7

PREFA CE

The first International Symposium on the Biology of the Seal was held at the University of Guelph, O n ­tario, C anada from 13 to 17 August 1972. The sym­posium developed from discussions originating in D ub­lin in 1969 at the meeting of the M arine Mammals Committee of the International Council for the Ex­ploration of the Sea (IC E S). T he culmination of three years’ organization resulted in the first interna­tional meeting, and this volume. The president of ICES Professor W. Cieglewicz, offered admirable support as well as honouring the participants by attending the symposium.

T he programme committee was composed of experts representing the m ajor international sponsors. W. N. Bonner, Head, Seals Research Division, Institute for M arine Environmental Research (IM E R ), represented IC ES; A. W. Mansfield, Director, Arctic Biological Station, Fisheries Research Board of C anada (FRB) represented the International Commission for N orth ­west Atlantic Fisheries (IC N A F ); and K. S. Norris, Director, M arine M am m al Council Executive Com­mittee, represented the International Biological Pro­gram (IBP). The Food and Agriculture Organization of the U nited Nations (FAO) also offered its support to the programme and ICNAF has contributed to the financing of this volume.

Sponsors of national origin were the Fisheries R e­search Board of C anada (FR B ), the National R e­search Council of C anada (N R C C ), the Canadian National Sportsmen’s Show (CNSS), the W orld W ild­life Fund (Canada) (W W F), and the University of Guelph.

In his preliminary remarks Professor Ronald intro­duced the representatives of these groups; namely J. R. Weir, Chairman, Fisheries Research Board of Canada; S. Bata, International Director and J. S. McCormack, Director, W orld Wildlife Fund (C anada); and R. T.D. Birchall, President, Canadian National Sportsmen’s Show and a D irector of W W F (C anada).

W. C. W inegard, President of the University of Guelph, welcomed participants to the symposium and commented particularly on how pleased he was to welcome representatives from so many countries. Later, at a banquet sponsored by the D epartm ent of the En­vironment, Canada, he offered an invitation to the group to return in 1975 for a Second International Seal Symposium.

Altogether 62 papers were presented. A further 14

papers were read by title and are included either in full or abstract form in this volume. T he 139 particip­ants represented 16 countries, permitting scientific interchange of a truly international nature.

In his opening address, V. B. Scheffer suggested that a dream was becoming a reality with a meeting of such a large group of pinniped biologists. This he felt was very relevant at a time when the relationship of marine mammals and m an was being closely examined on biological, political and ethical grounds.

T he scientific session commenced with a seven paper section on evolution chaired by E. D. Mitchell which showed the origins and subsequent development of this amphibious group of higher vertebrates. M any of the arguments for particular evolutionary trends are speculative in nature and different interpretations can be attached to the same fossil material. Readers of this volume should be aware of such differences when read­ing the papers in this section. T he twelve papers of S. H. Ridgway’s section on functional anatomy illus­trated the fundam ental structure of the seal, as well as its associated control mechanisms. R. J. Schusterman followed this theme by introducing ten papers on be­haviour. H e established a m ajor focus on social or­ganization and communication and their association with the functional anatomy of the pinnipeds. D. E. Sergeant chaired the population dynamics section of seven papers, covering the modelling of populations and method of analysis of seal populations around the world. In the fifth section, J. R. Geraci, by means of papers and a panel discussion dealt with the care and m anagement of captive pinnipeds. W. N. Bonner co­ordinated a presentation in the broad area of ecology, and was able to bring together studies on environmen­tal factors and their associated behavioural and gene­tic control systems. T he physiology section was chaired by H. T. Andersen, his introductory remarks forming the initial paper of the section. T he other six papers of his section emphasized the underwater responses of seals. T he final and general section, chaired by J. E. King, offered a broad coverage of several of the more interesting areas in various disciplines.

A. W. Mansfield acted as rapporteur for the entire programme, and his report stressed the need for con­tinued cooperation by all biologists so tha t they might understand seals and their importance to environmen­tal studies.

This volume includes with one exception, those pa-

8 K . Ronald

pers either presented, read by title, or abstracted, but the continuing discussion on the biology of the seals led to one further paper tha t is included here. Some of the discussion was formal and, where recordable, is included here, but by far the greater part of discussion was informal and hence must remain as extremely valuable, but merely mental recollections of the par­ticipants in the symposium.

T he symposium achieved its purpose of bringing together scientists interested in the Pinnipedia and it offered leads into the international examination of marine mammals.

The editors w ith little apology recognized tha t they have not reached a completely uniform format in this volume since they have allowed use of both English and metric systems of measurement and both English and N orth American word usage for the sake of har­mony. The main editorial structure has been the con­sistency of usage throughout a particular paper.

Attempts have also been made to attain a fairly uniform taxonomy for the species, but where there has been any doubt caution has not overridden clarity. As in other m am m alian groups, the systematics of the Pinnipedia are still open to much interpretation. The references are cited according to an Annotated Biblio- praphy on the Pinnipedia*. T he ‘List of the marine

* R onald, K ., L. M . H anly and P. J . H ealey, College o f Bio­logical Science, U niversity o f Guelph, Ontario, Canada.

T he following have kindly acted as Discussion Leaders of the different Sections and also assisted in the editing of the contributions:

Evolution Section

E. D. M itchellArctic Biological Station, Fisheries Research Board of C anada, Ste. A nne de Bellevue, Quebec, Canada.

Functional Anatomy Section

S. H . RidgwaySchool of A natom y, University of Cam bridge, Cam bridge, England.

Behaviour Section

R. J . Schusterm anD epartm ent of Psychology, California State University H ayw ard, California 94542, U.S.A.

Population Dynamics Section

D. E. SergeantA rctic Biological Station, Fisheries Research Board of C anada, Ste. Anne de Bellevue, Q uebec, Canada.

mammals of the world’ by D. W. Rice and V. B. Scheffer (U.S. Fish and Wildlife Service, W ashing­ton, 1968) has been used as the standard reference on nomenclature.

The work of the chairmen of each of the seven sec­tions of this volume is especially recognized. As well, the convenor wishes to thank the programme com­mittee for their ability to support a somewhat unortho­dox procedural system, and particularly the sponsors ICES, ICNAF, IBP, CNSS, FRB, NRCC, W W F (C a­nada), FAO, and the University of Guelph for their valuable financial assistance.

T he convenor is most grateful to M r. H. Tambs- Lyche, General Secretary of ICES, for his advice and encouragement from the embryonic stages of the sym­posium to the publication of the proceedings; he also recognizes the considerable am ount of expert help pro­vided by A. W. Mansfield in co-editing this volume.

Finally, the effort put into both the symposium and this volume by Mrs. Ginny Bandesen has been beyond measure, but I hope tha t she will accept the results of the symposium recorded here as tangible proof of her most valuable contribution. To the members of the D ean of the College of Biological Science’s office, the university support staff and our host Dr. W. C. Wine- gard, I express on behalf of the participants and my­self, our sincerest thanks.

K. Ronald, Convenor

Care and Management Section

J . R. GeraciD epartm ent of Zoology, University of Guelph, Guelph, O ntario, Canada.

Ecology Section

W. N. BonnerSeals Research Division IM E R , c/o Fisheries L abora ­tories, Lowestoft, Suffolk, England.

Physiology Section

H. T . AndersenN utrition Institute, University of Oslo, Blindern, Oslo, Norway.

General Session

J . E. K ingD epartm ent of Zoology, University of New South Wales, Kensington, N.S.W ., Australia.

Summary

A. W. M ansfield (R apporteur)Arctic Biological Station, Fisheries Research Board of C anada, Ste. Anne de Bellevue, Quebec, C anada.

338

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

T H E D IS T R IB U T IO N AND IN T R A S P E C IF IC V A R IA T IO N O F H E L M IN T H

PA RA SITES IN PIN N IPED S

M. D . D a i l e y

Department o f Biology, California State University, Long Beach, California, U .S .A .

IN T R O D U C T IO N

Annotated lists of pinniped parasites have been pub­lished since the time of Linnaeus in 1758. They have usually been restricted to parasites of various pinniped groups or specific geographical locations. The present paper presents a comparative approach, emphasizing the occurrence of helminths in sympatric pinniped populations and their intraspecific variation.

The monograph of Delyamure (1955) was used as a basis for tabulating helminths from five subfamilies of pinnipeds (Arctocephalinae, Cystophorinae, O tarii­nae, Monachinae, Phocinae) and one family (Odo- benidae). The classification used by Rice and Scheffer (1968) and King (1964) was adopted throughout this work.

O T A R IID A E

T he otariids are separated into two subfamilies, the sea lions O tariinae and the fur seals Arctocephalinae.

Distribution of otariids is limited to the subantarctic in the New Zealand and Australia area (Hookers sea lion, JPhocarctos hookeri Gray, 1844; Australian sea lion, Neophoca cinerea Peron, 1816), to South Ame­rica (South American sea lion Otaria flavescens Shaw, 1800) and to the west coast of N orth America, the Aleutian Islands and the Sea of Okhotsk (California sea lion, Zalophus californianus Lesson, 1828; Steller or northern sea lion, Eumetopias jubatus Schreber, 1776).

OTARIINAE

The helminths reported from O tariinae are present­ed in Tables 83 and 84. In Delyamure (1955), the table for this subfamily listed nine helm inth species belonging to seven genera for E. jubatus, seven species from six genera for Z. calif ornianus, three species from three genera for O. flavescens and no reports for either Neophoca cinerea or Phocarctos hookeri.

Table 83. Comparison of helm inth parasites in O tariinae (Cestoda and Acanthocephala)

Otariinae

Species o f H elm inth Eumetopias Zalophus Otaria Neophoca Phocarctosjubatus 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............................Corynosoma austra le ........................C. hamanni.....................................C. obtuscens....................................C. osmeri.........................................C. semerme....................................C. strumosum..................................C. villosum ..................................

++

+I+

T he distribution and intraspecific variation o f helm inth parasites in pinnipeds 339

Table 84. Comparison of helm inth parasites in O tariinae (Trem atoda and N em atoda)

Otariinae

Species o f H elm inth Eumetopias £ alophus Otaria Neophoca Phocarctosjubatus californianus flavescens cinera hookeri

Trem atoda

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

S. haematobium .................................................. -t-

Nem atoda

Anisakis patagonica............................................. + _j_A. s im ilis .............................................................. + -Î- 4 -A. simplex.............................................................. +A. tridentata ..................................................... -fContracaecum 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 belong­ing to 11 genera: (Cestoda) Adenocephalus, Anophry- ocephalus, Diphyllobothrium. Diplogonoporus; (Ne­matoda) Anisakis, Contracaecum, Parafilaroides, Ter­ranova, Uncinaria; (Acanthocephala) Bolbosoma, Co- rynosoma. Trematodes have never been reported from this host.

In Z. californianus there are now 17 species be­longing to 15 genera: (Cestoda) Diphyllobothrium: (Nematoda) Anisakis, Contracaecum, Dirofilaria,Dipe­talonema, Parafilaroides, Termnova, Uncinaria; (Ac­anthocephala) Corynosoma; (Trematoda) Pricetrema, Stictodora, Stephanoprora, Zalophotrema, Hetero­phyes, Schitosoma.

Helminths reported from O. flavescens now include 12 species from seven genera: (Cestoda) Diphyllobo­thrium, Phyllobothrium (larval stage); (Nematoda) Anisakis, Contracaecum, Terranova, Uncinaria; (Ac­anthocephala) Corynosoma; no trematodes have been found. Finally N . cinera has three species from three genera: (Cestoda) Diphyllobothrium; (Nematoda) Con­tracaecum; (Acanthocepala) Corynosoma while P. hookeri has only one helminth, the nematode, Terra­nova decipiens.

Cestoda

Some interesting observations can be made from these comparisons. A common species Diphyllobothri­um pacificum is shared by Eumetopias and Zalophus, while other members of the same genus D. arctocepha- linum and D. scoticum are shared by Neophoca and Otaria respectively. The occurrence of D. pacificum is most likely explained by the overlapping distribution of the Steller and California sea lions, which share common hauling-out areas, such as Ano Nuevo Island. This probably explains the occurrence of the same para ­site in the northern fur seal Callorhinus ursinus (Lin­naeus, 1758) (Table 85) since all three species come to­gether on San Miguel Island off the California coast. The South American or Falkland fur seal, Arctocephalus australis (Zimmerman, 1783) is also reported to have D. pacificum (Table 85) which may have been derived from Zalophus at the Galapagos Islands. Neophoca shares its species of Diphyllobothrium (D. arctocephali- num )with three species of fur seals, the Australian fur seal, Arctocephalus doriferus Wood Jones, 1925; the South African fur seal, A. pusillus Schreber, 1776 and the Tasmanian fur seal, A. tasmanicus Scott and Lord, 1926 (Table 85). This parasite thus appears to

22'

340 M . D. D ailey

T able 85. Comparison of helm inth parasites in Arctocephalinae (Cestoda and Acanthocephala)

Arctocephalinae

Species o f H elm inth Arctocephalus A. A . A. A. A Callorhinusaustralis 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 stra le ...........................................C. osculatum ......................................................... +C. semerme........................................................ +C.'strumosum..........................................................C. ventronudum.................................................C. villosum ........................................................

be endemic in fur seals of the Southern hemisphere. Neophoca shares its breeding grounds with A. dori­ferus.

Nematoda

In the Otariinae, the nematodes are represented by the universal genera Anisakis, Contracaecum and Ter­ranova, one of which occurs in every species of pinni­ped except three, the ribbon seal, Histriophoca fasciata (Zimmerman, 1783), the New Zealand fur seal, Arcto­cephalus forsteri (Lesson, 1928) and the Guadalupe fur seal, A. philippii (Peters, 1866) in which no para ­sites are reported. The wide distribution of these ascarids is probably due to the lack of host specificity in their intermediate (crustacean and teleost) and definitive hosts. O ther genera of nematodes shared by Eumetopia and Zalophus also appear to be a product of mixing populations. The lungworms in the genus Parafilaroides are reported from both hosts, but pri­marily only from those Steller sea lions examined along the California coast. These lungworms and their host relationship will be discussed later under interspecific variation.

Hookworms of the genus Uncinaria present an inter­esting situation. Parasites of this genus are also found in terrestrial carnivores, primarily canids, where the sexually m ature worms occur in the adult animal. In

pinnipeds, hookworms have been reported from only four species, three sea lions (Otaria, Zalophus and Eumetopias) and one fur seal (Callorhinus), all of which inhabit overlapping geographical areas from the Falkland Islands, up the west coast of the Americas to the Bering Sea. T he adult worms in these animals occur only in the pups, an apparent adaption to the aquatic environment. Uncinaria sp. in Zalophus ap­pears to be an intermediate between U. lucasi of Cal­lorhinus and U. hamiltoni of Otaria (for further dis­cussion see Dailey and Hill (1970) and Margolis and Dailey (1972). O ther examples of parasite interchange between terrestrial animals and pinnipeds are more frequently seen now that increased numbers of pinni­peds are kept in captivity, particulary Zalophus. Di- petalonema immitis was reported from a zoo animal in New Orleans, Louisiana, an endemic area for that parasite in dogs. Heartworm has not been recorded from any wild otariids to da te ; however the tissue filarid Dipetalonema odendhali occurs in a high per­centage of examined Zalophus (personal observation).

T rematoda

A strange situation is presented by this group of parasities since only Zalophus is infected. Delyamure (1955) pointed out tha t up until the time of his writing all trematodes were recovered from sea lions living

T he distribution and intraspecific variation o f helm inth parasites in pinnipeds 341

Table 86. Comparison of helm inth parasites in Arctocephalinae (T rem atoda and Nematoda)

Arctocephalinae

Species of Helm inth Arctocephalus A. A. A. A. A. Callorhinusaustralis forsteri doriferus pusillus tasmanicus tropicalis ursinus

Trem atoda

Cryptocoty le jejuna. . . . Phocitrema fusiforme. . Pricetrema zaloph i.. . . Zolophotrema hepaticum

N em atoda

Anisakis pacificus................................................ o_A. s im ilis .............................................................. +

A - SP....................................................................... +Contracaecum callotariae .................................... _l_C. cor dero i......................................................... +C. osculatum ..................................................... + -j- _j_ _j_ _lC. rectangulum ................................................ -f-Dipetalonema spirocauda.................................... _1_Phocanema decipiens........................................... _l_Porrocaecum callotariae...................................... _j_P. sulcatum........................................................... -fTerranova decipiens............................................. + + _j_Uncinaria lucasi.................................................. +

in the Washington Zoo and none had been taken under natural conditions. This is no longer the situ­ation. The author has found P. zalophi, Z. hepaticum and S. ubelakeri in non-captive animals. Only two species, P. zalophi and Z. hepaticum appear to be endemic parasites of pinnipeds, where Stictodora and Stephanoprora are commonly found in birds. The Heterophyes and Schistosoma infections were both reported from zoo animals and are obviously a product of urban captivity.

Acanthocephala

These are well represented in the Otariinae, with all but P. hookeri having a t least one species. A total of eight acanthocephalan species are represented in two genera, all but one B. bobrovi belonging to the genus Corynosoma. Only two species of the genus Bol- bosoma, commonly a cetacean parasite, have been reported from pinnipeds, B. bobrovi and B. nipponicum. These worms appear to be endemic to the Bering sea area occurring in three widely distributed pinniped hosts, E. jubatus, C. ursinus and the ringed seal, Pus a hispida Schreber, 1775. In the genus Corynosoma, Otaria and Neophoca share the species C. australe, and Eumetopias and Zalophus share C. strumosum.

Bibliography

Baylis, 1916, 1920, 1933; Bose, 1805; Ciurea, 1933; Dailey, 1969; Dailey and Brownell, 1972; Dailey and

Hill, 1970; Delyamure, 1955; Dougherty and Herman, 1947; Faust, 1937; Forssell, 1904; Fujita, 1921; H er­man, 1942; Johnston, 1937; Johnston and Best, 1937; King, 1964; Krabbe, 1878; Kreis, 1938; Krotov and Delyamure, 1952; Lincicome, 1943; Linstow, 1880, 1907; Margolis, 1956; Margolis and Dailey, 1972; Markowski, 1952; Monticelli, 1890; Nybelin. 1931; Perry, 1967; Price, 1932; Raillet and Henry, 1912; Rennie and Reid, 1912; Rudolphi, 1802; Skrjabin, 1959, 1965; Stunkard, 1948; Stunkard and Alvey, 1929; van Cleave, 1953.

ARCTOCEPHALINAE

The fur seals offer an unusual comparison since only Callorhinus ursinus is a northern animal, while all seven species of Arctocephalus have a southern distribution. Unfortunately detailed comparison is re­stricted by the lack of work done on certain species: no reports on A. philipii or A. forsteri,1 and only a few reports on the South African species A. pusillus; the Australian fur seal, A. doriferus; the Tasmanian fur seal, A. tasmanicus; and the Kerguelen fur seal, A. tropicalis Gray, 1872. A moderate amount of study has been conducted on A. australis and C. ursinus has been well studied.

1 Johnston (1937) reports parasites'from “ the Australian hair seal” which he calls A. forsteri. K ing (1964) lists these under the Australian fur seal, A. doriferus.

342 M . D . D ailey

Cestoda

Diphyllobothrium pacificum is shared by A. australis and C. ursinus while D. arctocephalinum has been found in A. doriferus, A. pusillus and A. tasmanicus. These worms were also reported from members of the O tariinae and are discussed under that group. The larval stage of Phyllobothrium delphini, commonly a cetacean parasite in this stage and of elasmobranch fishes as adults, has been reported from three arcto- cephalines. This parasite has also been reported from Otaria and two species of M onachinae (Table 91); thus it appears to be an incidental parasite of pinnipeds in the southern hemisphere. T he ne­matodes shared by Callorhinus and Arctocephalus are the ubiquitous C. osculatum and T. decipiens. The only non-ascarid species reported for this group are the filarid Dipetalonema spirocauda and the hook­worm Uncinaria lucasi, both from C. ursinus. W hether representatives of these nematode groups are present in Arctocephalus and just have not been found, or w hether the host environment is unsuitable for sustain­ing the parasite is unknown. T he possibility of A. au­stralis contacting these parasites seems high owing to its zoogeographic association with Otaria and Zalo­phus in the Galapagos Islands.

Trem atoda

There are no common genera in the arctocephalines. Callorhinus has three species tha t are shared with Zalophus and members of the Phocinae (Table 92) and are probably endemic in the northern hemisphere. Zalophotrema hepaticum, also a common parasite in Zalophus, is shared by A. australis bu t absent from Callorhinus. This could indicate that the parasite is endemic to the southern range of Zalophus, extending to the Galapagos Islands area where large numbers of Zalophus and A. australis mingle.

Acanthocephala

Only a limited am ount of comparative information is available. Two species of the previously mentioned genus Bolbosoma are found only in Callorhinus. Two species of the genus Corynosoma are shared by Arcto­cephalus and Callorhinus, while one species is shared by two arctocephalines. Owing to the wide distribution of these acanthocephalans in all groups of pinnipeds, it is difficult to draw any conclusions from these infections.

Bibliography

Anderson, 1959; Baird, 1853, Baylis, 1916, 1920; Baylis and Daubney, 1923; Bcsc, 1802; Cholodkovsky,

1915; Delyamure, 1955; Delyamure and Parukhin, 1968 ; Forssell, 1904; Goto and Ozaki, 1930; Johnston, 1937; Johnston and Best, 1937; Keyes, 1965; King 1964; Krabbe, 1878; Krotov and Delyamure, 1952; Leidy, 1858; Lent and Freitas, 1948; Linstow, 1907; Lühe, 1911; Markowski, 1952; Neiland, 1961; Nicoll, 1923; Nybelin, 1931; Price, 1932; Rudolphi, 1802, 1819; Skrijabin, 1959; Stiles and Hassall, 1912; Stun­kard, 1948; Stunkard and Alvey, 1929; van Cleave, 1953; Yamaguti, 1939.

P H O C ID A E A N D O D O B E N ID A E

PHOCINAE

The northern seals belonging to this sub-family con­tain 37 genera and 62 species of helminths. There are no reports for Histriophoca fasciata, but the seven re­maining species have been quite well studied.

Cestoda

These are represented by nine species of Diphyllo­bothrium, three species of Diplogonopornus and one each of the remaining genera (Table 87). Common species are found in the harbour seal, Phoca vitulina Linnaeus, 1758; ringed seal, Pusa hispida; bearded seal, Erignathus barbatus Erxleben, 1777 and harp seal, Pagophilus groenlandicus Erxleben, 1777. This large num ber of common cestodes results from the wide­spread distribution of pelagic crustaceans and teleost fish that are the intermediate hosts of diphyllobothriids in northern seas. Further evidence of the success of Diphyllobothrium is its wide representation in the M onachinae of the southern hemisphere (Table 91). O f the eight genera of cestodes listed, only two Ano- phryocephalus and Pyramicocephalus appear to be exclusively pinniped parasites. Trigonocotyle is prim ­arily found in toothed whales; Polypocephalus from elasmobranchs ; Diplongonoporus is shared with whales, sea otter and man, and Schistocephalus is endemic in piscivorous birds.

T he two relict species of Phocinae, the Caspian seal, Pusa caspica Gmelin, 1788 and the Baikal seal, Pusa sibirica Gmelin, 1788 have been well examined but contain few parasites. These two animals will be con­sidered later in this section.

Nematoda

Delyamure (1955) listed seven genera and nine spe­cies of nematodes from the Phocinae, but this has now increased to 16 genera and 21 species (Table 89). O ther than the common ascarid types (Anisakis, Con­tracaecum, Phocascaris, Phoconema, Terranova) we find representatives of five other superfamilies (Diocto- phymoidea, Filarioidea, Metastrongyloidea, Strongy-

T he distribution and intraspecific variation o f helm inth parasites in pinnipeds 343

Table 87. Comparison of helm inth parasites in Phocinae (Cestoda)

Species o f Helm inth

Phocinae

Phocavitulina

Pusahispida

P. P. Erignathus caspica sibirica barbatus

Halichoerus Pagophilus Histriophoca grypus groenlandicus fascia ta

Cestoda

Anophryocephalus anophrys................. +Diphyllobothrium alascense................. ........ +D . cor d a tu m ........................................... ........ + +D. h ians ..................................................D . lanceolatum ...................................... -f + + +D. latum .................................................. + +D . macrocephalus................................... +D. osm eri...............................................D. phocarum........................................... +D . schistochilus...................................... +D . sp ........................................................Diplogonoporous fasc ia tu s ................... +D. m utabilis........................................... -fD . tetrapterus........................................ ........ + + +Polypocephalus tortus............................ +Pyramicocephalus phocarum................. -j_ +Schistocephalus solidus.......................... ........ + +Trigonocotyle skrjabin i........................ ........ + -l-

T able 88. Comparison of helm inth parasites in Phocinae (T rem atoda and Acanthocephala)

Phocinae

Species o f Helm inth Phocavitulina

Pusahispida

P.caspica

P. Erignathus sibirica barbatus

Halichoerus Pagophilus Histriophoca grypus groenlandicus fasciata

Trematoda

Ciureana badamschimi............................ +Cryptocotyle lin g u a ................................. ■ ................ + + +Echinostoma acanthoides........................ ................ + +

Mesorchis advena......................................Metorchis a lb id u s ...................................Microphallus orientalis.......................... ■ f

Orthosplanchnus arcticus........................ + +

0 . frater cu iu s .......................................... - f

Opisthorchis fe lineus ............................... +

0 . tenuicollis.............................................Phocitrema fusiforme............................... ................ + +

Pseudamphistomum truncatum .............. ................ + _i_ + + - fRossicotrema 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. va lidum ............................................... +

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

C. wegeneri.................................................................................... +

344 M . D. Dailey

Table 89. Comparison of helm inth parasites in Phocinae (Nematoda)

Phocinae

Species o f H elm inth Phoca Pusa P . P. Erignathus Halichoerus Pagophilus Histriophocavitulina hispida caspica sibirica barbatus grypus groenlandicus fasciata

Nem atoda

Anisakis rosmari................................................... +A. schupakovi....................................................... +A. s im 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. gym nurus.......................................................... +Phocascaris netsiki................................................ + +P. phocae................................................................ + +Phoconema decipiens........................................... +Skrjabinaria spirocauda...................................... + +Terranova decipiens.......................................... - • + + + + 'Trichinella sp ira lis ............................................. + +Uncinaria lucasi.......................................... + ___________________________________________________________

Table 90. Comparison of helminth parasites in M onachinae (Trem atoda, N em atoda and Acanthocephala)

M onachinae

Species o f Helm inth Monachusmonachus

M . M . schauinslandi tropicalis

Leptonychotesweddelli

Lobodoncarcinophagus

Hydrurgaleptonyx

Ommatophocarossi

Trematoda

Ogmogaster antarcticus................... + +

0 . p lica tu s ......................................... + +

Orthosplanchnus sp ............................ +

Nem atoda

Anisakis pegreffii...............................A. s im 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...............................................

T he distribution and intraspecific variation o f helm inth parasites in pinnipeds 345

Table 91. Comparison of helminth parasites in M onachinae (Cestoda)

Monachinae

Species o f H elm inth Monachus M . M . Leptonychotes Lobodon Hydrurga Ommatophocamonachus schauinslandi tropicalis weddelli carcinophagus leptonyx rossi

Cestoda

Baylisia baylisi.................................................... +Bothriocephalus sp ............................................... +Cysticercus cellulosae........................................... 4-Diphyllobothrium archeri.................................... 4-D. cameroni....................................................... +D . coniceps....................................................... +D . elegans.......................................................... +D. h ians............................................................ + +D . lanceolatum ................................................ +D . lash leyi....................................................... 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. perfolia tus ....................................................... 4 -Phyllobothrium delphini...................................... 4- 4 _

Table 92. Comparison of helm inth parasites in Cystophorinae and Odobenidae (T rem atoda and Cestoda)

Cystophorinae and Odobenidae

Species o f Helminth Cystophora cris ta ta

Mirounga M . leonina angustirostris

Odobenusrosmarus

Trem atoda

Cryptocotyle lin g u a ......................................Metorchis a lb idu s ........................................Microphallus orientalis............................... +Odhneriella rossica ......................................Opisthorchis tenuicollis...............................Orthosplanchnus fraterculus........................

+

Pseudamphistomum truncatum ...................Zalophotrema hepaticum .............................

+

Cestoda

Anophryocephalus atiophrys........................Baylisiella tecta.............................................

+

Diphyllobothrium cor da tu 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 (Nem atoda and Acanthocephala)

Cystophorinae and O dbenidae

Species o f H elm inth Cystophora Mirounga M . leonina Odobenuscristata angustirostris rosmarus

Nem atoda

Anisakis a la ta .......................................................A . bicolor.............................................................. tA. patagonica ....................................................... +A.rosm ari................ +A. s im ilis .............................................................. +Contracaecum osculatum...................................... + +C. radiatum ............................................................C. rectangulum .................................................... +Dirofilaria im m itis ............................................. +Filaria sp ...............................................................Phocascaris cytophorae......................................... +P. osculatum ......................................................... +P. phocae................................................................. +Skrjabinaria spirocauda...................................... +Terranova decipiens.............................................. +Trichinella sp ira lis ..............................................Uncinaria h am ilton i........................................... +

A canthocephala

Corynosoma bullosum........................................... + tC. clavatum............................................................C. semerme............................................................ +C. strumosum.......................................................... +C. va lidu m ............................................................C. sp ................................ +________________________________________________

loidea, Trichuroidea), more than in any other sub­family of Pinnipedia. However, only Otostrongylus, Parafilaroides and Skrjabinaria seem to be unique to pinnipeds. Dioctophyme, Dipetalonema, Dirofilaria, Eustrongyloides (a synonym of Dioctophyme according to Yamaguti, 1961), Halocercus, Trichinella and Un­cinaria are all found in other groups of mammals.

Trem atoda

Delyamure (1955) compared northern and southern true seals and found the northern group infected with eight of the 10 genera represented a t that time. C ur­rently there are 15 genera reported for these groups (Tables 88, 90, 92), of which five (Echinostoma, Mesorcha, Phocitrema, Rossicotrema, Ciureana (a synonym of Cryptoctyle according to Yamaguti, 1958) are unique to Phocinae, and one (Ogmogaster) unique to Monachinae. T he Cystophorinae share all five of their species with Phocinae, and the Monachinae share one genus. However, Zalophotrema is the only genus that is unique to the Pinnipedia. Orthosplanch- nus is primarily a parasite of pinnipeds but has also been reported from sea otters (Rausch, 1953). All others are accidental parasites of pinnipeds, being found typically in other mammals or marine birds. The sharing of Z. hepaticum between P. vitulina and

the northern elephant seal, Mirounga angustirostris Gill, 1866, can most likely be attributed to their south­ern distribution into waters off Baja California, where the parasite is endemic. Orthosplanchnus is universal, being found in both hemispheres.

Acanthocephala

Two genera and 10 species are represented in the Phocinae. B. nipponicus has been previously discussed under the Otariinae. O f the remaining nine species only five are reported from this subfamily. T he most commonly shared species are C. semerme and C. stro- mosum, which are also found in Arctocephalinae, Cystophorinae and O tariinae but are absent in M ona­chinae (Tables 85, 93, 83, 80). The large number of species unique to this group can probably be accounted for by intraspecific variation in response to closely related but different hosts. T he amphipods used as first intermediate hosts in acanthocephalan life cycles are usually fairly non-specific and widely distributed. The same can be said for the fishes which serve as the second intermediate hosts. Therefore universal species such as C. semerme and C. stromosum would be expected with minimal need for spéciation in the populations concerned.

T he two members of the Phocinae with the least

T he distribution and intraspecific variation o f helm inth parasites in pinnipeds 347

number of parasites and smallest geographical distri­bution are the landlocked Caspian and Baikal seals. Delyamure (1955) mentions various workers who have attempted to use the helminth fauna to solve the question of the origin of these two species. In compar­ing the helminths of the Caspian seal with those of northern seals, there are no common species of cestodes or nematodes, but common trematodes and acantho- cephalans occur. Delyamure cites Dogiels’ (1947) ex­planations that the original parasite fauna of relict animals is reduced or lost and is replaced by a few species not normally infecting seals. This is borne out by the addition of non-pinniped trematodes such as Mesorchis and Ciureana and the nam atode Eustrong- lytoides. The Baikal seal has a single helminth para ­site, Contracaecum osculatum. From comparison of this parasite with specimens of C. osculatum taken from the Caspian and northern seals Mozgovoi and Ryzhikov (1950) concluded that the Baikal seal was more similar to northern seals than to the Caspian seal.

Bibliography

Ball, 1930; Baylis, 1916, 1920, 1932; Belopolskaya, 1960; Bruyn, 1933; Creplin, 1825; Delyamure, 1955; Delyamure et al., 1964; Delyamure and Alegseev, 1966; Diesing, 1850; Dogiel, 1947; Dougherty, 1946; Duncan, 1956; Fabricius, 1780; Forssell, 1904; Ger- manos, 1895; Goto and Ozaki, 1930; Guiart, 1935; Heinze, 1934; Höst, 1932; Johnston et al., 1966; Kenyon, 1962; King, 1964; Kurochkin, 1958; K u r­ochkin and Zablotskii, 1958; Leuckart, 1863; Lühe, 1910; Lyster, 1940; Montreuil, 1958; Mozgovoi and Ryzhikov, 1950; Muller, 1776; Neiland, 1962; Odhner, 1905; Owen, 1835; Railliet, 1899; Ransom, 1920; Rausch, 1953; Rudolphi, 1802, 1819; Shchupakov, 1936; Stiles, 1901; Stiles and Hassall, 1899; Stunkard and Alvey, 1929; Taylor et al., 1961; van Cleave, 1953; W ardle, McLeod and Stewart, 1947; Yamaguti, 1939, 1958, 1961; Yurakhno, 1968.

MONACHINAE

The sub-family M onachinae is composed of two groups of seals: the monk seals (Monachus monachus Herm ann, 1779; M . tropicalis Gray, 1850; M.schauins- landi Matschie, 1905), all of temperate waters; and the Antarctic seals (Leptonychotes weddelli Lesson, 1826; Lobodon carcinophagus Hombron and Jacqui- not, 1842; Hydrurga leptonyx Blainville, 1820; and Ommatophoca rossi Gray, 1844).

The cestodes are represented by 23 species, 17 of which are in the genus Diphyllobothrium (Table 91). There are no cestode species common to the monk

seals and Antarcdc seals. Owing to their low numbers and reduced gregarious nature, monk seals are not well represented by helminth parasites. None have been reported from M . tropicalis and only four from M . schauinslandi. In contrast, the Antarctic species minths, with only the two ascaroids, Contracaecum osculatum and Terranova decipiens in common with Antarctic forms, and one cestode, D. hians shared with M . schauinslandi. In contrast, the Antarctic species have a number of common helminths. Leptonychotes and Lobodon share two trematode species of Ogmo- gaster, which is also a common genus in whales (Table 91).

Cestoda

Among the 13 species of cestodes listed for the A nt­arctic seals is Baylisia which is unique to the crab- eater seal Lobodon carcinophagus. The Ross seal has four cestodes, of which D. scotti and D. antarcticus are unique to it. The other two diphyllobothriids, D. mo­bile and D. wilsoni are shared with Lobodon, and Lobodon and Hydrurga respectively. Lobodon and Hydrurga have four species and two genera in com­mon. The wide distribution of Diphyllobothrium and the catholic feeding habits of these seals would tend to account for the infections.

Nematoda

Species infecting members of the M onachinae are all ascaroids except for the lungworm Parafilaroides hydrurgae (Table 90). This appears to be the only reported occurrence of this genus in the southern hemisphere and presents the question of why it is found only in the leopard seal Hydrurga leptonyx? If a coprophagous tidepool fish is the necessary inter­mediate host as seen with P. decorus (Dailey, 1970), then the leopard seals northern migration to warmer areas during winter months may provide the answer. King (1964) states that Hydrurga lives on the outer 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, Leptonychotes and Ommatophoca tend to stay with the ice.

Acanthocephala

Seven species of Corynosoma (Table 90) are known, of which only C. hamanni is found in more than one host.

Bibliography

Ariola, 1900; Baird, 1853; Baylis, 1916, 1920; Bever- ly-Burton, 1971; Cam pana-Rouget and Biocca, 1955;

348 M . D . D ailey

Chapin, 1925; Dailey, 1970; Delyamure, 1955; Dies- ing, 1850; Golvan, 1959; Gower, 1939; Johnston, 1931, 1937; Johnston and Mawson, 1941; Johnston and Best, 1942; Joyeux and Baer, 1936; King, 1964; K rab­be, 1865, 1878; Leiper and Atkinson, 1915; Linstow, 1892, 1905, 1907; Markowski, 1952; Mawson, 1953; Meggitt, 1924; Nickol and Holloway, 1968; Railliet and Henry, 1907, 1912; Rausch, 1969; Rennie, 1907; Rennie and Reid, 1912; Rudolphi, 1802; Shipley, 1907; Yamaguti, 1961, 1963.

CYSTOPHORINAE

The hooded seal Cystophora cristata Erxleben, 1777, northern elephant seal (Mirounga angustirostris) and southern elephant seal (M. leonina) make up the Cy­stophorinae, [but see King, (Relationships of the hood­ed and elephant seals (genera Cystophora and M i­rounga)). J. Zool., 148:385-98. Eds.]. The family Odobenidae contains only one species, the walrus, Odohenus rosmarus Linnaeus, 1758.

Cestoda

The hooded seal is a N orth Atlantic species and shares only the few universal helminths with the temperate and southern Mirounga. Four of the five cestodes reported for Cystophora (Anophryocephalus, Diphyllobothrium latum, Dipogonoporus, Pyramico- cephalus) are also found in the ringed seal Pusa hispida. M . leonina has two species of cestodes, of which Baylisiella tecta is unique, and M . angustirostris has nono. Odobenus has three species of Diphyllobo­thrium, of which D. romeri is unique.

Nematoda

The superfamilies Ascaroidea, Filaroidea, Strongy- loidea and Trichuroidea are represented. T he Diro­filaria sp. reported for Cystophora, and Trichinella spiralis in Odobenus are evidently aberrant parasites for these hosts. T he heartworm Skriabinaria in Cysto­phora also infects two N orth Atlantic seals Phoca vitulina and Pusa hispida. The vector of this parasite is unknown at this time, but mosquitoes are the chief intermediate hosts in other members of this family (Setariidae). Delyamure (1955) discusses the biology and ecology of filarids parasitic upon marine mammals. C. osculatum and T . decipiens are again the most common nematodes reported. The hookworm U. ha- miltoni from the southern elephant seal is also found in the South American sea lion, no doubt as a result of their common distribution.

T rematoda

The trematodes of Cystophorinae (Table 91) have been previously discussed under the northern seals

(Phocinae). T he walrus shares two species of trem a­todes w ith members of the Phocinae, but Odhneriella rossica is unique to it. Only one other species in this genus has been described, it was reported from the white whale Delphinapterus leucas Pallas, 1776 by Price (1932).

Acanthocephala

Only the genus Corynosoma occurs, being represented by three species in Cystophorinae and four in Odobe­nus. C. bullosum is common to Cystophora and both species of Mirounga, while only the polyzonal C. sem­erme and C. stromosum are shared with Odobenus.

Bibliography

Baylis, 1916, 1920; Berland, 1963; Caballero and Peregrina, 1938; Cameron et al., 1940; Creplin, 1825 ; Delyamure, 1955; Delyamure and Skrjabin, 1965, 1966; Delyamure and Treshcher, 1966; Forssell, 1904; Gedoelst, 1911; Hsü, 1935; King, 1964; Markowski, 1952; Monticelli, 1890; O dhner, 1905; Price, 1932; Roth and Madsen, 1953: Schmidt and Dailey, 1971; Skrjabin, 1915; Stiles and Hassell, 1896; Stunkard and Alvey, 1929; Yurakhno, 1968; Zschokke, 1903.

In the preceding comparison of pinniped helminths, several general observations can be made. T he infor­m ation tends to support the assumption that the center of pinniped evolution was the northern hemisphere, specifically the N orth Pacific. T he higher num ber of helminths from hosts in this area indicate a longer association between northern seals than between their southern counterparts. Also, it appears that most of the pinniped helminth parasites are worms supplied by a terrestrial animal reservoir. This is borne out by the fact that only a few genera reported from pinni­peds are not also found in the endemic terrestrial an ­imal populations.

T he reasons for the num ber of helminth parasites in a given host is complex and depends on a variety of coexisting factors (diversity of individuals, zoogeo- graphical distribution, diversity of habitat, behavior patterns, presence or absence of interm ediate hosts, etc.) that apply to both parasite and host. Inasmuch as nearly all of these factors have not been explored sufficiently in either parasite or host, definitive answers to many questions will have to remain unanswered until such information becomes available.

IN T R A SPE C IF IC V A R IA T IO N IN H E L M IN T H S IN F E C T ­

IN G SY M P A T R IC SPECIES O F P IN N IP E D P O P U L A T IO N S

In the preceding tables it is apparent that several species of helminths occur in pinnipeds where popula­tions are sympatric. A good example of this can be

T he distribution and intraspecific variation o f helm inth parasites in pinnipeds 349

BODY LENGTH IN MM

Figure 225. Regression o f esophageal length on body length o f 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 o f each sample.

seen in the lungworms found in the California sea lion (.Zalophus californianus) and Steller sea lion (Eum a- topias jubatus). Four species of the genus Parafilar­oides have been reported for these two sea lions by Dougherty and Herm an (1947): Parafilaroides decorus in Z. californianus and P. prolificus, P. nanus and P. sp. in E. jubatus. The three species from the latter host were described from a single male Steller sea lion at the San Diego Zoo. At Ano Nuevo Island, Santa Cruz County, California the only common ground where these two sea lions mingle in large numbers, Dailey and Hill (1970) found 10 of 14 Z. californianus and four of nine E. jubatus infected w ith lungworms. No P. nanus or P. prolificus were found in that study. Com­prehensive literature reviews by Margolis (1954). De­lyamure (1955), Dailey and Brownell (1972) and M ar­golis and Dailey (1972) reveal that only once have lung­worms been recovered from the Steller sea lion north of Ano Nuevo Island although extensive examinations have been carried out and other helminths reported. This fact, together, with the morphological similarities of the four species, suggests that P. decorus may infect Steller sea Hons only in California, and that in tra ­specific morphological variation, due to host influence, may account for some or all of the lungworm species originally reported from this host.

A study was carried out to determine this possibility by Hill (1971). An unweaned Steller sea lion pup was

captured at Ano Nuevo Island and experimentally infected with P. decorus using techniques similar to Dailey (1970). A dult lungworms recovered from this cross-infection 60 days post-infection were compared morphologically with populations of lungworms ob­tained from two wild caught E. jubatus and Z. cal­ifornianus. Eleven quantitative parameters were meas­ured for each sample. The means of the five samples were compared by one way analysis of variance. Sign­ificant differences were found between samples of various esophageal and body measurements, but not between samples of spicules or vagina vera measure­ments. These differences were best accounted for as arising from a gradient of morphological variation within one species. There did not seem to be any meaningful separation of samples according to host species. The regression of esophageal length on body length showed a significant correlation (P < 0-01 ) (Fig. 225). This study supports including P. nanus, P. prolificus and P. sp. as synonyms of P. decorus.

Future studies of this type, conducted on other closely related species of helminths in sympatric popu­lations of pinnipeds, are needer. Such studies conducted on genera with numerous species, such as Diphyllobo­thrium and Corynosoma, would undoubtedly reveal similar examples of intraspecific variation due to host influence. Davey (1971) has concluded an excellent study on the Anisakis groups where he reduces the

350 M . D. D ailey

existing number of recognized species to only three (A. simplex, A. typica, A . physeteris). In groups such as the Ascaridata, where criteria for taxonomic separ­ation are tenuous a t best, biological evidence seems essential.

A C K N O W L E D G E M E N T S

I would like to express my appreciation to Mrs Jackie Testa, Mrs Lorraine Sjoberg, Mrs Mikel Floth, and M r R alph Appy for their help in the preparation of this paper.

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