat. 4.5: 427-431. Laursen, eds. , Investigation .

July 1987 Heckmann et al.; Whale Parasites 371

Fig. 14. SEM micrograph of bowhead whale skin representing the t\pes of organisms, bacteria (b) and diatoms (d), that could invade erosions in the host epidermis (e). Note micron bar.

beha\ ior patterns of whales in the vicinity of the Lowry, L F., K. J Frost, and J J Burns 1978. Food of Beaufort Sea lease area. Final Report to the Bu- ringed seals and bowhead whales near Point Bar- reau of Land Management from the Naval row, Alaska. Canadian Field-Naturalist 92: 67-70.

Research Laboratory, Barrow, Alaska. Martin. W E , C K Haun. H S Barrow, and H Kudo, R. R. 1966. Pages 518-.564 in Protozoology. Cr.\\toto. 1970. Nematode damage to brain of Charles C. Thomas, Springfield, Illinois. , Lagenorphijnchus ohliquidens Leung, Y. 1967. An illustrated key to the species ofwhale- Trans. Amer. Microsc. Soc. 89: 200-205.

lice (Amphipoda, Cyamidae), ectoparasites of Meyers. B J 1979. Anisakine in fresh com- Cetacea, with a guide to the literature. Cruste- mercial fish from waters along the Washington,

ceana 12; 279-291. Oregon and California coasts. J. Food Protection .380-384. Levine. N D , J O Corliss, F E G Cox. G Derou.x. J 42: Crain. B M Honingberg. G F Leedale. A R MiGAKi, G 1981. The microscopic examination of the

LoEBLiCH III, J LoM, D. Lynn. E G Merinfeld. bowhead whale, Balaena mijsticetus, and the gray \' F C Page, G Poljanskv. Spr.\gue, J Vavr\, whale, Eschrichtius robustus. for changes due to AND F G Wallace 1980. A newly re\ ised classifi- toxic substances and infectious agents. Pages

cation of Protozoa. J. Protozoolog>' 27: 37-58. 173-199 in T. F. Albert, ed.. Tissue structural

Lowry, L. F., and J Burns 1979. Tissues, structure and studies and other investigations on the biology of

function (RU 280g). Pages 437-447 in J. Kelley endangered whales in the Beaufort Sea. Report to and G. Laursen, eds., In\estigation of the occur- the Bureau of Land Management from the De- rence and behavior patterns of whales in the vicin- partment of Veterinary Science, LTniversity of ity of the Beaufort Sea lease area. Final Report to Maryland, College Park. 953 pp.

the Bureau of Land Management from the Naval MiGAKi. G . R A Heckmann. and T F. Albert 1982. Arctic Research Laboratory, Barrow, Alaska. Gastric nodules caused b\ "anisakis type" larvae in

Lowry. L. F., and J J Burns 1980. utilized by the bowhead whale (Balaena inysticetus). J. bowhead whales near Barter Island, Alaska, Wildl. Dis. 18: 353-358. autumn 1979. Marine Fisheries Review 42(9-10): Neiland. K. 1962. Alaskan species of acanthocephalan

88-91. genus Corynosoma Luche, 1904. J. Parasitol.

Lowry. L. F., and K J Frost 1984. Foods and feeding of 48(1): 69-76. bowhead whales in western and northern Alaska. Nemoto. T 1956. On the diatoms of the skin film of Scientific Report. Whales Research Institute whales in the Northern Pacific. Sci. Rep. Whales 35:1-16. Res. Inst. 11:99-1.32. 372 Great Basin Naturalist Vol. 47, No. 3

1977. 1974. Larval nematodes of the family anisaki- Nemoto. T., F L Brownell, Jr . andT. Isfiimaru ShirakiT Cocconeis diatoms on the skin oiFranciscana. Sci. dae (Menatoda) in the northern Sea of Japan—as a Rep. Whales Res. Inst. 29: 101-105. causative agent of eosinophilic phegmone or gran- uloma in the gastro-intestinal tract. Acta Medicaet Olsen, O. W. 1974. Animal parasites, their hfe cycles and Biologia 22; 57-98. ecology. University Park Press. Shults, L M 1979. Og,mogaster antarcticus Johnston, Omura. H. 19.50. Diatom infection on blue and fin whales 1931 (Trematoda; Notocotylidae) from the bow- in the antarctic area V (the Ross Sea area). head whale, Balaena mysticetus L., at Barrow, Sci. Rep. Whales Res. Inst. 4: 14-26. Alaska. Canadian J. Zool. 57; 1.347-1348. Oshima, T. 1972. Anisakis and anisakiasis in Japan and inerinis T. Smith. J W 1971. Thysanoessa and longicau- .301-.39.3 K. Morishita, Y. adjacent area. Pages in data (Euphausiidae) as first intermediate hosts of Komuja, and H. Matsubayashi, eds.. Progress of Anisakis sp. (Nematoda; Ascaridata) in the North medical parasitology in Japan. Vol. IV. Megura Sea, to the north of Scotland and at Faroe. Nature Parasitological Museum, Tokyo. 2.34: 478. Anisakis Rausch, R L, and F H Fay 1966. Studies on the Smith, J W , and R Wootten 1978. and An- helminth fauna of Alaska. XLIV. Revision of Og- isakiasis. Pages 93-163 in W. H. R. Lumsden, R.

mogfl.sfer Jagerskiold, 1891, with a description of Muller, and J. R. Baker, eds., Advances in para- O. pentalmeatus sp. n. (Trematoda: Notocotyli- sitology (16). Parasites .52; Stroud, R K , and M D Dailey 1978. and dae). J. Parasitol. 26-38. associated pathologv in pinnipeds stranded along Rausch. R L.. and D W Rice 1970. O^mogaster trilin- the Oregon coast. Wildl. Dis. 14: 292-298. eatus sp. n. (Trematoda; Notocotylidae). Proc. J.'

Stroud, R K , andT Roffe 1979. Causes of death in Helm. Soc. Washington 37; 196-200. J marine mammals stranded along the Oregon RiDGW.w, S. H. 1972. Homeostasis in the aquatic environ- coast. J. Wildl. Dis, 15:91-97. ment. Pages 590-747 in S. Ridgway, ed.. Mam- Wootten, R 1978, The occurrence of larval anisakid mals of the sea, biology and medicine. Charles C. nematodes in small gadoids from Scottish waters. Thomas Co. .58; 347-3.56. J. Mar. Biol. Ass. U.K. Ridgway. S. H.. and M, D. Dailey. 1972. Cerebral and Wootten, R , and I F. Waddell 1977. The occurrence cerebellar involvement of trematode parasites in of larval nematodes in the musculature of and and their possible role in stranding. J. whiting from Scottish waters. J. du Conseil. Int. Wildl. Dis. 8; 33-43. E.xplor. Mer. 37: 266-273.

in , YosHiMUR.\ 1967. Clinicopatho- Schmidt, J D., and L. S Roberts 1984. Page 492 YoKOGAWA, M AND H Foundations of parasitology. C. V. MosbyCo., St. logical studies on larval anisakiasis in Japan. Amer. 723-728. Louis. J. Trop. Med. Hyg. 16;