7

PREFACE

The first International Symposium on the Biology papers were read by title and are included either in of the Seal was held at the University of Guelph, On­ full or abstract form in this volume. The 139 particip­ tario, Canada from 13 to 17 August 1972. The sym­ ants represented 16 countries, permitting scientific posium developed from discussions originating in Dub­ interchange of a truly international nature. lin in 1969 at the meeting of the Marine In his opening address, V. B. Scheffer suggested that Committee of the International Council for the Ex­ a dream was becoming a reality with a meeting of ploration of the Sea (ICES). The culmination of such a large group of biologists. This he felt three years’ organization resulted in the first interna­ was very relevant at a time when the relationship of tional meeting, and this volume. The president of ICES marine mammals and man was being closely examined Professor W. Cieglewicz, offered admirable support as on biological, political and ethical grounds. well as honouring the participants by attending the The scientific session commenced with a seven paper symposium. section on evolution chaired by E. D. Mitchell which The programme committee was composed of experts showed the origins and subsequent development of representing the major international sponsors. W. N. this amphibious group of higher vertebrates. Many of Bonner, Head, Seals Research Division, Institute for the arguments for particular evolutionary trends are Marine Environmental Research (IMER), represented speculative in nature and different interpretations can ICES; A. W. Mansfield, Director, Arctic Biological be attached to the same fossil material. Readers of this Station, Fisheries Research Board of Canada (FRB) volume should be aware of such differences when read­ represented the International Commission for North­ ing the papers in this section. The twelve papers of west Atlantic Fisheries (ICNAF); and K. S. Norris, S. H. Ridgway’s section on functional anatomy illus­ Director, Marine Council Executive Com­ trated the fundamental structure of the seal, as well mittee, represented the International Biological Pro­ as its associated control mechanisms. R. J. Schusterman gram (IBP). The Food and Agriculture Organization followed this theme by introducing ten papers on be­ of the United Nations (FAO) also offered its support haviour. He established a major focus on social or­ to the programme and ICNAF has contributed to the ganization and communication and their association financing of this volume. with the functional anatomy of the . D. E. Sponsors of national origin were the Fisheries Re­ Sergeant chaired the population dynamics section of search Board of Canada (FRB), the National Re­ seven papers, covering the modelling of populations search Council of Canada (NRCC), the Canadian and method of analysis of seal populations around the National Sportsmen’s Show (CNSS), the World Wild­ world. In the fifth section, J. R. Geraci, by means of life Fund (Canada) (WWF), and the University of papers and a panel discussion dealt with the care and Guelph. management of captive pinnipeds. W. N. Bonner co­ In his preliminary remarks Professor Ronald intro­ ordinated a presentation in the broad area of ecology, duced the representatives of these groups; namely J. R. and was able to bring together studies on environmen­ Weir, Chairman, Fisheries Research Board of Canada; tal factors and their associated behavioural and gene­ S. Bata, International Director and J. S. McCormack, tic control systems. The physiology section was chaired Director, World Wildlife Fund (Canada); and R. T. by H. T. Andersen, his introductory remarks forming D. Birchall, President, Canadian National Sportsmen’s the initial paper of the section. The other six papers Show and a Director of WWF (Canada). of his section emphasized the underwater responses of W. C. Winegard, President of the University of seals. The final and general section, chaired by J. E. Guelph, welcomed participants to the symposium and King, offered a broad coverage of several of the more commented particularly on how pleased he was to interesting areas in various disciplines. welcome representatives from so many countries. Later, A. W. Mansfield acted as rapporteur for the entire at a banquet sponsored by the Department of the En­ programme, and his report stressed the need for con­ vironment, Canada, he offered an invitation to the tinued cooperation by all biologists so that they might group to return in 1975 for a Second International understand seals and their importance to environmen­ Seal Symposium. tal studies. Altogether 62 papers were presented. A further 14 This volume includes with one exception, those pa- 8 K. Ronald pers either presented, read by title, or abstracted, but mammals of the world’ by D. W. Rice and V. B. the continuing discussion on the biology of the seals Scheffer (U.S. Fish and Wildlife Service, Washing­ led to one further paper that is included here. Some ton, 1968) has been used as the standard reference on of the discussion was formal and, where recordable, is nomenclature. included here, but by far the greater part of discussion The work of the chairmen of each of the seven sec­ was informal and hence must remain as extremely tions of this volume is especially recognized. As well, valuable, but merely mental recollections of the par­ the convenor wishes to thank the programme com­ ticipants in the symposium. mittee for their ability to support a somewhat unortho­ The symposium achieved its purpose of bringing dox procedural system, and particularly the sponsors together scientists interested in the Pinnipedia and it ICES, ICNAF, IBP, CNSS, FRB, NRCC, WWF (Ca­ offered leads into the international examination of nada), FAO, and the University of Guelph for their marine mammals. valuable financial assistance. The editors with little apology recognized that they The convenor is most grateful to Mr. H. Tambs- have not reached a completely uniform format in this Lyche, General Secretary of ICES, for his advice and volume since they have allowed use of both English encouragement from the embryonic stages of the sym­ and metric systems of measurement and both English posium to the publication of the proceedings; he also and North American word usage for the sake of har­ recognizes the considerable amount of expert help pro­ mony. The main editorial structure has been the con­ vided by A. W. Mansfield in co-editing this volume. sistency of usage throughout a particular paper. Finally, the effort put into both the symposium and Attempts have also been made to attain a fairly this volume by Mrs. Ginny Bandesen has been beyond uniform for the species, but where there has measure, but I hope that she will accept the results of been any doubt caution has not overridden clarity. As the symposium recorded here as tangible proof of her in other mammalian groups, the systematics of the most valuable contribution. To the members of the Pinnipedia are still open to much interpretation. The Dean of the College of Biological Science’s office, the references are cited according to an Annotated Biblio- university support staff and our host Dr. W. C. Wine- praphy on the Pinnipedia*. The ‘List of the marine gard, I express on behalf of the participants and my­ self, our sincerest thanks. * Ronald, K., L. M. Hanly and P. J. Healey, College of Bio­ K. Ronald, logical Science, University of Guelph, Ontario, Canada. Convenor

The following have kindly acted as Discussion Care and Management Section Leaders of the different Sections and also assisted in J. R. Geraci the editing of the contributions: Department of Zoology, University of Guelph, Guelph, Ontario, Canada. Evolution Section Ecology Section E. D. Mitchell Arctic Biological Station, Fisheries Research Board W. N. Bonner of Canada, Ste. Anne de Bellevue, Quebec, Canada. Seals Research Division IMER, c/o Fisheries Labora­ tories, Lowestoft, Suffolk, England.

Functional Anatomy Section Physiology Section S. H. Ridgway H. T. Andersen School of Anatomy, University of Cambridge, Nutrition Institute, University of Oslo, Blindern, Cambridge, England. Oslo, Norway.

Behaviour Section General Session R. J. Schusterman J . E. King Department of Psychology, California State University Department of Zoology, University of New South Hayward, California 94542, U.S.A. Wales, Kensington, N.S.W., Australia.

Population Dynamics Section Summary D. E. Sergeant A. W. Mansfield (Rapporteur) Arctic Biological Station, Fisheries Research Board of Arctic Biological Station, Fisheries Research Board Canada, Ste. Anne de Bellevue, Quebec, Canada. of Canada, Ste. Anne de Bellevue, Quebec, Canada. 338

Rapp. P.-v. Réun. Cons. int. Explor. Mer, 169: 338-352. 1975.

THE DISTRIBUTION AND INTRASPECIFIC VARIATION OF HELMINTH PARASITES IN PINNIPEDS

M. D . D a il e y Department of Biology, California State University, Long Beach, California, U.S.A.

INTRODUCTION Distribution of otariids is limited to the subantarctic Annotated lists of pinniped parasites have been pub­ in the New Zealand and Australia area (Hookers sea lished since the time of Linnaeus in 1758. They have lion, JPhocarctos hookeri Gray, 1844; Australian sea usually been restricted to parasites of various pinniped lion, cinerea Peron, 1816), to South Ame­ groups or specific geographical locations. The present rica (South American Otaria flavescens Shaw, paper presents a comparative approach, emphasizing 1800) and to the west coast of North America, the the occurrence of helminths in sympatric pinniped Aleutian Islands and the Sea of Okhotsk (California populations and their intraspecific variation. sea lion, californianus Lesson, 1828; Steller The monograph of Delyamure (1955) was used as or northern sea lion, Eumetopias jubatus Schreber, a basis for tabulating helminths from five subfamilies 1776). of pinnipeds (Arctocephalinae, Cystophorinae, Otarii­ nae, , ) and one family (Odo- OTARIINAE benidae). The classification used by Rice and Scheffer The helminths reported from Otariinae are present­ (1968) and King (1964) was adopted throughout this ed in Tables 83 and 84. In Delyamure (1955), the work. table for this subfamily listed nine helminth species belonging to seven genera for E. jubatus, seven species OTARIIDAE from six genera for Z. calif ornianus, three species from The otariids are separated into two subfamilies, the three genera for O. flavescens and no reports for either sea lions Otariinae and the fur seals Arctocephalinae. Neophoca cinerea or Phocarctos hookeri.

Table 83. Comparison of helminth parasites in Otariinae (Cestoda and )

Otariinae

Species of Helminth Eumetopias Zalophus Otaria Neophoca Phocarctos jubatus californianus flavescens cinerea hookeri

Cestoda Adenocephalus pacificus...... A. phocarum...... Anophyrocephalus ochotensis...... Diphyllobothrium arctocephalinum . D.pacificum ...... D . scoticum...... Diplogonoporus fasciatus ...... + D. tetrapterus...... + Phyllobothrium delphini...... Acanthocephala Bolbosoma bobrovi...... australe...... C. hamanni...... C. obtuscens...... C. osmeri...... + C. semerme...... I C. strumosum...... + C. villosum ...... The distribution and intraspecific variation of helminth parasites in pinnipeds 339

Table 84. Comparison of helminth parasites in Otariinae (Trematoda and Nematoda)

Otariinae

Species of Helminth Eumetopias £ alophus Otaria Neophoca Phocarctos jubatus californianus flavescens cinera hookeri

Trematoda Pricetrema zalophi...... Stephanoprora denticulata Strictodora ubelakeri . . . . Zalophotrema hepaticum . Heterophyes heterophyes...... j- Schistosoma mansoni...... 4- S. haematobium ...... -t-

Nematoda Anisakis patagonica...... + _j_ A. sim ilis...... + -Î- 4 - A. simplex...... + A. tridentata...... -f Contracaecum osculatum...... 4 - + + 4 . C. rectangulum...... + Dipetalonema odendhali...... 4 - Dirofilaria im m itis...... + Parafilaroides decorus...... + P. nanus...... + P. prolificus...... + P. sp...... + Terranova decipiens...... -f -f + + Uncinaria ham iltoni...... + 4 . u . sp...... +

Currently in E. jubatus there are 18 species belong­ Cestoda ing to 11 genera: (Cestoda) Adenocephalus, Anophry- Some interesting observations can be made from ocephalus, Diphyllobothrium. Diplogonoporus; (Ne­ these comparisons. A common species Diphyllobothri­ matoda) Anisakis, Contracaecum, Parafilaroides, Ter­ um pacificum is shared by Eumetopias and Zalophus, ranova, Uncinaria; (Acanthocephala) Bolbosoma, Co- while other members of the same genus D. arctocepha- rynosoma. Trematodes have never been reported from linum and D. scoticum are shared by Neophoca and this host. Otaria respectively. The occurrence of D. pacificum In Z. californianus there are now 17 species be­ is most likely explained by the overlapping distribution longing to 15 genera: (Cestoda) Diphyllobothrium: of the Steller and California sea lions, which share (Nematoda) Anisakis, Contracaecum, Dirofilaria,Dipe­ common hauling-out areas, such as Ano Nuevo Island. talonema, Parafilaroides, Termnova, Uncinaria; (Ac­ This probably explains the occurrence of the same para­ anthocephala) Corynosoma; (Trematoda) Pricetrema, site in the northern Callorhinus ursinus (Lin­ Stictodora, Stephanoprora, Zalophotrema, Hetero­ naeus, 1758) (Table 85) since all three species come to­ phyes, Schitosoma. gether on San Miguel Island off the California coast. The Helminths reported from O. flavescens now include South American or Falkland fur seal, 12 species from seven genera: (Cestoda) Diphyllobo­ australis (Zimmerman, 1783) is also reported to have thrium, Phyllobothrium (larval stage); (Nematoda) D. pacificum (Table 85) which may have been derived Anisakis, Contracaecum, Terranova, Uncinaria; (Ac­ from Zalophus at the Galapagos Islands. Neophoca anthocephala) Corynosoma; no trematodes have been shares its species of Diphyllobothrium (D. arctocephali- found. Finally N. cinera has three species from three num )with three species of fur seals, the Australian genera: (Cestoda) Diphyllobothrium; (Nematoda) Con­ fur seal, Arctocephalus doriferus Wood Jones, 1925; tracaecum; (Acanthocepala) Corynosoma while P. the South African fur seal, A. pusillus Schreber, 1776 hookeri has only one helminth, the , Terra­ and the Tasmanian fur seal, A. tasmanicus Scott and nova decipiens. Lord, 1926 (Table 85). This parasite thus appears to

22' 340 M. D. Dailey

Table 85. Comparison of helminth parasites in Arctocephalinae (Cestoda and Acanthocephala)

Arctocephalinae

Species of Helminth Arctocephalus A. A. A. A. A Callorhinus australis forsteri doriferus pusillus tasmanicus tropicalis ursinus

Cestoda Adenocephalus pacificus...... + A. septentrionalis...... Diphyllobothrium arctocephalinum...... + + + D. atlanticum...... + D. krooyi...... + D. krotovi...... D. macrophallos...... D. pacificum...... + D. sp...... Diplogonoporus tetrapterus...... Phyllobothrium delphini...... + P. sp...... +

Acanthocephala Bolbosoma bobrovi...... B. nipponicum...... Corynosoma au strale...... C. osculatum...... + C. semerme...... + C.'strumosum...... C. ventronudum...... C. villosum ...... be endemic in fur seals of the Southern hemisphere. pinnipeds, hookworms have been reported from only Neophoca shares its breeding grounds with A. dori­ four species, three sea lions (Otaria, Zalophus and ferus. Eumetopias) and one fur seal (Callorhinus), all of which inhabit overlapping geographical areas from the Nematoda Falkland Islands, up the west coast of the Americas to the Bering Sea. The adult worms in these In the Otariinae, the are represented by occur only in the pups, an apparent adaption to the the universal genera Anisakis, Contracaecum and Ter­ aquatic environment. Uncinaria sp. in Zalophus ap­ ranova, one of which occurs in every species of pinni­ pears to be an intermediate between U. lucasi of Cal­ ped except three, the , Histriophoca fasciata lorhinus and U. hamiltoni of Otaria (for further dis­ (Zimmerman, 1783), the New Zealand fur seal, Arcto­ cussion see Dailey and Hill (1970) and Margolis and cephalus forsteri (Lesson, 1928) and the Guadalupe Dailey (1972). Other examples of parasite interchange fur seal, A. philippii (Peters, 1866) in which no para­ between terrestrial animals and pinnipeds are more sites are reported. The wide distribution of these frequently seen now that increased numbers of pinni­ ascarids is probably due to the lack of host specificity peds are kept in captivity, particulary Zalophus. Di- in their intermediate ( and teleost) and petalonema immitis was reported from a zoo definitive hosts. Other genera of nematodes shared by in New Orleans, Louisiana, an endemic area for that Eumetopia and Zalophus also appear to be a product parasite in dogs. Heartworm has not been recorded of mixing populations. The lungworms in the genus from any wild otariids to date; however the tissue Parafilaroides are reported from both hosts, but pri­ filarid Dipetalonema odendhali occurs in a high per­ marily only from those Steller sea lions examined along centage of examined Zalophus (personal observation). the California coast. These lungworms and their host relationship will be discussed later under interspecific T rematoda variation. Hookworms of the genus Uncinaria present an inter­ A strange situation is presented by this group of esting situation. Parasites of this genus are also found parasities since only Zalophus is infected. Delyamure in terrestrial carnivores, primarily canids, where the (1955) pointed out that up until the time of his writing sexually mature worms occur in the adult animal. In all trematodes were recovered from sea lions living The distribution and intraspecific variation of helminth parasites in pinnipeds 341

Table 86. Comparison of helminth parasites in Arctocephalinae (Trematoda and Nematoda)

Arctocephalinae

Species of Helminth Arctocephalus A. A. A. A. A. Callorhinus australis forsteri doriferus pusillus tasmanicus tropicalis ursinus

Trematoda Cryptocoty le jejuna. . . . Phocitrema fusiforme. . Pricetrema zalophi.. .. Zolophotrema hepaticum

Nematoda Anisakis pacificus...... o_ A. sim ilis...... + A- SP...... + Contracaecum callotariae...... _l_ C. corderoi ...... + C. osculatum...... + -j- _j_ _j_ _l C. rectangulum...... -f- Dipetalonema spirocauda...... _1_ Phocanema decipiens...... _l_ Porrocaecum callotariae...... _j_ P. sulcatum...... -f Terranova decipiens...... + + _j_ Uncinaria lucasi...... +

in the Washington Zoo and none had been taken Hill, 1970; Delyamure, 1955; Dougherty and Herman, under natural conditions. This is no longer the situ­ 1947; Faust, 1937; Forssell, 1904; Fujita, 1921; H er­ ation. The author has found P. zalophi, Z. hepaticum man, 1942; Johnston, 1937; Johnston and Best, 1937; and S. ubelakeri in non-captive animals. Only two King, 1964; Krabbe, 1878; Kreis, 1938; Krotov and species, P. zalophi and Z. hepaticum appear to be Delyamure, 1952; Lincicome, 1943; Linstow, 1880, endemic parasites of pinnipeds, where Stictodora and 1907; Margolis, 1956; Margolis and Dailey, 1972; Stephanoprora are commonly found in birds. The Markowski, 1952; Monticelli, 1890; Nybelin. 1931; Heterophyes and Schistosoma infections were both Perry, 1967; Price, 1932; Raillet and Henry, 1912; reported from zoo animals and are obviously a product Rennie and Reid, 1912; Rudolphi, 1802; Skrjabin, of urban captivity. 1959, 1965; Stunkard, 1948; Stunkard and Alvey, 1929; van Cleave, 1953. Acanthocephala These are well represented in the Otariinae, with all but P. hookeri having at least one species. A total ARCTOCEPHALINAE of eight acanthocephalan species are represented in The fur seals offer an unusual comparison since two genera, all but one B. bobrovi belonging to the only Callorhinus ursinus is a northern animal, while genus Corynosoma. Only two species of the genus Bol- all seven species of Arctocephalus have a southern bosoma, commonly a cetacean parasite, have been distribution. Unfortunately detailed comparison is re­ reported from pinnipeds, B. bobrovi and B. nipponicum. stricted by the lack of work done on certain species: These worms appear to be endemic to the Bering sea no reports on A. philipii or A. forsteri,1 and only a few area occurring in three widely distributed pinniped reports on the South African species A. pusillus; the hosts, E. jubatus, C. ursinus and the , Pus a Australian fur seal, A. doriferus; the Tasmanian fur hispida Schreber, 1775. In the genus Corynosoma, seal, A. tasmanicus; and the Kerguelen fur seal, A. Otaria and Neophoca share the species C. australe, tropicalis Gray, 1872. A moderate amount of study and Eumetopias and Zalophus share C. strumosum. has been conducted on A. australis and C. ursinus has been well studied. Bibliography 1 Johnston (1937) reports parasites'from “the Australian hair Baylis, 1916, 1920, 1933; Bose, 1805; Ciurea, 1933; seal” which he calls A. forsteri. King (1964) lists these under the Dailey, 1969; Dailey and Brownell, 1972; Dailey and Australian fur seal, A. doriferus. 342 M. D. Dailey

Cestoda 1915; Delyamure, 1955; Delyamure and Parukhin, 1968 ; Forssell, 1904; Goto and Ozaki, 1930; Johnston, Diphyllobothrium pacificum is shared by A. australis 1937; Johnston and Best, 1937; Keyes, 1965; King and C. ursinus while D. arctocephalinum has been 1964; Krabbe, 1878; Krotov and Delyamure, 1952; found in A. doriferus, A. pusillus and A. tasmanicus. Leidy, 1858; Lent and Freitas, 1948; Linstow, 1907; These worms were also reported from members of the Lühe, 1911; Markowski, 1952; Neiland, 1961; Nicoll, Otariinae and are discussed under that group. The 1923; Nybelin, 1931; Price, 1932; Rudolphi, 1802, larval stage of Phyllobothrium delphini, commonly a 1819; Skrijabin, 1959; Stiles and Hassall, 1912; Stun­ cetacean parasite in this stage and of elasmobranch kard, 1948; Stunkard and Alvey, 1929; van Cleave, fishes as adults, has been reported from three arcto- 1953; Yamaguti, 1939. cephalines. This parasite has also been reported from Otaria and two species of Monachinae (Table 91); thus it appears to be an incidental parasite PHOCIDAE AND of pinnipeds in the southern hemisphere. The ne­ PHOCINAE matodes shared by Callorhinus and Arctocephalus are The northern seals belonging to this sub-family con­ the ubiquitous C. osculatum and T. decipiens. The tain 37 genera and 62 species of helminths. There are only non-ascarid species reported for this group are no reports for Histriophoca fasciata, but the seven re­ the filarid Dipetalonema spirocauda and the hook­ worm Uncinaria lucasi, both from C. ursinus. W hether maining species have been quite well studied. representatives of these nematode groups are present in Arctocephalus and just have not been found, or Cestoda whether the host environment is unsuitable for sustain­ These are represented by nine species of Diphyllo­ ing the parasite is unknown. The possibility of A. au­ bothrium, three species of Diplogonopornus and one stralis contacting these parasites seems high owing to each of the remaining genera (Table 87). Common its zoogeographic association with Otaria and Zalo­ species are found in the harbour seal, vitulina phus in the Galapagos Islands. Linnaeus, 1758; ringed seal, hispida; , Erignathus barbatus Erxleben, 1777 and , Pagophilus groenlandicus Erxleben, 1777. This large Trem atoda number of common cestodes results from the wide­ There are no common genera in the arctocephalines. spread distribution of pelagic and teleost Callorhinus has three species that are shared with fish that are the intermediate hosts of diphyllobothriids Zalophus and members of the Phocinae (Table 92) in northern seas. Further evidence of the success of and are probably endemic in the northern hemisphere. Diphyllobothrium is its wide representation in the Zalophotrema hepaticum, also a common parasite in Monachinae of the southern hemisphere (Table 91). Zalophus, is shared by A. australis but absent from Of the eight genera of cestodes listed, only two Ano- Callorhinus. This could indicate that the parasite is phryocephalus and Pyramicocephalus appear to be endemic to the southern range of Zalophus, extending exclusively pinniped parasites. Trigonocotyle is prim ­ to the Galapagos Islands area where large numbers of arily found in toothed whales; Polypocephalus from Zalophus and A. australis mingle. elasmobranchs ; Diplongonoporus is shared with whales, sea otter and man, and Schistocephalus is Acanthocephala endemic in piscivorous birds. The two relict species of Phocinae, the Caspian seal, Only a limited amount of comparative information Pusa caspica Gmelin, 1788 and the , Pusa is available. Two species of the previously mentioned sibirica Gmelin, 1788 have been well examined but genus Bolbosoma are found only in Callorhinus. Two contain few parasites. These two animals will be con­ species of the genus Corynosoma are shared by Arcto­ sidered later in this section. cephalus and Callorhinus, while one species is shared by two arctocephalines. Owing to the wide distribution Nematoda of these acanthocephalans in all groups of pinnipeds, Delyamure (1955) listed seven genera and nine spe­ it is difficult to draw any conclusions from these cies of nematodes from the Phocinae, but this has now infections. increased to 16 genera and 21 species (Table 89). Other than the common ascarid types (Anisakis, Con­ Bibliography tracaecum, Phocascaris, Phoconema, Terranova) we Anderson, 1959; Baird, 1853, Baylis, 1916, 1920; find representatives of five other superfamilies (Diocto- Baylis and Daubney, 1923; Bcsc, 1802; Cholodkovsky, phymoidea, , Metastrongyloidea, Strongy- The distribution and intraspecific variation of helminth parasites in pinnipeds 343

Table 87. Comparison of helminth parasites in Phocinae (Cestoda)

Phocinae

Species of Helminth Phoca Pusa P. P. Erignathus Halichoerus Pagophilus Histriophoca vitulina hispida caspica sibirica barbatus grypus groenlandicus fascia ta

Cestoda Anophryocephalus anophrys...... + Diphyllobothrium alascense...... + D . cordatu m ...... + + D. hians...... D. lanceolatum...... -f + + + D. latum ...... + + D . macrocephalus...... + D. osm eri...... D. phocarum...... + D . schistochilus...... + D. sp...... Diplogonoporous fasciatu s...... + D. mutabilis...... -f D. tetrapterus...... + + + Polypocephalus tortus...... + Pyramicocephalus phocarum...... -j_ + Schistocephalus solidus...... + + Trigonocotyle skrjabini...... + -l-

Table 88. Comparison of helminth parasites in Phocinae (Trematoda and Acanthocephala)

Phocinae

Species of Helminth Phoca Pusa P. P. Erignathus Halichoerus Pagophilus Histriophoca vitulina hispida caspica sibirica barbatus grypus groenlandicus fasciata

Trematoda Ciureana badamschimi...... + Cryptocotyle lin g u a ...... ■ ...... + + + Echinostoma acanthoides...... + + Mesorchis advena...... Metorchis albidus......

Microphallus orientalis...... ■ f

Orthosplanchnus arcticus...... + + 0. frater cuius...... - f

Opisthorchis felineus...... + 0. tenuicollis......

Phocitrema fusiforme...... + + _i_ Pseudamphistomum truncatum...... + + + - f Rossicotrema venustum...... + Zo-lophotrema hepaticum...... +

Acanthocephala Bulbosoma nipponicum...... _L Corynosoma falcatum ...... + -f. C. hadweni...... -f. X

C. magdaleni...... + 4 -

C. reductum...... +

C. semerme...... + + -X. C. strumosum...... + __

C. validum ...... + C. ventronudum...... +

C. wegeneri...... + 344 M. D. Dailey

Table 89. Comparison of helminth parasites in Phocinae (Nematoda)

Phocinae

Species of Helminth Phoca Pusa P. P. Erignathus Halichoerus Pagophilus Histriophoca vitulina hispida caspica sibirica barbatus grypus groenlandicus fasciata

Nematoda Anisakis rosmari...... + A. schupakovi...... + A. sim ilis...... + A. sp...... + Ascaris dehiscens...... + Contracaecum osculatum...... + + + C. sp...... + Dioctophyme renale...... Dipetalonema spirocauda...... + Dirofilaria spirocauda...... + Eustrongyloides excisus...... + Halocercus gymnurus...... + + Otostrongylus circumlitus...... + + + Parafilaroides arcticus...... + P. caspicus...... + P. gymnurus...... + Phocascaris netsiki...... + + P. phocae...... + + Phoconema decipiens...... + Skrjabinaria spirocauda...... + + Terranova decipiens...... - • + + + + ' Trichinella spiralis...... + + Uncinaria lucasi...... + ______

Table 90. Comparison of helminth parasites in Monachinae (Trematoda, Nematoda and Acanthocephala)

Monachinae

Species of Helminth Monachus M . M . Leptonychotes Lobodon Hydrurga Ommatophoca monachus schauinslandi tropicalis weddelli carcinophagus leptonyx rossi

Trematoda Ogmogaster antarcticus...... + + 0. plicatus...... + + Orthosplanchnus sp...... +

Nematoda Anisakis pegreffii...... A. sim ilis...... 4* Contracaecum ogmorhini...... + C. osculatum...... + + + C. radiatum...... + + + + C. rectangulum...... -f + + C. stenocephalum...... + C. turgidum...... Parafilaroides hydrurgae...... + Phocascaris hydrurgae...... + Terranova decipiens...... +

Acanthocephala Corynosoma antarcticum...... + C. australe...... + C. bullosum...... + C. clavatum...... + C. hamanni...... + C. rauschi...... + C. sipho...... The distribution and intraspecific variation of helminth parasites in pinnipeds 345

Table 91. Comparison of helminth parasites in Monachinae (Cestoda)

Monachinae

Species of Helminth Monachus M . M . Leptonychotes Lobodon Hydrurga Ommatophoca monachus schauinslandi tropicalis weddelli carcinophagus leptonyx rossi

Cestoda Baylisia baylisi...... + Bothriocephalus sp...... + Cysticercus cellulosae...... 4- Diphyllobothrium archeri...... 4 - D. cameroni...... + D. coniceps...... + D . elegans...... + D. hians...... + + D. lanceolatum...... + D. lashleyi...... 4- D. latum...... + D . m obile...... 4 - + D. perfoliatum...... 4- D. quadratum...... + + D. rufum...... + D. scoticum...... 4 . D . sco tti...... D . tectum ...... + 4 . D. ventropapillatum...... 4 . D . wilsoni...... 4 . 4- 4 . Diplogonoporus tetrapterus...... 4 - Glandicephalus antarcticus...... 4 . G. perfoliatus...... 4 - Phyllobothrium delphini...... 4 - 4 _

Table 92. Comparison of helminth parasites in Cystophorinae and Odobenidae (Trematoda and Cestoda)

Cystophorinae and Odobenidae

Species of Helminth Cystophora Mirounga M . leonina Odobenus cris ta ta angustirostris rosmarus

Trematoda Cryptocotyle lin g u a ...... Metorchis albidus...... Microphallus orientalis...... + Odhneriella rossica...... Opisthorchis tenuicollis...... + Orthosplanchnus fraterculus...... Pseudamphistomum truncatum...... + Zalophotrema hepaticum ......

Cestoda Anophryocephalus atiophrys...... + Baylisiella tecta...... Diphyllobothrium cor datu m ...... D . latum...... - f ; D . pterocephalum...... + D . romeri ...... + D . tectum ...... + Diplogonoporus tetrapterus...... + Pyramicocephalus phocarum...... + 346 M. D. Dailey

Table 93. Comparison of helminth parasites in Cystophorinae and Odobenidae (Nematoda and Acanthocephala)

Cystophorinae and Odbenidae

Species of Helminth Cystophora Mirounga M . leonina Odobenus cristata angustirostris rosmarus

Nematoda Anisakis alata...... A . bicolor...... t A. patagonica...... + A.rosm ari...... + A. sim ilis...... + Contracaecum osculatum...... + + C. radiatum...... C. rectangulum...... + Dirofilaria im m itis...... + Filaria sp...... Phocascaris cytophorae...... + P. osculatum...... + P. phocae...... + Skrjabinaria spirocauda...... + Terranova decipiens...... + Trichinella spiralis...... Uncinaria hamiltoni...... +

Acanthocephala Corynosoma bullosum...... + t C. clavatum...... C. semerme...... + C. strumosum...... + C. validu m ...... C. sp...... +______loidea, Trichuroidea), more than in any other sub­ the northern , Mirounga angustirostris family of Pinnipedia. However, only Otostrongylus, Gill, 1866, can most likely be attributed to their south­ Parafilaroides and Skrjabinaria seem to be unique to ern distribution into waters off Baja California, where pinnipeds. Dioctophyme, Dipetalonema, Dirofilaria, the parasite is endemic. Orthosplanchnus is universal, Eustrongyloides (a synonym of Dioctophyme according being found in both hemispheres. to Yamaguti, 1961), Halocercus, Trichinella and Un­ cinaria are all found in other groups of mammals. Acanthocephala Two genera and 10 species are represented in the Trematoda Phocinae. B. nipponicus has been previously discussed Delyamure (1955) compared northern and southern under the Otariinae. Of the remaining nine species true seals and found the northern group infected with only five are reported from this subfamily. The most eight of the 10 genera represented at that time. Cur­ commonly shared species are C. semerme and C. stro- rently there are 15 genera reported for these groups mosum, which are also found in Arctocephalinae, (Tables 88, 90, 92), of which five (Echinostoma, Cystophorinae and Otariinae but are absent in Mona­ Mesorcha, Phocitrema, Rossicotrema, Ciureana (a chinae (Tables 85, 93, 83, 80). The large number of synonym of Cryptoctyle according to Yamaguti, 1958) species unique to this group can probably be accounted are unique to Phocinae, and one (Ogmogaster) unique for by intraspecific variation in response to closely to Monachinae. The Cystophorinae share all five of related but different hosts. The amphipods used as their species with Phocinae, and the Monachinae first intermediate hosts in acanthocephalan life cycles share one genus. However, Zalophotrema is the only are usually fairly non-specific and widely distributed. genus that is unique to the Pinnipedia. Orthosplanch- The same can be said for the fishes which serve as nus is primarily a parasite of pinnipeds but has also the second intermediate hosts. Therefore universal been reported from sea otters (Rausch, 1953). All species such as C. semerme and C. stromosum would others are accidental parasites of pinnipeds, being be expected with minimal need for spéciation in the found typically in other mammals or marine birds. populations concerned. The sharing of Z. hepaticum between P. vitulina and The two members of the Phocinae with the least The distribution and intraspecific variation of helminth parasites in pinnipeds 347

number of parasites and smallest geographical distri­ seals and Antarcdc seals. Owing to their low numbers bution are the landlocked Caspian and Baikal seals. and reduced gregarious nature, monk seals are not Delyamure (1955) mentions various workers who have well represented by helminth parasites. None have attempted to use the helminth fauna to solve the been reported from M. tropicalis and only four from question of the origin of these two species. In compar­ M. schauinslandi. In contrast, the Antarctic species ing the helminths of the Caspian seal with those of minths, with only the two ascaroids, Contracaecum northern seals, there are no common species of cestodes osculatum and Terranova decipiens in common with or nematodes, but common trematodes and acantho- Antarctic forms, and one cestode, D. hians shared with cephalans occur. Delyamure cites Dogiels’ (1947) ex­ M. schauinslandi. In contrast, the Antarctic species planations that the original parasite fauna of relict have a number of common helminths. Leptonychotes animals is reduced or lost and is replaced by a few and Lobodon share two trematode species of Ogmo- species not normally infecting seals. This is borne out gaster, which is also a common genus in whales by the addition of non-pinniped trematodes such as (Table 91). Mesorchis and Ciureana and the namatode Eustrong- lytoides. The Baikal seal has a single helminth para­ Cestoda site, Contracaecum osculatum. From comparison of Among the 13 species of cestodes listed for the Ant­ this parasite with specimens of C. osculatum taken arctic seals is Baylisia which is unique to the crab- from the Caspian and northern seals Mozgovoi and eater seal Lobodon carcinophagus. The has Ryzhikov (1950) concluded that the Baikal seal was four cestodes, of which D. scotti and D. antarcticus are more similar to northern seals than to the Caspian unique to it. The other two diphyllobothriids, D. mo­ seal. bile and D. wilsoni are shared with Lobodon, and Lobodon and Hydrurga respectively. Lobodon and Bibliography Hydrurga have four species and two genera in com­ mon. The wide distribution of Diphyllobothrium and Ball, 1930; Baylis, 1916, 1920, 1932; Belopolskaya, the catholic feeding habits of these seals would tend 1960; Bruyn, 1933; Creplin, 1825; Delyamure, 1955; to account for the infections. Delyamure et al., 1964; Delyamure and Alegseev, 1966; Diesing, 1850; Dogiel, 1947; Dougherty, 1946; Nematoda Duncan, 1956; Fabricius, 1780; Forssell, 1904; Ger- manos, 1895; Goto and Ozaki, 1930; Guiart, 1935; Species infecting members of the Monachinae are Heinze, 1934; Höst, 1932; Johnston et al., 1966; all ascaroids except for the lungworm Parafilaroides Kenyon, 1962; King, 1964; Kurochkin, 1958; Kur­ hydrurgae (Table 90). This appears to be the only ochkin and Zablotskii, 1958; Leuckart, 1863; Lühe, reported occurrence of this genus in the southern 1910; Lyster, 1940; Montreuil, 1958; Mozgovoi and hemisphere and presents the question of why it is Ryzhikov, 1950; Muller, 1776; Neiland, 1962; Odhner, found only in the Hydrurga leptonyx? If 1905; Owen, 1835; Railliet, 1899; Ransom, 1920; a coprophagous tidepool fish is the necessary inter­ Rausch, 1953; Rudolphi, 1802, 1819; Shchupakov, mediate host as seen with P. decorus (Dailey, 1970), 1936; Stiles, 1901; Stiles and Hassall, 1899; Stunkard then the leopard seals northern migration to warmer and Alvey, 1929; Taylor et al., 1961; van Cleave, areas during winter months may provide the answer. 1953; Wardle, McLeod and Stewart, 1947; Yamaguti, King (1964) states that Hydrurga lives on the outer 1939, 1958, 1961; Yurakhno, 1968. fringes of the ice pack and moves as far north as the beaches of southern Australia and New Zealand, where tidepool fish could be found, while Lobodon, MONACHINAE Leptonychotes and Ommatophoca tend to stay with The sub-family Monachinae is composed of two the ice. groups of seals: the monk seals (Monachus monachus Hermann, 1779; M. tropicalis Gray, 1850; M.schauins- Acanthocephala landi Matschie, 1905), all of temperate waters; and Seven species of Corynosoma (Table 90) are known, the Antarctic seals (Leptonychotes weddelli Lesson, of which only C. hamanni is found in more than one 1826; Lobodon carcinophagus Hombron and Jacqui- not, 1842; Hydrurga leptonyx Blainville, 1820; and host. Ommatophoca rossi Gray, 1844). Bibliography The cestodes are represented by 23 species, 17 of which are in the genus Diphyllobothrium (Table 91). Ariola, 1900; Baird, 1853; Baylis, 1916, 1920; Bever- There are no cestode species common to the monk ly-Burton, 1971; Campana-Rouget and Biocca, 1955; 348 M. D. Dailey

Chapin, 1925; Dailey, 1970; Delyamure, 1955; Dies- (Phocinae). The shares two species of trema­ ing, 1850; Golvan, 1959; Gower, 1939; Johnston, 1931, todes with members of the Phocinae, but Odhneriella 1937; Johnston and Mawson, 1941; Johnston and rossica is unique to it. Only one other species in this Best, 1942; Joyeux and Baer, 1936; King, 1964; K rab­ genus has been described, it was reported from the be, 1865, 1878; Leiper and Atkinson, 1915; Linstow, white whale Delphinapterus leucas Pallas, 1776 by 1892, 1905, 1907; Markowski, 1952; Mawson, 1953; Price (1932). Meggitt, 1924; Nickol and Holloway, 1968; Railliet and Henry, 1907, 1912; Rausch, 1969; Rennie, 1907; Acanthocephala Rennie and Reid, 1912; Rudolphi, 1802; Shipley, Only the genus Corynosoma occurs, being represented 1907; Yamaguti, 1961, 1963. by three species in Cystophorinae and four in Odobe­ nus. C. bullosum is common to Cystophora and both CYSTOPHORINAE species of Mirounga, while only the polyzonal C. sem­ The Cystophora cristata Erxleben, 1777, erme and C. stromosum are shared with Odobenus. northern elephant seal (Mirounga angustirostris) and southern elephant seal (M. leonina) make up the Cy­ Bibliography stophorinae, [but see King, (Relationships of the hood­ ed and elephant seals (genera Cystophora and M i­ Baylis, 1916, 1920; Berland, 1963; Caballero and rounga)). J. Zool., 148:385-98. Eds.]. The family Peregrina, 1938; Cameron et al., 1940; Creplin, 1825 ; Odobenidae contains only one species, the walrus, Delyamure, 1955; Delyamure and Skrjabin, 1965, Odohenus rosmarus Linnaeus, 1758. 1966; Delyamure and Treshcher, 1966; Forssell, 1904; Gedoelst, 1911; Hsü, 1935; King, 1964; Markowski, 1952; Monticelli, 1890; Odhner, 1905; Price, 1932; Cestoda Roth and Madsen, 1953: Schmidt and Dailey, 1971; The hooded seal is a North Atlantic species and Skrjabin, 1915; Stiles and Hassell, 1896; Stunkard and shares only the few universal helminths with the Alvey, 1929; Yurakhno, 1968; Zschokke, 1903. temperate and southern Mirounga. Four of the five cestodes reported for Cystophora (Anophryocephalus, In the preceding comparison of pinniped helminths, Diphyllobothrium latum, Dipogonoporus, Pyramico- several general observations can be made. The infor­ cephalus) are also found in the ringed seal Pusa mation tends to support the assumption that the center hispida. M . leonina has two species of cestodes, of of pinniped evolution was the northern hemisphere, which Baylisiella tecta is unique, and M . angustirostris specifically the North Pacific. The higher number of has nono. Odobenus has three species of Diphyllobo­ helminths from hosts in this area indicate a longer thrium, of which D. romeri is unique. association between northern seals than between their southern counterparts. Also, it appears that most of Nematoda the pinniped helminth parasites are worms supplied The superfamilies Ascaroidea, Filaroidea, Strongy- by a terrestrial animal reservoir. This is borne out by loidea and Trichuroidea are represented. The Diro­ the fact that only a few genera reported from pinni­ filaria sp. reported for Cystophora, and Trichinella peds are not also found in the endemic terrestrial an­ spiralis in Odobenus are evidently aberrant parasites imal populations. for these hosts. The heartworm Skriabinaria in Cysto­ The reasons for the number of helminth parasites phora also infects two North Atlantic seals Phoca in a given host is complex and depends on a variety vitulina and Pusa hispida. The vector of this parasite of coexisting factors (diversity of individuals, zoogeo- is unknown at this time, but mosquitoes are the chief graphical distribution, diversity of habitat, behavior intermediate hosts in other members of this family patterns, presence or absence of intermediate hosts, (). Delyamure (1955) discusses the biology etc.) that apply to both parasite and host. Inasmuch and ecology of filarids parasitic upon marine mammals. as nearly all of these factors have not been explored C. osculatum and T . decipiens are again the most sufficiently in either parasite or host, definitive answers common nematodes reported. The hookworm U. ha- to many questions will have to remain unanswered miltoni from the southern elephant seal is also found until such information becomes available. in the , no doubt as a result of their common distribution. INTRASPECIFIC VARIATION IN HELMINTHS INFECT­ ING SYMPATRIC SPECIES OF PINNIPED POPULATIONS T rematoda In the preceding tables it is apparent that several The trematodes of Cystophorinae (Table 91) have species of helminths occur in pinnipeds where popula­ been previously discussed under the northern seals tions are sympatric. A good example of this can be The distribution and intraspecific variation of helminth parasites in pinnipeds 349

BODY LENGTH IN MM Figure 225. Regression of esophageal length on body length of female worms. Abbreviations: A - experimental infection in Eumetopias jubatus; B & G - natural infection in E. jubatus; D & E - natural infection in £ alophus californianus; Pn — Parafilaroides nanus; Pp — Parafilaroides prolificus; Circles — mean of each sample.

seen in the lungworms found in the California sea lion captured at Ano Nuevo Island and experimentally (.Zalophus californianus) and (Euma- infected with P. decorus using techniques similar to topias jubatus). Four species of the genus Parafilar­ Dailey (1970). Adult lungworms recovered from this oides have been reported for these two sea lions by cross-infection 60 days post-infection were compared Dougherty and Herman (1947): Parafilaroides decorus morphologically with populations of lungworms ob­ in Z. californianus and P. prolificus, P. nanus and P. tained from two wild caught E. jubatus and Z. cal­ sp. in E. jubatus. The three species from the latter host ifornianus. Eleven quantitative parameters were meas­ were described from a single male Steller sea lion at ured for each sample. The means of the five samples the San Diego Zoo. At Ano Nuevo Island, Santa Cruz were compared by one way analysis of variance. Sign­ County, California the only common ground where ificant differences were found between samples of these two sea lions mingle in large numbers, Dailey and various esophageal and body measurements, but not Hill (1970) found 10 of 14 Z. californianus and four between samples of spicules or vagina vera measure­ of nine E. jubatus infected with lungworms. No P. ments. These differences were best accounted for as nanus or P. prolificus were found in that study. Com­ arising from a gradient of morphological variation prehensive literature reviews by Margolis (1954). De­ within one species. There did not seem to be any lyamure (1955), Dailey and Brownell (1972) and M ar­ meaningful separation of samples according to host golis and Dailey (1972) reveal that only once have lung­ species. The regression of esophageal length on body worms been recovered from the Steller sea lion north of length showed a significant correlation (P < 0-01 ) Ano Nuevo Island although extensive examinations (Fig. 225). This study supports including P. nanus, P. have been carried out and other helminths reported. prolificus and P. sp. as synonyms of P. decorus. This fact, together, with the morphological similarities Future studies of this type, conducted on other of the four species, suggests that P. decorus may infect closely related species of helminths in sympatric popu­ Steller sea Hons only in California, and that intra­ lations of pinnipeds, are needer. Such studies conducted specific morphological variation, due to host influence, on genera with numerous species, such as Diphyllobo­ may account for some or all of the lungworm species thrium and Corynosoma, would undoubtedly reveal originally reported from this host. similar examples of intraspecific variation due to host A study was carried out to determine this possibility influence. Davey (1971) has concluded an excellent by Hill (1971). An unweaned Steller sea lion pup was study on the Anisakis groups where he reduces the 350 M. D. Dailey existing number of recognized species to only three Ciurea, J. 1933. Les vers parasites de l’homme, de mammifères et des oiseaux provenant des poissons du Danube et de le Mer (A. simplex, A. typica, A. physeteris). In groups such Noire. Arch. Roumaines Pathol. Exp. Microbiol., 6:150-71. as the Ascaridata, where criteria for taxonomic separ­ Creplin, F. C. 1825. Observations de Entozois. Gryphiswaldiae. ation are tenuous at best, biological evidence seems Dailey, M. D. 1969. Stictodera ubelakeri a new species of heterophyd essential. trematode from the California sea lion {Zalophus californianus). South. Calif. Acad. Sei., Bull., 68:82-85. Dailey, M. D. & Hill, B. L. 1970. A survey of Metazoan parasites ACKNOWLEDGEMENTS infecting the California (Zalophus californianus) and Steller (Eumetopias jubatus) sea lion. South. Calif. Acad. Sei., Bull., I would like to express my appreciation to Mrs 69:126-32. Jackie Testa, Mrs Lorraine Sjoberg, Mrs Mikel Floth, Dailey, M. D. & Brownell, R. L. 1972. A checklist of marine and Mr Ralph Appy for their help in the preparation mammals parasites, pp. 528—89. In Mammals of the sea, of this paper. biology and medicine. Ed. by S. H. Ridgway. Charles C. Thomas, Springfield, 111. Davey, J. T. 1971. A revision of the genus Anisakis Kujardin, REFERENCES 1845 (Nematoda: Ascaridata). J. Helminthol., 45:51-72. Delamure, S. L., Kurochkin, Y. V. & Skryabin, A. S. 1964. Anderson, R. C. 1959. The taxonomy of Dipetalonema spirocauda [On the helminth fauna of the Caspian seal, Phoca caspica G.M .] (Leidy, 1858) n. comb. (= Skrjabinaria spirocauda) and Dirofilaria Astrakh. Zapovedn., Tr., 9:105-18. roemeri (Linstow 1905) n. comb. (= Dipetalonema roemeri). Can. Delamure, S. L. & Skrjabin, A. S. 1965. [On the method of J. Zool., 37:481-93. helminthological examination of marine mammals. (Special Ariola, V. 1900. Sopra alcuni dibotrii nuovi o poco noti e sulla features in the collection of helminthological material from classificazione del genera Bothriocephalus. Mus. Zool. Genova, pinnipeds and cetaceans).] In Morskie Mlekopitayushchie, Bull., 52:22. [2nd All-Union Conf. Study Mar. Mamin, Sept. 13, 1963, Baird, W. 1853. Descriptions of some new species of entozoa from Leningrad. Ed. by K. K. Chapskii]. Moscow, Akad. Nauk. the collection of the British Museum. Zool. Soc. Lond., Proc., S.S.S.R., Leningrad. Part 21, [1853]: 18-25. Delamure, S. L. & Skrjabin, A. S. 1966. [A new Diphyllobo- Ball, G. H. 1931. An Acanthocephalan Corynosoma strumosum ÛiT)iàe-Diphyllobothrium pterocephallum sp. nov. - a parasite of (Rudolphi), from the California . Univ. Calif., Cystophora cristata.] Helminthologia, 7:65-70. Publ. Zool., 33:301-05. Delamure, S. L. 1953. [Helminthofauna of marine mammals in Baylis, H. A. 1916. Some Ascarids in the British Museum (Natural the light of their ecology and phylogeny.] Akad. Nauk S.S.S.R., History). Parasitology, (London), 8:360-78, pis. 14-17. Moscow, Izv. Isr. Program Sei. Trnasl., 1968. Baylis, H. A. 1920. On the classification of the Ascaridae. I. The Delamure, S. L. & Alekseev, E. V. 1966. [Parafilaroides arcticus systematic value of certain characters of the alimentary canal. n. sp., a parasite of the ringed seal of the Chukotsk Seal] pp. Parasitology, Lond., 12:253-64. 11-15. In Parzity, Promezhutochnye Khoziaeva i Perenoschiki. Baylis, H. A. 1932. A list of worms parasitic in Cetacea. Disc. Nauka Dumka, Kiev. Rep., 6:393-418. Delamure, S. L. & Parukhin, A. M. 1968. [A new diphyllo- Baylis, H. A. 1932. A new species of the nematode genus Uncinaria bothriid parasitic in the South African fur seal] pp. 2.>—34. from a sea lion with some observations on related species. In [Parasites of marine mammals], Biol. Morya Akad. Nauk Parasitology, Lond., 24:308-16. Baylis, H. A. & Daubney, R. 1923. A further report on parasitic Ukr. S.S.R., 14. Delamure, S. L. & Treshchev, V. V. 1966. [On the helminth nematodes in the collection of the zoological survey of India. fauna of the hooded seal (Cystophora cristata Erxleben), inhabiting Ind. Mus. Calcutta, Rec., 25:551—78. the Greenland Sea.] Zool. Zh., 45:1867—71. Belopolskaia, M. M. 1960. [The helminthofauna of Phoca vitulina Diesing, K.M . 1850. Systema Helminthum I. W. Braunmuller, largha.] Vest. Leningrad. Univ., Ser. Biol., Vestn., 15:113-21. Berland, B. 1963. Phocascaris cystophorae sp. nov. (Nematoda) from Vindobonal. Dogiel, V. A. 1947. [The importance of parasitological data in the hooded seal, with an emendation of the genus. Univ. the solution of zoogeographical questions.] Zool. Zh., 26: Bergen. Arb., Naturvidensk. Rekke, 17:1-22. Beverly-Burton, M. 1971. Helminths from , Lepto­ 481-92. Dougherty, E. C. 1946. The genus Aelurostrongylus Cameron, 1927 nychotes weddelli (Lesson, 1826) in the Antarctic. Can. J. Zool., (Nematoda: Metastrongylidae) and its relatives: with de­ 49:75-83. scriptions of Parafilaroides gen nov. and Angiostrongylus gubernacu- Bose, L. A. Y. 1802. Historie naturelle des vers contenant leur latus sp. nov. Helminthol. Soc. Wash., D.C., Proc., 13.16—25. description et leurs moeurs. In Buffon, Historie Naturelle. Dougherty, E. C. & Herman, C. M. 1947. New species of the Vol. 2. Ed. by K. K . Costell. Paris. genus Parafilaroides Dougherty, 1946 (Nematoda: Metastrongy­ Bruyn, W. M. 1933. Beiträge zur Kenntnis von Strongylus circum- lidae), from sea lions, with a list of the lungworms of the litus Railliet aus den Lungen des Seehundes: die neue Gattung Pinnipedia. Helminthol. Soc. Wash., D.C., Proc., 14.77—87. Otostrongylus. Zool. Anz., 103:142—53. Duncan, A. 1956. Notes on the food and parasites of gray seals, Caballero, Y., Eduaordo, C. & Peregrina, D. I. 1938. Nematodo Halichoerus grypus (Fabricius), from the Isle of Man. Zool. de los mamiferos de Mexico. Univ. Nac. Mex., Inst. Biol., Soc. Lond., Proc., 126:635-44. An., 9:289-306. ^ Fabricius, O. F. 1780. Fauna Groenlandica, Systematice Sistens Cameron, T.W .M ., Parnell, I. W. & Lyster, L. L. 1940. The Animalia Groenlandicae Occidentalis Hactenus Indagata, etc. helminth parasites of sledge-dogs in northern Canada and Hafnia and Lipsiae. Newfoundland. Can. J. Res., 18:325—32. Faust, E. C. 1937. Mammalian heart worms of the genus Diro­ Campana-Rouget, Y. & Biocca, E. 1955. Une nouvelle espece filaria. Festsch. Bernhard Nocht, Geburtstag, Hamburg, 80: d’Anisakis chez un phoque Méditerranéen. Ann. Parasitai. 131-39. Hum. Comp., 30:477-80. Forssell, A. 1904. Echinorhynchus semermis n. sp. Fauna Fenn., Chapin, E. A. 1925. Descriptions of new internal parasites. U.Ü. Soc. Fauna Flora Fenn., 30:175—79. Natl. Mus., Proc., 6 8 , art. 2:1-4. The distribution and intraspecific variation of helminth parasites in pinnipeds 351

Fujita, T. 1921. On the parasites of Japanese fishes II. Dobuts Krotov, L. V. & Keliamure, S. L. 1952. [Data on the parasitic Zasshi, 33:1-8. worm fauna of mammals and birds of the USSR.] Gelmintol. Gedoelst, L. 1911. Synopsis de parasitologie de l’homme et des Lab., Akad. Nauk S.S.S.R., Tr., 6:278-92. animaux domestiques. Lierre & Bruxelles. Kurochkin, Y. V. 1958. [Helminth fauna of Caspian seals in the Germanos, N. K. 1895. Bothriocephalus schistochilos n. sp., ein neuer period of reproduction.] Rab. Gelmintol. 80-letiiu Akad. Cestode aus dem Darm von Phoca barbata. Jena. Z. Med. K. I. Skrjabin. Moscow: 188—94. Naturwiss., 30:1-38. Kurochkin, Y. V. & Zablotskii, V. I. 1958. [On the helminth Golvan, Y. J. 1959. Acanthocephales du genre Corynosoma Lühe, fauna of Caspian seals.] Tr. Astrakh. Zapoved., 4:337-43. 1904. Parasites de mammifères d’Alaska et de Midway. Ann. Leidy, J. 1858. Contributions to helminthology. Acad. Nat. Sei., Parasitol. Hum. Comp., 34:288-321. Phila., Proc., 10:110-12. Goto, S. & Ozaki, Y. 1930. Brief notes on new trematodes. Jap. Leiper, R. T. & Atkinson, E. L. 1914. Helminths of the British J. Zool., Trans. & Abstr., 3:73-82. Antarctic Expedition 1910-1913. Zool. Soc. Lond., Proc. Gower, W. C. 1939. Host-parasite catalogue of the helminths of [1914]: 222-26. ducks. Am. Midi. Nat., 22:580-628. Lent, H. & Freitas, J. F. T. 1948. Um a colecao de nematodeos, GuiartjJ. 1936. Cestodes parasites provenant des campagnes parasitos de vertebrados, do Museo de Historia Natural de scientifiques de S.A.S. le Prince Albert 1-er de Monaco ( 1886— Montevideo. Inst. Oswaldo Cruz., Mem., 46:1-71. 1913). In Albert 1-er, Prince Souvérain de Monaco, ed., Leukart, K. G. 1863. Die Menschlichen Parasiten und die von Résultas des campagnes scientifiques accomplies sur son ihnen herrührenden Krankheiten. Ein Hand- und Lehrbuch yacht par Albert 1-er, Prince Souvérain de Monaco. Im­ für Naturforscher und Aerzte. Vol. 1. Heidelberg, Leipzig. primerie, Monaco. Lincicome, D. R. 1942. Acanthocephala of the genus Corynosoma Heinze, K. 1934. Die parasitischen Würmer. Wiss. Erg. Deut. from the California sea lion. J. Parasitol., 29:102-06. Grönl. Exped. Alfred Wegener 1929, 1930-31, 6:185-89. Linnaeus, C. 1758. Systema naturae, regnum animale. 10th ed. Herman, C. M. 1942. The effect of Higueronia on nematodes and Lipsiae. nemathelmintic gastric ulcers of California sea lions. Rev. Linstow, O. von. 1892. Helminthen von Süd-Georgien, nach der Med-Trop. Parasitol., Bacteriol., Clin. Lab., 8:45-47. Ausbeute der deutschen Station von 1882-1883. Jahrb. Wiss. Hill, B. L. 1971. Comparative morphology of Parafilaroides decorus Aust. Hamburg, 9:59-77. (Nematoda: Metastrongyloidea) in the California and Steller Linstow, O. von. 1905. Helminthen aus Ceylon und aus ark­ sea lions. Unpublished masters thesis, Calif. State Univ., tischen Breiten. Z. Wiss. Zool., 82:182-93. Long Beach. Linstow, O. von. 1907. Nematoden aus dem Königlichen Zoo­ Höst, P. 1932. Phocascaris phocae, n. g., n. sp., eine neue logischen Museum zu Berlin. Mitt. Zool. Mus., 3:251-59. Ascaridenart aus Phoca groenlandica Fabr. Zentralbl. Bakteriol. Lühe, M. 1910. Cestoden. Heft. 18. In Die Süsswasserfauna Parasitenkd. Infektionskr., 125:335-40. Deutschlands. By A. Brauer. Hsü, H. F. 1935. Contributions à l’Etude de Cestodes de Chine. Lühe, M. 1911. Acanthocephalen. Heft. 16. In Die Süsswasser­ Rév. Suisse Zool., 42:447-570. fauna Deutschlands. Ed. by A. Brauer. Johnson, M. L., Fiscus, C. H., Ostenson, B. T. & Barbour, M. L. Lyster, L. L. 1940. Parasites of some Canadian sea mammals. 1966. Marine mammals. Vol. 33:877-924. In Environment of Can. J. Res., Sect. C, Bot. Sei., 18:395-409. the Cape Thompson region, Alaska. Ed. by N. J. Wilimovsky. Margolis, L. 1954. List of the parasites recorded from sea mammals U.S. At. Energy Comm., Washington. caught off the West Coast of North America. J. Fish. Res. Bd Johnston, T. H. 1931. New trematodes from the subantarctic and Can., 11:267-83. Antarctic. Aust. J. Exp. Biol. Med. Sei., 8:91-98. Margolis, L. 1956. Parasitic helminths and from Johnston, T. H. 1936. Entozoa from the Australian hair seal. Pinnipedia of the Canadian Pacific Coast. J. Fish. Res. Bd Linn. Soc. N.S.W., Proc., 61:9-16. Can., 13:489-505. Johnston, T. H. & Best, E. W. 1937. Acanthocephala. Aust.Natl. Margolis, L. & Dailey, M. D. 1972. Revised annotated list of Antarct. Res. Exped. (A.N.A.R.E.), 1911-1914, Sei. Rep., parasites from sea mammals caught off the west coast of North Ser. C, Zool. Bot., 10:1-20. America. U.S. Natl. Oceanic. Atmos. Admin. Tech. Rep., Johnston, T. H. & Best, E. W. 1942. Australian Acanthocephala. Natl. Mar. Fish. Serv., Spec. Rep. Fish., 647. 3. R. Soc. South. Aust., Trans, and Proc., 65:250-54. Markowski, S. 1952. The cestodes of pinnipeds in the Arctic and Johnston, T. H. & Mawson, P.M. 1941. Nematodes from other regions. J. Helminthol., 26:171-214. Australian marine mammals. South. Aust. Mus., Rec.. 6 : Mawson, P. M. 1953. Parasitic nematoda collected by the 429-34. Australian National Antarctic Research Expedition: Heard Joyeux, C. & Baer, J. C. 1936. Fauna de France. 30. Cestodes. Island and Macquarie Island, 1948-1951. Parasitology, Lond. Paris. 43:291-97. Kenyon, K. W. 1962. Notes on phocid seals at Little Diomede Meggitt, F. J. 1924. The cestodes of mammals. H. Pohle, London. Island, Alaska. J. Wildl. Manage., 26:380-87. Monticelli, F. S. 1890. Note elminthologiche. Soc. Nat. Napoli Keyes, M. C. 1965. Pathology of the . Am. Vet. Bull., 4:189-208. Med. Assoc., J., 147:1090-95. Montreuil, P. L. J. 1958. Corynosoma magdaleni sp. nov. (Acantho­ King, J. E. 1964. Seals of the world. British Museum (Natural cephala) : A parasite of the in eastern Canada. Can. History). J. Zool., 36:205-15. Krabbe, H. 1865. Helminthologiske Undersøgelser i Danmark og Mozgovoi, A. A. & Ryzhikov, K. M. 1950. [The problem of the paa Island, med særligt Hensyn til Blæreormlidelserne paa origin of the Baikal seal in the light of helminthological science.] Island. Dansk. Vidensk. Selsk. Skr., naturvid.-math afd., Akad. Nauk S.S.S.R., Leningrad, Dokl., 72:997-99. 7:347-408. 1865. Muller, O. F. 1776. Zoologiae Danicae prodomus seu animalium Krabbe H. 1878. Sælernes og Tandhvalernes Spolorme. Overs. Daniae et Norvegiae indigenarum characteres. Nomina et Over K. Dan. Vidensk. Selsk. Forh., 1:43-51. Synonyma imprimis popularum. Kreis, H. A. 1938. Beiträge zur Kenntnis parasitischer Nema­ Neiland, K. A. 1961. Suspected role of parasites in non-rookery toden. 6 . Parasitische Nematoden aus dem Zoologischen Garten mortality of fur seals (Callorhinus ursinus). J. Parasitol., 47:732. in Basel. Zentralbl. Bakteriol. Parasitenkd. Infektionskr., Abt., Neiland, K. A. 1962. Alaskan species of acanthocephalan genus 2, 141:279-304. Corynosoma Luehe, 1904. J. Parasitol., 48:69-75. 352 M. D. Dailey

Nickol, B. B. & Holloway, H. L. 1968. Morphology of the presoma Shchupakov, I. G. 1936. [Parasitic fauna of the Caspian seal.] of Corynosoma hamanni (Acanthocephala: Polymorphicae). J. Uch. Zap. Leningrad. Ord. Lenina Gos. Univ. Im. A. S. Morphol., 124:217-26. Bubnova, 7, Ser. Biol., 3:134-43. Nicoll, W. A. 1923. A reference list of the trematode parasites Shipley, A. E. 1907. Cestodes (National Antarctic Expedition of British mammals. Parasitology, 15:236-52. 1901-1904). Nat. Hist., 3, Zool. Bot. Nybelin, O. 1931. Saügetier und Vogelcestoden von Juan Fer­ Skrjabin, A. S. 1959. [New species of helminths from marine nandez. pp. 493-523. In The natural history ofjuan Fernandez mammals of the Pacific Ocean and far eastern seas.] Krym. and Easter Island. 3. Zoology. Ed. by C. Skottberg. Almquist Pedagog. Inst., Izv., 34:99—118. and Wiksells, Uppsala. Skrjabin, A. S. 1965. [Larval forms of helminths from marine Odhner, T. 1906. Die Trematoden des Arktischen Gebietes. mammals of far eastern seas.] pp. 39-40. In Morskie Mlekopi- Fauna Arct., f :291—372. tayushchie, [2nd All-Union Conf. Study Mar. M amm, Sept. 13, Owen, A. 1835. Description of a microscopic entozoon infesting 1963, Leningrad. Ed. by K. K. Chapskii]. Akad. Nauk S.S.S.R., the muscles of the human body. Zool. Soc. Lond., Trans., Moscow, Leningrad. 1:315-24. Skrjabin, K. I. 1915. [Odhneriella rossica n. g., n. sp., an agent of Perry, M. L. 1967. A new species of Dipetalonema from the Cali­ worm liver diseases in .] Arkh. Vet. Nauk., 45:1057-64. fornia sea lion and a report of Microfilariae from a Steller sea Stiles, C. W. 1901. Uncinariasis (anchylostomiasis) in man and lion (Nematoda: Filaroidea). J. Parasitol., 53:1076-81. animals in the United States. Texas Med. News, 10:523-32. Price, E. W. 1932. The trematode parasites of marine mammals. Stiles, C. W. & Hassall, A. 1896. Notes on parasites. Vet. Mag., U.S. Natl. Mus., Proc., 81 Artie. 13:1-68. 3:151-69. Railliet, A. 1899. Sur quelques parasites rencontrés à l’autopsie Stiles, C. W. & Hassall, A. 1899. Internal parasites of the fur seal, d’une Phoque (Phoca vitulina L.) Soc. Biol., C. R. Hebd. pp. 99-177. In The fur seal and fur seal islands of the North Séances et M ém ., Ser. 11, 1:128-30. Pacific Ocean. Part 3. Ed. by D. S. Jordan. U.S. Treas. Dep., Railliet, A. & Henry, A. 1912. Helminthes recueillis par l’éx- Doc. 2017, Gov. Print. Off., Wash., D.C. pedition Antarctique Française du Pourquoi-Pas? II. Cestodes Stiles, C. W. & Hassall, A. 1912. Index catalogue of medical and des phoques. Mus. Natl. Hist. Nat., Bull., 18:153-59. veterinary zoology subjects: Cestoda and Cestodaria. U.S. Ransom, B. H. 1920. Synopsis of the trematode family Hetero- Publ. Health and Mar. Hosp. Sev. Hyg. Lab., Bull., 85:467. phyidae with descriptions of a new genus and five new species. Stunkard, H. W. 1948. Pseudophyllidian cestodes from Alaskan U.S. Natl. Mus., Proc., 57:527-73. pinnipedia. J. Parasitol., 34:211-28. Rausch, R. L. 1953. Studies on the helminth fauna of Alaska. Stunkard, H. W. & Lavey, C. H. 1929. A new liver fluke, Z “^pho- X III. Disease in the sea otter, with special reference to helminth trema hepaticum, from the California sea lion, Za^°P^us califor­ parasites. Ecology, 34:584-604. nianus. J. Parasitol., 16:106-07. Rausch, R. L. 1969. Diphyllobothriid cestodes from the Hawaiian Taylor, A. E. R., Brown, D. H., Heyneman, D., & McIntyre, , Monachus schauinslandi Matschie, from Midway Atoll. R. W . 1961. Biology of filaroid nematode Dipetalonema spiracauda J. Fish. Res. Bd Can., 26:947-56. (Leidy, 1858) from the heart of captive harbor seals and sea Rennie, J. 1907. “Scotia” collections. On Echinorhynchus antarcticus lions, together with pathology ofhosts. J. Parasitol., 47:971—76. n. sp. and its allies. R. Soc. Edin., Proc., 26:437-46. Van Cleave, H. J. 1953. Acanthocephala of North American Rennie, J. & Reid, A. 1912. The Cestoda of the Scottish Antarctic mammals. 111. Biol. Monogr., 23:1—179. Expedition (Scotia). R. Soc. Edinb., Trans., 48:441—54. Wardle, R. A., McLeod, J. A. & Stewart, I. E. 1947. Lühe’s Rice, D. W. & Scheffer, V. B. 1968. A list of the marine mammals “Dipyllobothrium” (Cestoda). J. Parasitol., 33:319-30. of the world. U.S. Fish Wildl. Serv., Spec. Sei. Rep., Fish. Yamaguti, S. 1939. Studies of the helminth fauna of Japan. Ser., 579. 16 pp. Part 29. Acanthocephala II. Jap. J. Zool., 8:317-51. Roth, H. & Madsen, H. 1953. Die Trichinose in Grønland, Yamaguti, S. 1958. Systema Helminthum. Vol. 1. Part 1. Digenc- absch iessender Bericht der Jahre 1948—1953. pp. 340—341. In tic trematodes. Interscience. Proc.. 14th Int. Cong. Zool., Sect. 10. Parasitol. Yamaguti, S. 1961. Systema Helminthum. Vol. III. Part I.N em a­ Rudolphi, C. A. 1802. Fortsetzung der Beobachtungen über die todes. Interscience. Eingeweidewürmer. Arch. Zool. Zoot., 2:1—67. Yamaguti, S. 1963. Systema Helminthum. Vol. V. Acantho­ Rudolphi, C. A. 1819. Entozoorum synopsis cui accedunt man­ cephala. Interscience. tissa duplex et indices locupletissimi. Berolini. Yurakhno, M. V. 1968. [Microphallus orientalis n. sp. (Trema­ Schmidt, G. D. & Dailey, M. D. 1971. A Zoogeographie note on toda: Microphallidae), a parasite of the Pacific walrus and the Acanthocephalian Corynosoma bullosum (Linstow 1892). Am. bearded seal.] Zool. Zh., 77:630-31. Microsc. Soc., Trans., 90:94-95. Zschokke, F. 1903. Die Arktischen cestoden. Fauna Arct., 3:1-32.