Download effects of parasites on marine maniacs

EFFECTS OF PARASITES ON MARINE MANIACS
JOSEPH R. GERACI and DAVID J. ST.AUBIN
Department of Pathology
Ontario Veterinary College
University of Guefph
Guelph, Ontario
Canada
INTRODUCTION
Parasites of marine mammals have been the focus of numerous reports dealing with taxonomy,
distribution and ecology (Defyamure, 1955). Descriptions of associated tissue damage are also available,
with attempts to link severity of disease with morbidity and mortality of individuals and populations. This
paper is not intended to duplicate that Iiterature. Instead we focus on those organisms which we perceive
to be pathogenic, while tempering some of the more exaggerated int~~retations.
We deal with life cycles by emphasizing unusual adap~t~ons of selected organisms, and have necessarily limited our selection of the literature to highlight that theme. For this discussion we address the
parasites of cetaceans---baleen
whales (mysticetes), and toothed whales, dolphins and porpoises (odontocetes): pinnipeds-true
seals (phocidsf, fur seals and sea Iions (otariidsf and walruses (adobenids);
sirenians~anatees
and dugongs, and the djminutive sea otter.
ECTOPARASITES
We use the term “ectoparasite’” loosely, when referring to organisms ranging from algae to fish which
somehow cling to the surface of a marine mammal, and whose mode of attachment, feeding behavior, and
relationship with the host or transport animal are sufficiently obscure that the term parasite cannot be
excluded. What is clear is that these organisms damage the integument in some way.
For example: a whale entering the coid waters of the Antarctic can acquire a yelIow film over its body.
Blue whales so discoiored are known as “sulfur bottoms”. The organisms responsible are diatoms,
principally morphs of Cocconeis ceticoia and ~~vico~~ spp, (Hart, 1935) which attach to the surface by
innocuous sucker-like valves, but on occasion penetrate the epidermis and become saprophytic (Hart,
1935). The film is shed when the whales return to warmer waters.
Several arthropods atso injure the integument of whales by burrowing to secure firm anchorage. Such
are the sessile barnacles (~ir~pedia) Coro~iii~ d~ude~u and C~~pt~~e~~s r~~&~j~~ecti which attach so
deeply onto their respective hosts, the humpback whales, ~eg~~teru novueo~gliae, and gray whales,
Eschrictius gibbosus (Andrews, 1914; Clarke, 1966), that when the organisms are shed or removed, a pit
remains which eventually becomes a scar (Scheffer, 1939). Similarly, aberrant sessile barnacles, Xenobalanus globicipitis, burrow deeply in odontocetes, leaving characteristic star-shaped scars (Bane & Zullo,
1980). They align in such a way along the trailing edges of fins and flukes, that host dolphins long ago
became known as “tassle-fins”’ (True, 1891).
An equally decorative, but more serious tissue-invader is Penella bo~ffe~o~te~ue (family Pennellidae),
one of the largest parasitic copepods. It penetrates the skin of mysticetes and anchors within the blubber
(Clarke, 1966). The attachment is so “clean” as to be envied by population biologists seeking to devise a
permanent ~r~utaneous
mark for whales.
Whale lice (Amphipoda: Cyamidae) are less ornamental, and in fact are among the more unsightly
surface dwellers. Those of odontocetes are cosmopolitan, while on mysticetes they are more host-specific
(Leung, 1970). Cyamids reside in fissures and crevices, around sessile barnacles, and on the callosities on
the heads of right whales, (Leung, 1976; Scheffer, 1939). They are assumed to graze on algae, and
probabty ingest exfoliating epidermal cells as well (Leung, 1976).
Marine mammals are also parasitized by more conventional lice and mites. Sucking lice belonging to the
40X
.I’.!?. Grraci
and D.J. St. Althin
family Echinophtheridiae
(Siphunculata.
.4nopleura) concentrate on the head, neck, and flippers of
pinnipeds (Kim, 1972), causing little more than mild irritation (Fay, 1982). Transmission of lice, and
reproduction on the host occur when seals are out of water (Murray, 1964). Thus, heavy infestations
provide a clue that seals have spent an inordinate amount of time on land-a
behaviour normally
associated with illness. Not surprisingly then, we find heavy infestations of Echinophthirius horridus
associated with poor body condition in harbor seals, Phoccl vituliru~.Quite apart from any direct effect, E.
horridus can also serve as an intermediate host of the heartworm Dipetalonema
spirocauda (Geraci,
Fortin, St. Aubin & Hicks, 1981).
Mites (Demo&x sp.) can cause mange-like lesions in captive California sea lions, Zulophus culiforniunus (Nutting & Dailey, 1980). As in other species, the clinical condition may be an expression of
lowered immune function associated with the captive environment of the host. No similar infections have
been noted in the wild.
By far the largest organisms that attach to the surface of marine mammals are fish. Whalesuckers,
Remilegia austrulis, are obligate commensals (Rice & Caldwell, 1961), which can fasten firmly enough to
withstand the aerobatics of spinner dolphins, Stenella longirostris, and leave oval lesions in the host’s
epidermis. Whalesuckers typically do not feed on host tissue, though Rice and Caldwell (1961) found
epidermal tissue in the stomachs of two specimens. Lampreys, Entosphenus trident&us, on the other hand
rely on cetacean skin as a source of nutrients. Attached by the teeth of its sucking disc, the lamprey uses
a rasping tongue to abrade the epidermis down to the blubber (Pike 1951). As such, it can be regarded as
the most voracious marine mammal parasite.
ENDOPARASITES
Protozoa
Internal parasites of marine mammals tend to be less specialized to the marine environment than those
which colonize the surface. While their location and pathogenicity may be more predictable, their life
cycles are generally obscure, if not enigmatic. An example can be drawn from sarcosporidians which
infect muscle tissues of pinnipeds (Migaki & Albert, 1980) and cetaceans (Akao, 1970). On land, infection
with this parasite requires that the animal consume fecal sporocysts of the genus Surcocystis. Yet no
sexual stages of Surcocystis are reported from marine organisms, and only Eimeriu sp. are known from
marine mammals (Hsu, Melby & Altmman, 1974; Lainson, Naiff, Best & Shaw, 1983). Marine bird
droppings contain Isosporu-type oocysts which may prove to be those of Sarcocystis sp. (Pellerdy, 1974),
but any proposed transmission in and out of a seal or whale would require still unexplained feeding
patterns.
Equally curious is the finding of toxoplasma-like organisms in a harbor seal, Phoca vitulina, which had
never contacted feral or domestic felids, or their fecal material (Van Pelt & Dieterich, 1973). The seal,
taken from the wild as a newborn pup, was thought to have acquired the organism through the placenta.
Still unresolved is the source of the original infection in the mother.
An unusual adaptation is that of free-living holotrich ciliates in the upper respiratory tract of bottlenose
dolphins, Tursiops truncutus (Woodard, Zam, Caldwell & Caldwell, 1969). Dolphins along the Florida
coast harbor these protozoa, apparently without ill effect. Under certain conditions, the organism can
invade the lung and result in pneumonia. As far as we know, this is the only facultative endoparasite of
marine mammals.
Arthropods
Normally associated with the exterior surface of marine mammals, arthropods also parasitize the nasal
passages, trachea, and bronchi of pinnipeds. Nasal mites (Acarina: Gamasidae) of the genus Huluruchne
infest phocid seals (Arundel, 1978) and occasionally sea otters, Enhydru lutris (Kenyon, Yunker &
Newell, 1965); the genus Orthohaluruchne is found in otariids and walruses, Odobenus rosmurus (Kim,
Haas & Keyes, 1980; Fay & Furman, 1982). Mites can cause enough damage to mucous membranes to
affect an animal’s health adversely. Paroxysmal coughing and nasal contact transmit motile larvae
concentrated in the anterior portions of the airways (Kim et al., 1980). Adult mites anchor to mucosal
surfaces and, unlike sucking lice, cannot survive outside the moist environment of their host. They are
truly endoparasites.
Cestodes
Marine mammals host adult and larval stages of cestodes. Infections with mature pseudophyllideans,
principally Diphyllobothrium sp., are usually innocuous (Arundel, 1978), but in extreme circumstances
can result in debilitation and death of the host. The parasites can encyst in the colonic wall, or as a mass
weighing more than lkg, can obstruct the lumen of the gut (Cordes & O’Hara, 1979).
Parasites of Marine mammals
409
Larval tetraphyllideans
of the genera Phyllobothrium and Monorygma are distributed ubiquitously
among cetaceans and pinnipeds (Testa & Dailey, 1977). The parasites are presumed to complete their life
cycle in sharks (Delyamure, 1955), which either prey on marine mammals (Wood, Caldwell & Caldwell,
1970), or consume their remains (Clarke & Merrett, 1972). Phyllobothrium larvae encyst in blubber; those
of Monorygma localize in abdominal musculature or append to viscera. Their concentration in abdominal
tissues (Geraci, Testaverde, St. Aubin & Loop, 1978) probably reflects migration from the gut, and offers
some advantage in transmission to sharks, which show a predilection for attacking this vulnerable area.
The unusual finding of larval stages of Taenia solium in a Cape fur seal, Arctocephalus pusillus, signals
exposure to human fecal material, perhaps indirectly by consumption of a fish which had recently fed on
a gravid proglottid (De Graaf, Shaughnessy, McCully & Verster, 1980). Alternatively, the seal might have
been infected by feeding on contaminated invertebrates or carrion.
Acanthocephala
Bolbosoma and Corynosoma are two of the principal genera (subfamily Corynosomatinae)
of acanthocephalans which localize in the intestine of marine mammals (Arundel, 1978; Golvan, 19.59). The
worms cause little more than local irritation with occasional ulceration at the site of attachment, and are
usually of little pathological significance despite the occurrence in some hosts of thousands of parasites.
Heavy infestations in sea otters (Enhydra lutris) have been associated with ulceration and perforation of
the intestinal wall (Morejohn, Ames & Lewis, 1975).
Digenea
Digeneans parasitize the gastrointestinal
system of marine mammals, and also the nasal and cranial
sinuses of small cetaceans. Within the lumen of the gut or in nasal passages, they have little impact on the
host, but within the parenchyma of organs. They can be destructive. In the extreme, errant migrants from
the cranial sinuses somehow reach the brain, leading inevitably to the death of infected dolphins.
Throughout the gastrointestinal
system, digeneans have adapted to a broad spectrum of microenvironments. One of the more interesting is Labicola elongata (Monostromata: Labicolidae) which resides in
abscesses in the upper lip of dugongs, Dugong dugon (Blair, 1979). Tracts connecting the abscesses to the
labial mucosa presumably allow for the release of ova. Further along the alimentary canal, other digeneans
form similar cysts in the walls of the stomach and intestine. Braunina cordiformis (Strigeata: Brauninidae)
attaches to the lining of the second and third stomach compartments of odontocetes, and becomes nearly
enveloped by an outgrowth of vascularized connective tissue (Schryver, Medway & Williams, 1967).
Pholeter gastrophilus (Fasciolata: Troglotrematidae)
resides within fibrotic nodules in the submucosa of
the stomach, and elicits an intense inflammatory reaction (Woodard et al., 1969). The most detrimental of
these parasites seems to be Microphallus pirum (Microphallidae) which matures in the intestinal wall of
the sea otter (Rausch, 1953), and causes potentially fatal hemorrhagic enteritis.
In the pancreas and hepatobiliary system of nearly all marine mammals, members of the genera
Campula, Zalophotrema, Oschmarinella, and Orthosplanchnus induce necrosis of parenchymal tissue,
and chronic fibrosis and hyperplasia of ducts (Woodard et al., 1969; Fleischman & Squire, 1970). Campula
oblonga infects virtually all mature harbor porpoises, Phocoena phocoena, stranded along the New
England coast of the United States. In many of these animals, we have noted pancreatic fibrosis that was
sufficient to extensively compromise digestive and endocrine function, and we therefore presume that this
condition is a significant factor leading to natural mortality.
Other digeneans which have a major impact on small cetaceans are members of the genus Nasitrema
(Nasitrematidae). Normally an innocuous inhabitant of cranial sinuses (Neiland, Rice & Holdin, 1970), the
organism can invade the brain and cause extensive necrosis (Ridgway & Dailey, 1972). A similar condition
occurs in Amazon River dolphins, Inia geoffrensis, in which the campulid Hunterotrema macrosoma is
associated with both pulmonary and cerebral lesions (Woodard et al., 1969; Dailey, 1971). Cerebral
infection with Nasitrema sp. is a major factor in natural mortality of common dolphins along the Pacific
coast of the United States (Dailey & Walker, 1978), and is one of the few examples of parasitism linked
directly to stranding.
Nematoda
The most popular hypothesis advanced to explain cetacean mass strandings is that the metastrongylid
nematodes Stenurus minor and S. globicephalae lodge in the middle ear, and interfere with echolocation
and orientation (Delyamure, 1955). The evidence is fragmentary. Many whales and dolphins harbor
Stenurus sp. (Arnold & Gaskin, 1975), yet there are no reports of associated lesions. In stranded Atlantic
white-sided dolphins, Lagenorhynchus acutus, we have found as many as 3,300 worms densely clustered
in the cranial sinuses and extending into the middle ear (Geraci ef al., 1978). For the most part, the
410
J.R. Geraci and D.J. St. Auhin
nematodes elicit low grade inflammation of the mucous membranes, and rarely purulent sinusitis. The
condition, while likely to cause discomfort, would probably not impair hearing, unless the nematodes or
some toxic excretion were to penetrate into the inner ear. Because sound conduction in cetaceans depends
only partially on the movement of auditory bones (McCormick, Wever, Palin & Ridgway, 1970), the mere
presence of nematodes on those structures would not necessarily impede hearing-and
by extension
echolocation. It seems that Stenurus has been implicated in cetacean strandings more by the desire for a
simplistic answer than through any accumulated scientific evidence.
While the effect of Stenurlls remains in doubt, there is little question that other pseudaliid nematodes
can cause severe pulmonary infection in cetaceans. The Atlantic harbor porpoise can become host in the
extreme, with Pseudalius inpexus, S. minor, Torynurus convolutus, and Halocercus invaginatus all
crowding the main-stem bronchi (Arnold & Gaskin, 1975). There are always some associated lesions,
particularly with Halocercus sp. Adult worms, with coiled cephalic ends lodged firmly within bronchioles,
induce mucopurulent bronchitis and pneumonia (Cowan & Walker, 1979). Larvae in the sputum may be
destined for direct transfer to another host (Woodard et al., 1969) while adults eventually die and either
liquify or become enveloped in firm fibrous or calcified nodules. The consequence of infection can only be
surmised. Pneumonia must place a stiff burden on diving mammals compelled to keep pace with the herd.
Many do, as evidenced by the high prevalence of parasitic lesions in the lungs of robust free-ranging
cetaceans (Cowan, 1966; Conlogue et al., 1985). Others die as a direct effect, or through bacterial and
cardiovascular complications (Andersen, 1974), or hypersensitivity to the parasites (Sweeney & Ridgway,
1975).
Hypersensitivity
reaction is also associated with Parafilaroides decorus (Fleischman & Squire, 1970)
infection in California sea lions, Zalophus californianus (Sweeney & Gilmartin, 1974). Larvae induce
acute bronchitis, and bronchopneumonia
(Nicholson & Fanning, 1981), and stimulate mucous secretion
which can lead to asphyxiation. P. decorus is the only pseudaliid parasite of marine mammals for which
a life cycle is proposed, and the first metastrongylid found to utilize a vertebrate (a small tidal-pool fish,
Girella nigricans) as a single intermediate host (Dailey, 1970).
Parafilaroides sp. also infect phocid seals, but only the large crenosomatid nematode, Otostrongylus
circumlitus, has been associated with clinical disease, primarily in young harbor seals and ringed seals,
Phoca hispida. The parasite obstructs airways, causing bronchitis and pneumonitis,
and can penetrate
pulmonary vessels to emerge in the right ventricle (Van Den Broek & Wensvoort, 1959). Among 800
harbor seals stranded along the New England coast, 0. circumlitus was most prevalent in animals under
two years of age. It is not clear whether this pattern of infection relates to a change in food (intermediate
host) preference, acquired immunity, or early mortality of infected animals.
Captive harbor seals (Medway & Wieland, 1975) and sea lions (Forrester, Jackson, Miller &Townsend,
1973) can be infected with Dirofilaria immitis, the heartworm of other canids. However, the heartworm
that infects free-ranging seals is Dipetalonema spirocauda (Van Den Broek & Wensvoort, 1959; Schroeder
et al, 1973). The louse E. horridus is a natural vector (Geraci et al., 1981) for the worms which, as adults,
reside in the right heart and pulmonary arteries. Here, they and their microfilariae induce proliferation and
necrosis of vascular endothelium, and form verminous emboli leading to granulomatous pneumonia (Dunn
& Wolke, 1976). We might expect that pulmonary and cardiovascular complications associated with
heartworm would seriously reduce a seals’ ability to dive and feed. However, we have no direct
measurement of diving performance in infected animals.
One of the most devasting parasites of pinnipeds is Uncinaria lucasi, the hookworm responsible for
mass mortalities among the pups of fur seals, Callorhinus ursinus (Olsen, 1958). It is one of the few
nematodes transmitted in milk. Infective third stage larvae, possibly influenced by hormones in the
pregnant cow (Lyons & Keyes, 1978), migrate from the belly blubber to the mammary glands. Newborn
pups can consume as many as 1500 larvae with the first meal of milk, and two weeks later develop
potentially fatal hemorrhagic diarrhea and anemia. Eggs shed by survivors hatch in late summer, or in
spring after overwintering,
and develop eventually into soil-borne free-living third-stage larvae. These
penetrate the skin of seals of all ages, migrate to the belly blubber, and become a threat only to the next
generation of suckling pups. The tissue phase of the parasite affords protection from the hazards of
overwintering in the soil when temperatures can be lethal and seals are unavailable (Olsen & Lyons, 1965).
The most cosmopolitan of marine mammal parasites are the anisakine nematodes, Phocanemu decipiens, and several species of the genera Contrucuecum and Anisakis. The worms can be found free within
the stomach or attached to the gastric mucosa. Penetration by larvae (Young & Lowe, 1969) and adults
(McClelland, 1980) can lead to ulcers (Schroeder & Wegeforth, 1935), perforation into the abdominal
cavity (Fiscus, Baines & Wilke, 1964), and gastritis which may have an allergic component. Infections are
generally not serious to the host. However, marine mammals shed larvae which eventually infect
commercially valuable fish. People who eat the fish become ill (Margolis, 1977), and seals, for their role,
become targets of organized culls. In that sense, the parasite can indeed be fatal!
Parasites
of Marine mammals
411
The only other organism which rivals the public health importance of the anisakine nematodes is the
arctic form (Britov, 1977; Dick & Chadee, 1983) of Trichinella spiralis. Polar bears, Ursus maritimus, and
walruses, and to a lesser extent ringed seals and beluga whales, Delphinapterus leucas, are among the
many northern species infected (Rausch, 1970) by eating contaminated carrion and prey, including marine
amphipods (Fay, 1967) and fish (Kozlov, 1971). The literature on “arctic trichinosis” is dominated by
reports of periodic outbreaks among native people (Margolis, Middaugh & Burgess, 1979). We know of no
description of the effect of the organism on the host marine mammal, which is surprising in light of its
known pathogenicity in other species.
Placentonema and Crussicuuda (subfamily Crassicaudinae)
are the largest nematodes of cetaceans.
They were once prominent for that fact, but are now being reconsidered for their role as pathogens. The
parasites are peculiarly adapted to embed their cephalic ends into soft tissues, frequently those of the
urogenital system. Their posterior ends hang freely within a lumen, providing a mechanism for discharging
fertilized eggs into the sea. Thus the 9-m long P. gigantissima infects the uterus of the sperm whale.
Physeter catodon, early in pregnancy, and matures in the placenta of the developing fetus (Skrjabin,
Sobolev & Ivashkin, 1967). Crussicauda sp. are found in rorqual whales, entwined within genital tissues
(Gibson, 1973), and in kidneys where they induce the formation of large fibrous digitate structures
(Cockrill, 1969) that extend into the vena cava and hepatic portal vein (Gibson, 1973). In small cetaceans,
immature forms of C. grumpicolu migrate in fascia beneath the blubber and emerge in mammary glands
where they destroy functional secretory tissue. While the ova-rich milk presents no threat of infection to
the newborn, the effect of reduced lactation may lead to lower calf survival and herd productivity (Geraci,
Dailey & St. Aubin, 1978).
Adult Crassicuuda sp. also appear in the soft tissue of the cranial sinuses, and are associated with
lesions particularly in the developing pterygoid bone of juvenile dolphins (Walker & Cowan, 1981). The
absence of residual osseous lesions in older animals is strong evidence that parasitic infection is fatal in
young dolphins (Perrin & Powers, 1980; Walker & Cowan, 1981). Further studies are likely to reveal that
Crassicaudu sp. constitutes a significant factor in natural mortality of these and other (Raga, Barbonell &
Raduan, 1982) small odontocetes.
SUMMARY
This report examines the broad range of organisms which can parasitize marine mammals, and identifies
those which we feel have the greatest impact on individuals and populations.
Many parasites colonize and damage the integument in some way. Only the sucking lice of seals are
associated with debilitating disease. In addition, at least one species, E. horridus can serve as intermediate
host of the seal heartworm, D. spirocuudu.
Of the few protozoa, the one deserving most attention is Surcocystis sp. Its ubiquitous distribution
challenges our understanding of coccidian life cycles as currently perceived.
Acanthocephalans
and cestodes are rarely associated with clinically significant illness. It is intriguing
that cetaceans and pinnipeds serve as mammalian intermediate hosts for larval tetraphyllidians destined
to mature in elasmobranchs.
Digeneans occupy the gastrointestinal
tract and severely damage liver and pancreas of cetaceans.
Nusitrema
sp. infects cranial sinuses of small odontocetes, and enters the brain, thereby leading to
stranding and death in selected populations.
Nematodes represent the broadest group of parasites. Pseudaliids often infect the respiratory system,
causing sufficient damage to affect survival. There is no evidence that Stenurus sp., a pseudaliid inhabiting
the cranial sinuses of some whales and dolphins, plays any role in mass strandings, as has been popularly
suggested. Filarioids are highly pathogenic in pinnipeds and are probably responsible for significant
mortality, especially in young animals. Anisakine nematodes in the stomach are of little consequence to
the host. The role of marine mammals in transmitting the parasites to commercially exploited fish stocks
is a public health issue. The only other parasite which represents a threat to humans is Trichinella spiralis,
which is widespread in Arctic mammals.
The Crassicaudinae are the largest nematodes in cetaceans. Evidence is accumulating that the damage
they cause in cranial bone, mammary tissue and the urinary tract may influence productivity and survival
among certain groups.
Most of our understanding
of the parasites of marine mammals derives from studies on specimens
which come ashore. The information is fragmentary, and suffers from our inability to follow the progress
of infection and the overall condition of the parasitized animal. Yet we might conclude that the parasitism
we see is as advanced as can be tolerated by the host. Weak animals retreat from the protection of the
herd, become vulnerable to predators, and probably cannot survive in an environment which places heavy
demands on thermoregulation,
respiration and mobility.
412
J.R. Geraci and D.J. St. Aubin
Acknowledgements-We
thank the New England Aquarium, Boston, MA,
Canada, Arctic Biological Station, for their support in the collection and
Lautenslager and N.C. Palmer, Ontario Ministry of Agriculture and Food,
Watkins, Department of Pathology, Ontario Veterinary College, University
and Department of Fisheries and Oceans
examination of specimens, and Drs. J.P.
Guelph, and Drs. B.M. McGraw and A.R.
of Guelph, for reviewing the manuscript.
REFERENCES
AKAO S. 1970. A new species of Sarcocystis
parasitic in the whale Balaenoptera
borealis. Journal of Protozoolog!
17: 290-294.
ANDERSENS.H. 1974. A typical case history of the net-caught harbour porpoise, Phocoena phocoena, from Danish
waters. Aquatic Mammals 2: l-6.
ANDREWSR.C. 1914. The California gray whale (Rhachianectes glaucus Cope). Its history, habits, external anatomy.
osteology and relationship. In: Memoirs of the American Museum of Nutural History. Series 2 Vol. 1, No. 5, pp
229-289.
ARNOLD P.W. & GASKIN D.E. 1975. Lungworms (Metastrongyloidea:
Pseudaliidae) of harbor porpoise Phocoena
phocoena (L. 1758). Canadian Journal of Zoology 53: 713-735.
ARUNDEL J.H. 1978. Parasites and parasitic diseases of Australian marine mammals. In: The University of Sydney,
Post-Graduate Committee in Veterinary Science, Proceedings No. 36 of Course for Veterinurians pp 323-333 Lincoln
House, Sydney, Australia.
BANE G.W..& Z~LLO V.A. 1980. Observations on a stranded goosebeaked whale (Ziphius cavirostris, Cuvier 1823) and
its ectocommensal barnacles (Xenobalanus plobicipitis). The Journal of Elisha Mitchell Scientific Society 96: 1-3.
BLAIR D. 1979. A new family of Monostome fluk’es (Platyhelminths,~Digenea)
from the Dugong, Digong dugon
(Miiller). Annales de Parasitologie 54: 519-526.
BRI~OV V.A. 1977. Detection of the genetic relationship among nematode species of the genus Trichinella. Genetika
13: 1025-1029.
BROEKV. VAN DEN
&
Saugetierkundliche
WENSVOOR-rP. 1959. On parasites of seals from the Dutch coastal waters and their pathogenity.
Mitteilungen 7: 5841.
CLARKE M.R. & MERRETT i. 1972. The significance of squid, whale and other remains from the stomachs of
bottom-living deep-sea fish. Journal of the Marine Biolopica[ Association of the United Kingdom 52: 599403.
CLARKE R. 1966. The stalked barnacle”Conchoderma,
ectoparasitic on whales. Norsk Hvalfangst-Tidene Norwaegian
Whaling Gazette 55: 153-I 68.
COCKRILLW.R. 1960. Pathology of the cetacea. A veterinary study of whales. British Veterinury Journal 116: l-28.
CONLOGUEG.J., OGDEN J.A. & FOREYTW.J. 1985. Parasites of the Dali’s porpoise (Phocoenoides daUiTrue). Journal
of Wildrife Diseases 21: 160-166.
CORDS
COWAN
D.O. & O’HARA P.J. 1979. Diseases of captive marine mammals. Nebv Zealand Veterinury Journal27: 147-150.
D.F. 1966. Pathology of the pilot whale Globicephala melaena. A comparative survey. Archives of Pathology
82: 178-189.
D.F. & WALKERW.A. 1979. Disease factors in Stenella attenuutta and Stenella longirostris taken in the eastern
tropical Pacific yellowfin tuna purse seine fishery. Administrative Report No. LJ-79- 32C. National Marine Fisheries
Service, Southwest Fisheries Center, La Jolla, CA, U.S.A. 21 pp.
DAILEY M.D. 1970. The transmission of Parafilaroides decovus (Nematoda: Metastrongyloidea)
in the California sea
lion (Zalophus californianus). Proceedings of the Helmintholonical Societv of Washington 37: 215-222.
DAILEY M.i). 1971. -A new species of Hinthrotrema (Digenea: Campulidaej from the Amazon river dolphin (Inia
COWAN
geogrensis).
Bulletin Southern California Academy of Sciences 70: 79-80.
DAILEY M.D. & WALKERW.A. 1978. Parasitism as a factor (?) in single strandings of southern California cetaceans.
Journal of Parasitology64:
593-596.
A.S., SHAUGHNESSYP.D., MCCULLY R.M. & VERSTERA. 1980. Occurrence of Taeniu soliumin acape fur
seal (Arctocephalus pusillus). Onderstepoort Journal of Veterinary Research 47: 119-120.
DELYAMURES.L. 1955. Helminthofauna of Marine Mammals (Ecology and Phylogeny). (Edited by Skrjabin K.1.)
lzdatel’stvo Akiademii Nauk SSSR, Moscow.
DICK T.A. & CHADEE K. 1983. Interbreeding and gene flow in the genus Trichinella. Journal of Parasitology
DE GRAAF
69: 176-180.
DUNN J.L. & WOLKE R.E. 1976. Dipetalonema
spirocuuda infection in the Atlantic harbor seal (Phoca vitu/ina
Journal of Wildlife Diseases 12: 531-538.
FAY F.H. 1968. Experimental transmission of Trichinella spiralis via marine amphipods. Canadian Jcmrnal of Zoolog?
concolor).
46: 597.
FAY F.H. 1982. Ecology and biology of the Pacific walrus. Odobenus rosmarus divergens Illiger. North American Fauna
Report No. 74. U.S. Department of the Interior, Fish and Wildlife Service, Washington, DC, U.S.A. 279~~.
FAY F.H. & FURMAND.P. 1982. Nasal mites (Atari: Halarachnidae) in the spotted seal, Phocu largha Pallas, and other
pinnipeds of Alaskan waters. Journal of Wildlife Diseases 18: 6348.
FISCUS C.H., BAINES G.A. & WILKE F. 1962. Pelagic fur seal investigations, Alaska waters. U.S. Fish and Wildlife
Services,
Special Scientijc
Report on Fish 475: 1-59.
FLEISCHMANR.W. and SQUIRE R.A. 1970. Verminous pneumonia in the California sea lion (Zalophus californianus).
Pathologia Veterinaria 7: 89-101.
FORRESTERD.J., JACKSONR.F., MILLER J.F. & TOWNSENDB.C. 1973. Heartworms
Journal of American
Veterinary Medical Association
163: 568-570.
in captive California sea lions.
Parasites of Marine mammals
413
GERACI J.R., DAILEY M.D & ST. AUBIN D.J. 1978. Parasitic mastitis in the Atlantic white-sided dolphin, Lagenorhynchus acutus, as a probable factor in herd productivity. Journal of Fisheries Research Board of Canada
35: 1350-1355.
GERACI
J.R., TESTAVERDES., ST. AUBIN D.J. & LOOP T. 1978. A mass stranding of the Atlantic white-sided dolphin,
acutus: A study into pathobiology and life history. National Technical Information Service,
Washington, DC. U.S.A. PB289-361. 141 pp.
GERACI J.R., FORTIN J.F., ST. AUBIN D.J. & HICKS B.D. 1981. The seal louse, Echinophthirius
horridus: An
intermediate host of the seal heartworm, Dipetalonema spirocauda. Canadian Journal of Zoology 59: 1457-1459.
GIBSOND.I. 1973. Some “blue” whale nematodes. Parasitology 67: viii-ix.
GOLVAN Y.J. 1959. Acanthocephales
du genre Corynosoma Liihe 1904 parasites de mammiferes d’Alaska et de
midway. Annales de Parasitologic Humaine et Comparee 38: 288-321.
HART J. 1935. On the diatoms of the skin film of whales, and their possible bearing on problems of whale movement.
Discovery Report 10: 247-282.
Hsu C.K., MELBY E.C. & ALTMAN N.H. 1974. Eimeria phocae sp.n. from the harbor seal (Phoca vitutina concolor).
Lagenorhynchus
Journal of Parasitology 60: 399402.
KENYON K.W., YUNKER C.E. & NEWELL I.M. 1965. Nasal mites (Halarachnidae) in the sea otter. Journal of
Parasitology 51: 960.
KIM K.C. 1972. Louse populations of the northern fur seal (Callorhinus ursinus). American Journal of Veterinary
Research 33: 2027-2036.
KIM K.C., HAAS V.L. & KEYES M.C. 1980. Populations. microhabitat preference and effects of infestation of two
species of Orthohalarachne (Halarachnidae: Adarina) in the northern fur seal. Journal of Wildlife Diseases 16: 45-52.
KOZLOV D.P. 1971. K voprosu o putyakh zarazheniva lastonogikh trikhinel-lezom. Trudv Gel’mintoloaicheskoi
Laboratorii Akademii Nauk SSSR 21: 36-40. (Sources of Tri%hinella spiralis infection in pinnipeds. -Fisheries
Research Board of Canada 1974, Translation Series No. 3010).
LAINSON R., NAIFF R.D., BEST R.C. & SHAW J.J. 1983. Eimeria trichechi nsp. from the Amazonian manatee,
Trichechus inunguis (Mammalia: Sirenia). Systematic Parasitology 5: 287-289.
LELJNC Y.M. 1970. First record of the whale-louse genus Syncyamus (Cyamidae: Amphipoda) from the western
Mediterranean, with notes on the biology of adontocete cyamids. In: Investigations of Cetacea Vol. II, pp 243-247
(Edited by Pilleri G.) Printed by Benteli Ag, Berne-Bumpliz, Switzerland.
LEUNC Y.M. 1976. Life cycle of Cyamus scammoni (Amphipoda: Cyamidae), ectoparasite of gray whale, with a
remark on the associated species. Scientific Report of Whales Research Institute 28: 153-160.
LYONS E.T. & KEYES M.C. 1978. Observations on the infectivity of parasitic third-stage larvae of Uncinaria lucasi
Stiles 1901 (Nematoda: Ancylostomatidae) of northern fur seals, Callorhinus ursinus Linn., on St. Paul Island,
Alaska. Journal of Parasitology 64: 454-458.
MARGOLISH.S., MIDDAUGHJ.P. & BURGESSR.D. 1979. Arctic trichinosis: Two Alaskan outbreaks from walrus meat.
Journal of Infectious Diseases 139: 102-105.
MARGOLISL. 1977. Public health aspects of “codworm”
infection: A review. Journal of Fisheries Research Board of
Canada 34: 887-898.
MARLOWB.J. 1975. The comparative behaviour of the Australasian sea lions Neophoca cinerea and Phocarctos hookeri
(Pinnipedia: Otariidae). Mammalia 39: 159-230.
MCCLELLANDG. 1980. Phocanema decipiens: Pathology in seals. Experimental Parasitology 49: 405419.
MCCORMICKJ.G.. WEVER E.G.. PALIN J. & RIDGWAYS.H. 1970. Sound conduction in the dolphin ear. Journal ofthe
Acoustical
Society of America 48: 1418-1428.
MEDWAYW. & WEILANDT.C. 1975. Dirofilaria immitis infection in a harbor seal. Journal of the American Veterinary
Medical Association
167: 549-550.
MIGAKI G. & ALBERT T.F. 1980. Sarcosporidiosis
Association
in the ringed seal. Journal of the American
Veterinary Medical
177: 917-918.
MOREJOHNG.V., AMES J.A. & LEWIS D.B. 1975. Post mortem studies of sea otters, Enhydra lutris L., in California.
California Department of Fish & Game, Marine Resources Technical Report No. 30. 82 pp.
MURRAY M.D. 1964. Ecology of the ectoparasites of seals and penguins. In: Proceedings of the Symposium on
Antarctic Biology, Paris (1962) pp. 241-245 International Congress on Entomology, London, U.K. pp. 366.
NEILAND K.A., RICE D.W. & HOLDEN B.L. 1970. Helminths of marine mammals. I. The genus Nasitrema, air sinus
flukes of delphinid cetacea. Journal of Parasitology 56: 305-316.
NICHOLSONA. & FANNINGJ.C. 1981. Parasites and associated pathology of the respiratory tract of the Australian sea
lion, Neophoca cinerea. In: Wildlife Diseases of the Pacific Basin and Other Countries pp 178-181 Proceedings of the
4th International Conference of the Wildlife Disease Association, Sydney, Australia.
NUTTING W.B. & DAILEY M.D. 1980. Demodicosis (Atari: Demodicidae) in the California sea lion, Zalophus
californianus.
Journal of Medical Entomo!ogy
17: 344-347.
OLSEN O.W. 1958. Hookworms, Uncinaria lucasi I. Stiles, 1901, in fur seals, Callorhinus ursinus (Linn.), on the
Pribilof Islands. In: Twenty-third North American Wildlife Conference Proceedings- pp
_. 152-175.
OLSEN O.W. & LYONS E.T: 1965. Life cycle of Uncinaria lucasi Stiles, 1901 (Nematoda: Ancylostomatidae)
of fur
seals, Callorhinus ursinus Linn., on the Pribilof Islands. Alaska. Journal of Parasitoloav 51: 689-700.
PELLERDYL.P. 1974. Coccidia and Coccidiosis. Second Edition. Akademiai Kiado, Budapest and Paul Parey, West
Berlin.
PELT R.W. VAN & DIETERICHR.A. 1973. Staphylococcal infection and toxoplasmosis in a young harbor seal. Journal
of Witdtife Diseases 9: 258-261.
414
J.R. Geraci and D.J. St. Aubin
PERRIN W.F. & POWERSJ.E. 1980. Role of a nematode in natural mortality of spotted dolphins. Journal of Witdlife
Management
44: 960-963.
PIKE G.C. 1951. Lamprey marks on whales. Journal of the Fisheries Research Board of Canada 8: 27X-280.
RAGA J.A., BARBONELLE. & RADUAN M.A. 1982. Incidence of parasites in stranded Cetaceae on the Spanish
Mediterranean coasts. Memorias do Museo do Mar Serie Zoologica 2: l-l 1.
RAUSCHR.L. 1953. Studies on the helminth fauna of Alaska XIII. Disease in the sea otter, with special reference to
helminth parasites. Ecology 34: 584-604.
RAUSCH R.L. 1970. Trichinosis in the arctic. In: Trichinosis in Man and Animals pp 348-373 (Edited by Gould S.E.)
Charles C. Thomas, Springfield, Illinois, U.S.A.
RICE D.W. & CALDWELL D.K. 1961. Observations on the habits of the whalesucker (Remilegia australis). Norsk
Hvalfangst-tidende
5: 181-189.
RIDGWAYS.H. & DAILEY M.D. 1972. Cerebral and cerebellar involvement of trematode oarasites in doluhins and their
possible role in stranding. Journal of Wildlife Diseases 8: 33-43.
SCHEFFERV.B. 1939. Organisms collected from whales in the Aleutian Islands. Murrelet 20: 67.
SCHROEDERCR. & WEDGEFORTHH.M. 193.5.The occurrence of gastric ulcers in sea mammals of the California coast,
their etiology and pathology. Journal of the American Veterinary Medical Association 40: 333-342.
SCHROEDERR.J., DELLI QUADRI C.A., MCINTYRER.W. & WALKERW.A. 1973. Marine mammal disease surveillance
program in Los Angeles county. Journal of the American Veterinary Medical Association 163: 580-581.
SCHRYVERH.F., MEDWAY W. & WILLIAMS J.F. 1967. The stomach fluke Braunina cordiformis in the Atlantic
bottlenose dolphin. Journal of the American Veterinary Medical Association 151:884-886.
SKRJABINK.I., SOBOLEVA.A. & IVASHKINV.M. 1967. Spirurata of Animals and Man and the Diseases Caused by
Them. Part 4. Thelazioidea. (Israel Progr. Scientific Translation 1971).
SWEENEY J.C. & GILMARTINW.G. 1974. Survey of diseases in free-living California sea lions. Journal of Wildlife
Diseases 10: 370-371.
SWEENEY J.C. & RIDGWAY S.H. 1975. Common disease of small cetaceans. Journal of the American Veterinary
Medical Association
167: 533-540.
TESTA J. & DAILEY M.D. 1977. Five new morphotypes of Phyllobothrium delphini (Cestoda: Tetraphyllidea), their
relationship to existing morphotypes, and their zoogeography. Bulletin of the Southern California Academy of
Sciences 76: 99-l 10.
TRUE F.W. 1891. Observations on the life history of the bottlenose porpoise. In: United States National Museum
Proceedings 13 (1890): pp 197-203.
WALKER W.A. & COWAN D.F. 1981. Air sinus parasitism and pathology in free-ranging common dolphins (Delphinus
detphis) in the eastern tropical Pacific. Administrative Report No. LJ-81-23C. National Marine Fisheries Service,
Southwest Fisheries Center, La Jolla, California, U.S.A. 19 pp.
WOOD F.G., CALDWELL D.K. & CALDWELL M.C. 1970. Behavioural interactions between porpoises and sharks. In:
Investigations on Cetacea Vol. II, pp 164-277 (Edited by Pilleri G.) Brain Anatomy Institute, University of Berne,
Berne.
WOODARD J.C., ZAM S.G., CALDWELLD.K. & CALDWELLM.C. 1969. Some parasitic disease of dolphins. Pathology
Veterinarian 6: 257-272.
YOUNG
P.C. & LOWE D. 1969. Larval nematodes from fish of the subfamily anisakinae and gastro-intestinal
mammals. Journal of Comparative Pathology 79: 301-313.
lesions in