J. Helminthol. Soc. Wash. 64(2), 1997 pp. 161-168 Helminth Parasites of Sea Otters (Enhydra lutris} from Prince William Sound, Alaska: Comparisons with Other Populations of Sea Otters and Comments on the Origin of Their Parasites L. MARGOLIS,1'5 J. M. GROFF,2 S. C. JOHNSON,1-3 T. E. MCDONALD,1 M. L. KENT,1 AND R. B. BLAYLOCK1'4 1 Department of Fisheries and Oceans, Pacific Biological Station, Nanaimo, British Columbia, Canada V9R 5K6 (e-mail T.E.M.:[email protected]; e-mail M.L.K.:[email protected]) and 2 Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, California 95616 (e-mail: Joseph [email protected]) ABSTRACT: The helminths found in the gastrointestinal tracts and gallbladders of 68 sea otters (Enhydra lutris) from Prince William Sound, Alaska, and their prevalences were: Corynosoma enhydri (Acanthocephala), intes- tine, 51.5%; Orthosplanchnus fraterculus (Trematoda), gallbladder, 50%; Diplogonoporus tetrapterus (Cestoda), intestine, 12%; and Pseudoterranova decipiens (Nematoda), stomach, 1.5%. One pup examined was free of helminth parasites. Throughout its range from the Kuril and Komandorski islands in Russia, across the Aleutian Islands, Alaska, and south to California, the sea otter harbors a total of 17 or 18 species of helminths, of which 5 or 6 are incidental infections with larval (2 species of Anisakis) or juvenile worms (3 or 4 species of Poly- morphus). The adult worms of sea otters (12 species) are derived primarily (9 species) from pinnipeds. One species, Microphallus pirum (Trematoda), found widely in sea otters from the Komandorski Islands to California, may be primarily a parasite of various shorebirds. Only one species, C. enhydri, is uniquely a parasite of sea otters, occurring throughout its range at prevalences greater than 50%. California populations of sea otters harbor only M. pirum, C. enhydri, and Polymorphus species, lacking any species known to be transmitted by fish; the diet of these sea otters consists almost entirely of invertebrates. Northern sea otter populations from Russia and Alaska have a more varied diet and are hosts for at least 5 fish-transmitted parasites. Among the commonly occurring parasites, the most striking difference between Russian and Alaskan populations of sea otters is the absence of O. fraterculus from Russian populations and its frequent occurrence in Alaskan populations. KEY WORDS: parasites, helminths, Orthosplanchnus fraterculus, Diplogonoporus tetrapterus, Pseudoterra- nova decipiens, Corynosoma enhydri, sea otters, Enhydra lutris, Alaska, North Pacific Ocean, zoogeography. In spring 1989, a major oil spill in Prince Wil- Materials and Methods liam Sound, Alaska, caused by the grounding of Data on helminth parasites were recorded from 69 the T/V Exxon Valdez, resulted in substantial sea otters (37 9: 27 adults, 7 juveniles, 3 undetermined mortalities among the sea otter (Enhydra lutris) maturity; 26 6*: 12 adults, 8 juveniles, 6 undetermined population. More than 1,000 dead sea otters maturity; 1 pup; 6 undetermined sex: 3 adults, 3 un- were recovered during rescue operations in determined maturity). Fifty-nine of these animals were Prince William Sound and neighboring coastal collected live and necropsied either immediately fol- lowing death or euthanasia (usually within 1 to 6 days, areas (Bayha and Kormendy, 1990). We report rarely up to 10 days), or they were refrigerated and on the helminth parasites collected from some examined within several (maximum 6 to 8) hours after of the necropsied animals and compare the find- death. The remaining 10 otters were dead upon collec- ings with previous reports on helminth parasites tion, but appeared sufficiently fresh to yield valid par- of sea otters from North American and Asian asite prevalence data. .Stomach, intestine, and gallblad- der were examined macroscopically for all but 1 ? and populations. We conclude with a discussion of 1 c?, for which only the gallbladder was examined. the origin of the sea otter parasite fauna. Field circumstances did not permit microscopic ex- amination or the use of such techniques as sieving, 3 Present address: National Research Council of decanting, or centrifugation of gastrointestinal or gall- Canada, Institute for Marine Biosciences, 1411 Oxford bladder contents to detect very small helminths. Be- Street, Halifax, Nova Scotia, Canada B3H 3Z1 (e-mail: cause the number of worms of each species encoun- Stewart. [email protected]). tered in each animal was not counted, we report only 4 Corresponding author and present address: Gulf data on parasite prevalence. Coast Research Laboratory, P.O. Box 7000, 703 East Representative samples of helminths were fixed and Beach Drive, Ocean Springs, Mississippi 39566-7000 preserved in 10% formalin. For microscopic study, (e-mail: [email protected]). nematodes were cleared in lactophenol; trematodes and 5 Deceased, 13 January, 1997. cestodes were stained in Semichon's acetic carmine, 161 CCooppyyrriigghhtt ©© 22001111,, TThhee HHeellmmiinntthhoollooggiiccaall SSoocciieettyy ooff WWaasshhiinnggttoonn 162 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 64(2), JULY 1997 Table 1. Prevalence of helminth parasites in adult and juvenile sea otters (Enhydra lutris) from Prince William Sound, Alaska. No. No. Prevalence Site examined infected (%) Trematoda Orthosplanchnus fraterculus Gallbladder 68 34 50.0 Cestoda Diplogonoporus tetrapterus Intestine 66 8 12.1 Nematoda Pseudoterranova decipiens Stomach 66 1 1.5 Acanthocephala Coiynosoma cnhydri Intestine 66 34 51.5 dehydrated in a series of ethanols, cleared in xylene, ered from the stomach of only 1 adult female and mounted in Canada balsam; and acanthocephalans otter. The 1 pup examined was free of helminths. were studied unstained. For cestodes, transverse and longitudinal sections of mature and gravid proglottids Discussion were prepared, stained in hematoxylin, and mounted in permount after dehydration in ethanol and clearing The sea otter is an exclusively marine species in xylene. Representative voucher specimens have of the mammalian family Mustelidae. It inhabits been deposited in the U.S. National Parasite Collection (USNPC), Beltsville, Maryland: Orthosplanchnus fra- coastal areas on the North American and Asian terculus (USNPC 86771), Diplogonoporus tetrapterus sides of the North Pacific Ocean (Riedman and (USNPC 86772), Pseudoterranova decipiens (USNPC Estes, 1987) and was the object of intensive hu- 86773), and Corynosoma enhydri (USNPC 86774). man exploitation for its valuable pelt in the 18th The terms prevalence and intensity are used in accor- dance with the definitions provided by Margolis et al. and 19th centuries, which resulted in elimination (1982). Parasite prevalences among male, female, of the species from vast areas of its original adult, and juvenile sea otters were compared statisti- range. With complete protection from harvest- cally using Fisher's exact probability test (Sokal and ing, population numbers have been increasing in Rohlf, 1981). recent decades, and parts of the former sea otter Results range have been reoccupied by natural invasion or by deliberate reintroduction of the species. At Four species of helminth parasites were found present, populations exist in a disjunct distribu- in the sea otters, one each of Cestoda, Trema- tion between about 35°N and 60°N on the North toda, Nematoda, and Acanthocephala (Table 1). American coast and between about 45°N and Except for a statistically significant (P < 0.05) difference between adult male and female hosts 55°N on the Asian coast (Fig. 1). in prevalence of Diplogonoporus tetrapterus Within this distributional range, reports on (von Siebold, 1848) (4 of 12 males and 1 of 27 parasites of the sea otter have been published for females infected), no significant differences in populations from the Komandorski (Command- parasite prevalence were detected between male er) and Kuril islands on the Asian side of the and female hosts or between adult and juvenile Pacific, and from the Aleutian Islands, Prince hosts. We therefore have summarized prevalence William Sound, and California on the North data for all sea otters combined (Table 1). American side (Table 2). Isolated records of par- The most frequently encountered parasites asites of sea otters from islands north and south were the acanthocephalan Corynosoma enhydri of the western end of the Alaska Peninsula and Morozov, 1940, in the intestine and the digenean from southeast Alaska also have been docu- trematode Orthosplanchnus fraterculus Odhner, mented (Van Cleave, 1953; Adams and Rausch, 1905, in the gallbladder. Both were found in half 1989), as well as a record of C. enhydri from an of the animals examined. The cestode D. tetrap- unspecified locality in Alaska (Kikuchi and Na- terus occurred in the intestine of 12% of the ot- kajima, 1993). ters, and the nematode Pseudoterranova deci- Of the 4 parasite species recovered in the piens (Krabbe, 1878) (3 specimens) was recov- present study, C. enhydri is the only one specific CCooppyyrriigghhtt ©© 22001111,, TThhee HHeellmmiinntthhoollooggiiccaall SSoocciieettyy ooff WWaasshhiinnggttoonn MARGOLIS ET AL.—PARASITES OF SEA OTTERS 163 RUSSIA CANADA U.S.A. IIHill Ori9inal Distribution (1740) ffiffi Present Distribution (1984) MEXICO (*a30N Surviving Translocated Populations Hawaiian Islands Figure 1. North Pacific region showing original and present sea otter distribution. (Modified from Riedman and Estes [1987].) to the sea otter. No other definitive hosts are The tapeworm Diplogonoporus tetrapterus known. Although not reported by Rausch and apparently has a low prevalence in northern pop- Locker (1951) or Rausch (1953) from the 31 sea ulations of sea otters from both Asia and North otters they examined from Amchitka Island America and is absent from California sea otters. (Aleutian Islands), it appears to be widely dis- The highest reported prevalence (12%) is for the tributed around the North Pacific rim from the Prince William Sound population examined in Kuril Islands in Asia to California in North the present study. The difference in D. tetrap- America (Table 2). It is probably the most prev- terus prevalence between adult male and female alent, although not necessarily the most numer- hosts in our study suggests a more frequent oc- ous, parasite of sea otters. In the 3 studies in currence of fish, the probable second interme- which more than 60 animals were necropsied diate host of this cestode, in the diet of adult (Kuril Islands, Kovalenko, 1975; California, males. Hennessy and Morejohn, 1977; Hennessy et al., Like D. tetrapterus, P. decipiens has been 1979; Prince William Sound, present study), found in the northern populations of sea otters prevalences ranged from 52% (Prince William in Asia and North America but has not been re- Sound) to >90% (California) for adult and ju- ported from California sea otters. Prevalences of venile (excluding pups) hosts combined. P. decipiens are difficult to interpret from the Orthosplanchnus fraterculus, the second most information provided in most of the Asian and frequently encountered parasite in our study, Aleutian Islands studies, but in all cases, they also was commonly found by Rausch and Lock- appear to be substantially greater (up to 35-40% er (1951) and Rausch (1953) in sea otters from or even higher in some small samples) than the Amchitka Island (prevalence, 90%), but was not 1.5% prevalence reported by us for Prince Wil- found in the Asian populations of sea otters and liam Sound sea otters. Intensity of infection also is probably also absent from the California pop- reached much higher levels in Asian and Aleu- ulation. This parasite was found also in south- tian Island host samples, with up to 200 worms east Alaska (Adams and Rausch, 1989). It ap- in some otters (Afanasev, 1941; Kovalenko, pears, therefore, to be a core parasite of only 1975). Alaskan sea otter populations. Among sea otter parasites not reported in our CCooppyyrriigghhtt ©© 22001111,, TThhee HHeellmmiinntthhoollooggiiccaall SSoocciieettyy ooff WWaasshhiinnggttoonn 164 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 64(2), JULY 1997 Table 2. Comparison of helminth parasite occurrence in sea otters (Enhydra lutris) from Asian and North American populations.* Prince Amchitka, William Aleutian Sound, Komandorski Kuril Islands Alaska California Islands Islands Trematoda (Digenea) Microphallus pirum (syn. M. enhydrae)^ Nanophyetus sp. Orthosplanchnus fraterculus Phocitrema fiisiforme Pricetrema zalophi Cestoda Diplogonoporus tetrapterus Diplogonoporus sp.t Pyramicocephalus phocarum§ Nematoda Anisakis sp. larva I Anisakis sp. larva II Pseudoterranova azarasi Pseudoterranova decipiens +tt Acanthocephala Corynosoma enhydri syn. C. macrosomum Coiynosorna strutnosum Corynosoma villosum syn. C. sp. of Rausch and Locker, 1951 and of Rausch, 1953 Polymorphic altmani Polymorphus kenti Polymorphus major * Data compiled from Rausch and Locker (1951), Rausch (1953, 1964), Van Cleave (1953), and Kenyon (1969) for the Aleutian Islands; from Golvan (1959), Neiland (1962), Rausch (1964), Kenyon (1969), and the present paper for Prince William Sound; from Hennessy and Morejohn (1977) and Hennessy et al. (1979) for California; from Barabash-Nikiforov (1935, 1947), Morozov (1940, 1957), Afanasev (1941), and Kontrimavichus (1969) for the Komandorski Islands; and from Kovalenko (1975) for the Kuril Islands. All, except O. fraterculus (a parasite of the gallbladder), are parasites of the gastrointestinal tract. t Deblock and Pearson (1969) and Deblock (1971) regarded M. enhydrae and M. pirum as distinct species, but we treat them here as a single species. Lauckner (1985) believed that the sea otter "is host for 2 species of the genus Microphallus" but accepted the use of the name M. pirum for Rausch's (1953) material from Amchitka Island. $ Probably D. tetrapterus (see Rausch, 1964), but reported as Diplogonoporus grandis by Barabash-Nikiforov (1947) and Barabash-Nikiforov et al. (1968). § Unidentified cestodes reported from a Komandorski Islands sea otter by Barabash-Nikiforov (1935) were considered by Lauckner (1985) to be "possibly attributable to Pyramicocephalus phocarum." As the parasites were not described, there is no evidence to support this suggestion. || Although C. enhydri was not reported from Amchitka Island by Rausch and Locker (1951) or Rausch (1953), it has been found in sea otters from islands to the north and south of the western end of the Alaska Peninsula, adjacent to the eastern Aleutian Islands (Van Cleave, 1953, as Corynosoma sp.; Margolis, unpubl., based on specimens collected by Dr. Karl Kenyon at Amak Island, north side of the Alaska Peninsula). Kenyon (1969) reported from 1 to 98 Corynosoma sp. (total, 271 specimens) from 8 Amchitka Island sea otters. It is possible that this collection contained some C. enhydri. # Also reported from Prince of Wales Island, southeast Alaska, by Adams and Rausch (1989). ** The gall bladder, the site of O. fraterculus infection, was not examined in the California sample of sea otters. However, it appears to be a holarctic pinniped parasite not found in California waters. tt Without providing any justification for their decision, Barabash-Nikiforov et al. (1968) referred to nematodes previously identified (Afanasev, 1941; Barabash-Nikiforov, 1935, 1947) from Komandorski Islands sea otters as P. decipiens to P. azarasi. study, the trematode Microphallus pirum (Afan- sev, 1941), and was commonly found in the in- asev, 1941) and the 3 acanthocephalan species testine of Amchitka Island sea otters by Rausch of the genus Polymorphus deserve special men- and Locker (1951) and Rausch (1953) and in tion. Microphallus pirum was originally de- California sea otters by Hennessy et al. (1979). scribed from the Komandorski Islands (Afana- It also was reported previously from a Prince CCooppyyrriigghhtt ©© 22001111,, TThhee HHeellmmiinntthhoollooggiiccaall SSoocciieettyy ooff WWaasshhiinnggttoonn MARGOLIS ET AL.—PARASITES OF SEA OTTERS 165 William Sound sea otter (Kenyon, 1969). Thus, be assumed that they occur in crabs, a frequent it is widely distributed in sea otters. In our study, item in the diet of California sea otters (Riedman this species may have been overlooked because and Estes, 1990). of its small size (<1 mm in length). The three A total of 17 (or possibly 18) parasitic hel- species of Polymorphus uniquely reported from minth species have been reported from sea otters California sea otters, with individual species throughout their distributional range. Five (or 6) prevalences up to 5% (Hennessy and Morejohn, species are represented by juvenile forms that 1977), are primarily parasites of aquatic birds. occur infrequently and have been found in 1 lo- Hennessy et al. (1979) referred to 4 (unnamed) cality only. In addition to the species of Poly- species of Polymorphus, with combined preva- morphus from California already mentioned, in- lence of 10%, among California sea otters. The dividual encounters of 2 species of Anisakis lar- parasites did not reach sexual maturity in sea vae from Kuril Islands sea otters have been doc- otters (Hennessy, 1972; Hennessy et al., 1979). umented by Kovalenko (1975). Species of these Differences between the parasite fauna of the genera apparently do not mature in sea otters, southern (California) and northern populations which are dead ends in their life cycles. The of sea otters are largely the consequence of dif- normal definitive hosts are primarily anseriform ferences in their diets. California sea otters feed birds for the Polymorphus species and cetaceans almost entirely on a variety of macroinverte- for the Anisakis species. brates, whereas Alaskan and Russian popula- Among the 12 species that use sea otters as tions of sea otters include fish as well as inver- definitive hosts, 3 (C. enhydri, M. pirum, and O. tebrates as important elements in their diet fraterculus) may be considered core species, at (Riedman and Estes, 1990). The fish-transmitted least in some sea otter populations, because of parasites include D. tetrapterus, P. decipiens, P. their high prevalence and intensity of occur- azarasi (Yamaguti and Arima, 1942), C. stru- rence. Of these 3 species, 2 use the sea otter as mosum (Rudolphi, 1802), and C. villosum (Van the only (C. enhydri) or a frequent (M. pirum) Cleave, 1953) (see Schiller [1954] and Shults definitive host. Orthosplanchnus fraterculus is a and Frost [1988]), all of which were absent from common parasite of some pinnipeds, as are 8 of California sea otters. In contrast to C. strumosum the remaining 9 species of helminths found in and C. villosum, C. enhydri, as already noted, is sea otters (Rausch, 1953; Delyamure, 1955; found commonly in both the California and Dailey and Brownell, 1972; Margolis and Dai- northern populations of sea otters and is there- ley, 1972; Shults, 1986; Shults and Frost, 1988; fore probably transmitted by 1 or more inverte- Margolis and Arai, 1989). The only exception is brates. Afanasev (1941) claimed to have found Nanophyetus sp., presumably N. salmincola juvenile C. enhydri in the cottid fish Myoxoce- (Chapin, 1926), a parasite of various piscivorous phalus stelleri from the Komandorski Islands. birds and mammals, whose metacercarial stage However, the few morphometric data he provid- occurs primarily in freshwater and anadromous ed (length 4.6 mm; swollen proboscis with 24 salmonids (Millemann and Knapp, 1970). Infec- longitudinal rows of hooks) suggest that he may tion has been reported from only 1 Komandorski actually have been dealing with C. villosum, a Islands sea otter (Afanasev, 1941), which must species not known at the time. Only 1 other par- be considered an accidental or occasional host asite, M. pirum, has been found in both northern of this parasite acquired by ingestion of an anad- and California sea otters. Transmission to sea ot- romous salmonid. ters is via shore crabs, in which the metacercar- The helminth fauna of sea otters is thus made iae develop. Schiller (1954, 1959) found meta- up principally of species acquired indirectly cercariae in Pagurus hirsutiusculus and Telmes- from pinnipeds through intermediate hosts in the sus sp. in Alaska, Tsimbalyuk et al. (1968) re- food chain, plus 2 core species, also acquired ported metacercariae in P. hirsutiusculus and through the food chain, that have not been re- Pagurus middendorffii in the littoral zone of the ported from pinnipeds. None of the parasites of Komandorski Islands, and Kulikov et al. (1970) sea otters reflect the terrestrial ancestry of this discovered metacercariae in P. middendorffii and mammal or its relationship with its extant ter- Pagurus pubescens in the northern Kuril Islands restrial-freshwater feeding relatives (Kontrimav- area. Although the metacercariae of M. pirum ichus, 1969). With respect to this dominance of have not been reported from California, it can pinniped parasites among the parasites found in CCooppyyrriigghhtt ©© 22001111,, TThhee HHeellmmiinntthhoollooggiiccaall SSoocciieettyy ooff WWaasshhiinnggttoonn 166 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 64(2), JULY 1997 the sea otter, we note that the sea otter evolved ulate that lariform birds may prove to be impor- in the North Pacific Ocean some 1 to 3 million tant natural definitive hosts of M. pirum. This years ago (Riedman and Estes, 1990) when otar- would not be surprising, because the majority of iid pinnipeds, and presumably their parasites, the 40+ species of Microphallus use aquatic were already well established there. These par- birds as definitive hosts (Deblock, 1971). How- asites were thus available for colonizing a new ever, Schiller (1954) did not find M. pirum in mammalian host when the sea otter arrived on any of 59 shorebirds of 18 species, including 2 the scene. Phocid pinnipeds invaded the North specimens of glaucous-winged gulls, examined Pacific basin about 2.5 to 3 million years ago from Amchitka Island, where sea otters were (see Hoberg and Adams [1992]) and thus their commonly found by Rausch (1953) to be in- parasites also became available for colonizing fected with this trematode. Contrary to Schiller's the sea otter early during the latter's appearance (1954) findings, Ching (1965) reported M. pirum in the North Pacific. in the white-winged scoter Melanitta deglandi The origins of the nonpinniped parasites C. from an unspecified locality on the Pacific coast enhydri and M. pirum remain speculative, al- of North America, Tsimbalyuk and Tsimbalyuk though evidence has been accumulating to sug- (1967) reported 3 species of sandpipers (Calidris gest that the latter species may be primarily a alpina, Calidris maritima, and Tringa incand) parasite of shorebirds. Corynosoma and Micro- and the glaucos-winged gull as definitive hosts phallus each comprise more than 40 species on the Komandorski Islands, Hoberg (1979) re- (Deblock, 1971; Amin, 1985). The definitive ported M. pirum from the glaucos-winged gull hosts of members of the genus Corynosoma are at Ugaiushuk Island (located on the south side marine mammals and aquatic birds, with the of the Alaska Peninsula) and Kodiak Island, and largest number of species occurring in pinni- Alekseev and Smetanina (1970) and Smetanina peds, which are the likely original hosts for spe- (1981) found the parasite common in Larus cies of this genus. Corynosoma enhydri, there- crassirostris from Peter the Great Bay (the Japan fore, presumably arose from an ancestral species Sea coast of Russia), thus reinforcing the like- parasitic in pinnipeds. Because there are no Cor- lihood of seabirds being important and perhaps ynosoma species specific for terrestrial mammals the original definitive hosts of M. pirum. In this one can rule out the possibility that C. enhydri context, it is significant that Peter the Great Bay parasitized the sea otter's ancestors before they lies outside the historical range of the sea otter. inhabited the oceans. Microphallus pirum has been found in large Acknowledgments numbers in the arctic fox (Alopex lagopus), as We thank Drs. John Blake (University of well as in the sea otter, on the Komandorski Is- Alaska, Fairbanks), Bruce Rideout (San Diego lands (Afanasev, 1941). Schiller (1959) demon- Zoo), and Randy Basaraba (Washington State strated that the glaucous-winged gull (Larus University, Pullman) for their necropsy evalua- glaucescens) could be readily infected experi- tion and collection of samples. The assistance of mentally. The worms reared in gulls were larger David Whitaker and John Bagshaw (Pacific Bi- than those reared in hamsters or recovered from ological Station) with preparation of the sea otter natural infections in sea otters (Schiller, 1959) distributional map and histological sections of or arctic foxes (Afanasev, 1941). Although sea Diplogonoporus tetrapterus, respectively, is otters did not inhabit the Kodiak Island area at gratefully acknowledged. Dr. F. G. Hochberg the time of Schiller's studies, and the other (Santa Barbara Museum of Natural History) known mammalian definitive host, the arctic kindly provided literature and information on fox, also is absent from Kodiak Island, M. pirum parasites of California sea otters. metacercariae were nevertheless commonly found there in hermit crabs {Pagurus hirsutius- Literature Cited culus). Clearly, some other definitive host was Adams, A. M., and R. L. Rausch. 1989. A revision responsible for maintaining infections at Kodiak of the genus Orthosplanchnus Odhner, 1905 with Island. It is well known that microphallid trem- consideration of the genera Odhneriella Skriabin, 1915 and Hadwenius Price, 1932 (Digenea: Cam- atodes lack host specificity in the adult stage pulidae). Canadian Journal of Zoology 67:1268- (Stunkard, 1953). 1278. The above facts led Schiller (1959) to spec- Afanasev, V. P. 1941. Parasite fauna of commercial CCooppyyrriigghhtt ©© 22001111,, TThhee HHeellmmiinntthhoollooggiiccaall SSoocciieettyy ooff WWaasshhiinnggttoonn MARGOLIS ET AL.—PARASITES OF SEA OTTERS 167 mammals of the Komandorski Islands. Uchenye d'Alaska et de Midway. Annales de Parasitologie Zapiski Leningradskogo Gosudarstvennogo Univ- Humaine et Comparee 34:288-321. ersiteta 74, Seriya Biologicheskikh Nauk 18:93- Hennessy, S. L. 1972. The intestinal parasites and 117. (In Russian with German summary.) diet analysis of the southern sea otter. M.A. The- Alekseev, V. M., and Z. B. Smetanina. 1970. Trem- sis, California State University, Hayward, Califor- atodes of piscivorous birds from the Rimsky-Kor- nia. 44 pp. sakov Islands. In V. A. Leonov, ed. Parasitological Hennessy [Hennessey], S. L., F. G. Hochberg, G. V. and Zoological Investigations of the Far East. Morejohn, and K. L. Wagner. 1979. Intestinal Uchenye Zapiski Dalnevostochnyi Gosudarstven- parasites of the sea otter (Enhydra lutris) in Cal- nyi Universitet 16:96-103. (In Russian.) ifornia waters. Program and Abstracts, Sea Otter Amin, O. M. 1985. Classification. Pages 27-72 in D. Workshop, jointly sponsored by Santa Barbara W. T. Crompton and B. B. Nickol, eds. Biology Museum of Natural History, California Depart- of the Acanthocephala. Cambridge University ment of Fish and Game, and U.S. Fish and Wild- Press, Cambridge, U.K. life Service, 23-25 August 1979, Santa Barbara, Barabash-Nikiforov, I. I. 1935. The sea otters of the California, pp. 16-17. Commander Islands. 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