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Baumgartner , M. F. , Mullin , K. D. , May , L. N. , and Leming , T. D. ( 2001 ). Cetacean habitats in the northern Gulf of Mexico . Fish. Bull. (U.S.) 99 , 219 – 239 .

Cramer, K., Perryman, W. L., and Gerrodette, T. (In press). Declines in reproductive indices in two depleted dolphin populations in the east-ern tropical Pacifi c. Mar. Ecol. Prog. Ser .

Dolar , M. L. L. , Perrin , W. F. , Taylor , B. L. , Kooyman , G. L. , and Alava , M. N. R. ( 2006 ). Abundance and distributional ecology of cetaceans in the central Philippines . J. Cetacean Res. Manage. 8 , 93 – 111 .

Edwards , E. F. ( 2005 ). Duration of unassisted swimming activity for spotted dolphin ( Stenella attenuata ) calves: implications for mother-calf separa-tion during tuna purse-seine sets . Fish. Bull. (U.S.) 104 , 125 – 135 .

Escorza-Trevi ñ o , S. , Archer , F. I. , Rosales , M. , Lang , A. , and Dizon , A. E. ( 2005 ). Genetic differentiation and intraspecifi c structure of east-ern tropical Pacifi c spotted dolphins, Stenella attenuata , revealed by DNA analyses . Conserv. Genet. 6 , 587 – 600 .

Gerrodette , T. , and Forcada , J. ( 2005 ). Non-recovery of two spotted and spinner dolphin populations in the eastern tropical Pacifi c Ocean . Mar. Ecol. Prog. Ser. 291 , 1 – 21 .

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Jefferson , T. A. , Webber , M. A. , and Pitman , R. L. ( 2007 ). “ Marine Mammals of the World: A Comprehensive Guide to Their Identifi cation . ” Academic Press/Elsevier , San Diego, CA .

Kasuya , T. ( 2007 ). Japanese whaling and other cetacean fi sheries . Environ. Sci. Poll. Res. (online early) , 1 – 10 .

LeDuc , R. G. , Perrin , W. F. , and Dizon , A. E. ( 1999 ). Phylogenetic rela-tionships among the delphinid cetaceans based on full cytochrome bsequences . Mar. Mamm. Sci. 15 , 619 – 648 .

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Maldini , D. ( 2003 ). Evidence of predation by a tiger shark ( Galeocerdocuvieri ) on a spotted dolphin ( Stenella attenuata ) off Oahu, Hawaii .Aquat. Mamm. 29 , 84 – 87 .

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Noren , S. R. , and Edwards , E. F. ( 2007 ). Physiological and behavioral development in delphinid calves: implications for calf separation and mortality due to tuna purse-seine sets . Mar. Mamm. Sci. 23 , 15 – 29 .

Perrin , W. F. ( 2001 ). Stenella attenuata . Mamm. Species 633 , 1 – 8 . Perrin, W. F., Donovan, G. P., and Barlow, J. (eds.). (1994). Cetaceans

and gillnets. Rep. Int. Whal. Commn . 15 (Special Issue), 629. Perrin , W. F. , and Hohn , A. A. ( 1994 ). Spotted dolphin Stenella atten-

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Perrin, W. F., Mitchell, E. D., Mead, J. G., Caldwell, D. K., Caldwell, M. C., Van Bree, P. J. H., and Dawbin, W. H. (1987). Revision of the spotted dolphins, Stenella Spp. Mar. Mamm. Sci. 3, 99–170.

Pitman , R. L. , O’Sullivan , S. , and Mase , B. ( 2003 ). Killer whales ( Orcinusorca ) attack a school of pantropical spotted dolphins ( Stenella attenu-ata ) in the Gulf of Mexico . Aquat. Mamm. 29 , 321 – 324 .

Robertson , K. M. , and Chivers , S. ( 1997 ). Prey occurrence in pantropical spotted dolphins, Stenella attenuata , from the eastern tropical Pacifi c . Fish. Bull. (U.S.) 95 , 334 – 348 .

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Parasites J. ANTONIO RAGA , MERCEDES FERNÁNDEZ , JUAN A. BALBUENA AND F. JAVIER AZNAR

Beyond their sanitary or economic importance, parasites are an integral part of the biosphere. They are so diverse and pervasive that they virtually infect every free-living organism,

potentially infl uencing, among other things, host health, behavior and population size, food web dynamics, and community structure. These effects are usually undesirable when human health or econ-omy are at stake but confer parasites a paramount importance in nature that should not be neglected.

This entry provides an overview of the diversity of marine mam-mal parasites. Its aim is to explain concisely what they are and how they have become associated with their hosts. Other aspects, such as the impact of parasites on marine mammal populations, are cov-ered only briefl y as they have been dealt with extensively elsewhere ( Aznar et al. , 2001 ). Under the term “ parasite, ” we will only consider the protozoons and metazoons (helminths and arthropods) that have adopted this life history strategy. Some representative parasites of marine mammals are shown in Fig. 1 .

I. Parasite Diversity Protozoan parasites have been reported rarely in marine mam-

mals. Most species have been described only recently thanks to an increasing interest in these organisms and the use of new techniques with fresh samples. So our knowledge of protozoan diversity in marine mammals is likely to increase substantially in the coming years (Raga and Gulland, 2008). As for metazoan parasites, differences in sampling effort are considerable depending on the host group. In particular, beaked whales (Ziphiidae) and fur seals (Otariidae) are speciose taxa for which parasite studies are still very scarce, and therefore diversity is likely to be higher than currently perceived.

Another fundamental factor affecting current diversity estimates is the existence of sibling species. This phenomenon is relatively fre-quent among marine invertebrates and has been documented exten-sively in parasitic nematodes of cetaceans and pinnipeds (family Anisakidae). Accordingly, the actual diversity of many other parasite taxa might have been underestimated because of our inability to tell species apart based on morphology. We suspect that many parasites infecting marine mammals that are currently considered as cosmo-politan or widespread may actually represent complexes of sibling or pseudosibling species.

A. Cetaceans Four types of coccidians occur in cetaceans: Cystoisospora delphini

in common bottlenose dolphins ( Tursiops truncatus ) causing enteritis; Toxoplasma gondii (or Toxoplasma spp.) in four dolphin species, asso-ciated with toxoplasmosis; Sarcocystis spp. in toothed whales, usually with little or no obvious pathologic effect — fatal hepatic sarcocystosis has been reported only in one striped dolphin ( Stenella coeruleoalba ); and Neospora caninum in bottlenose dolphins although its patho-logical effect is currently unknown ( Dailey, 2005 ). The life cycles of these coccidians have not been elucidated in the aquatic environment, although there are reports of congenital and transplacental transmis-sion of Toxoplasma spp. in dolphins. Flagellates have been rarely

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Pfound in cetaceans. Jarrellia atramenti was described in the blowhole mucus of a pygmy sperm whale ( Kogia breviceps ), but whether or not this protozoon is a parasite is still unclear. Giardia spp. is found regu-larly in feces from North Atlantic right whales ( Eubalaena glacialis ) and bowhead whales ( Balaena mysticetus ). In addition, the sarcodinan Entamoeba spp. has been recorded in the contents of the colon of the bowhead whale. Parasitic ciliates have been reported in both baleen and toothed whales. Haematophagus megapterae feeds on blood cells and attaches to the baleen plates of humpback whales ( Megaptera novaeangliae ), fi n whales ( Balaenoptera physalus ), and blue whales (B. musculus ). Kyaroikeus cetarius , Planilamina ovata , and P. magna(family Kyaroikeidae) occur in the blowhole and lungs of many species of toothed whales. These ciliates are thought to have direct life cycles, requiring perhaps repeated exposure to be successfully transmitted ( Dailey, 2005 ).

Four families of fl ukes occur typically in cetaceans: species of Brachycladiidae (formerly Campulidae) occur in whales and dolphins; species of Pholeteridae and Brauninidae occur in dolphins, and spe-cies of Notocotylidae in whales. In terms of diversity and geographic range, the family Brachycladiidae is the most important. It comprises some 41 species, 35 of which are distributed among the most families of cetaceans. Species of Campula , Oschmarinella , and Brachycladium(formerly Zalophotrema ) inhabit the hepatic and pancreatic ducts of toothed whales ; Hadwenius , the intestine; Nasitrema , the air sinuses; and Hunterotrema , the lungs. Baleen whales harbor species of Brachycladium (formerly Lecithodesmus ) in the bile ducts. The life cycles of the brachycladiids are not known, although their widespread occurrence in fi sh and squid species eaten by cetaceans suggests that these prey act as second intermediate or transport hosts. Pholeter gastrophilus (Pholeteridae) parasitizes many toothed whales (mainly

(A) (B)

(C) (D)

Figure 1 Scanning electron micrographs of some representative parasites of marine mammals. (A) Frontal view of the mouth of Anisakis physeteris, a nematode from the stomach of the sperm whale (Physeter macrocephalus). (B) Scolex of Monorygma grimal-dii, a larval cestode from the abdominal mesenteries of the striped dolphin (Stenellacoeruleoalba). (C) Dorsal view of Antarctophthirus microchir, a sucking louse from the fur of the South American sea lion (Otaria fl avescens). (D) Lateral view of Corynosomacetaceum, an acantocephalan from the stomach of the franciscana (Pontoporia blainvil-lei). Scale bars A: 50 μ m; B: 100 μ m; C and D: 500 μ m .

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delphinids) throughout the world. These fl ukes bore into the wall of the glandular part of the stomach, and the duodenum, sometimes gen-erating extensive fi brosis. Their distribution among digestive chambers seems to be driven by the diet and digestive physiology of each host species ( Aznar et al. , 2006 ). Braunina cordiformis (Brauninidae) has a peculiar ovoid morphology and attaches to the stomach and the duo-denal ampulla of small toothed whales. Several species of Ogmogaster(Notocotylidae) have been found in the large intestine of baleen whales from the Antarctic, Pacifi c, Atlantic, and Mediterranean. The life cycle is unknown, but information derived from other notocotylids suggests that the cercaria (larvae) might not need a second intermediate host, encysting directly on crustaceans that are preyed upon by whales.

Cetaceans are infected with both adult and larval tapeworms. The adult forms belong to two families, Tetrabothriidae (16 species of 23 in marine mammals) and Diphyllobothriidae (11 of 48 in marine mammals). Their body sizes range from small (a few millimeters) to very large (several meters) and they dwell in the intestine, from the duodenum (e.g., Tetrabothrius forsteri ) to the terminal colon and rec-tum (e.g., Strobilocephalus triangularis ). The Tetrabothriidae have diversifi ed morphologically in cetaceans (represented by the genera Trigonocotyle , Strobilocephalus , Priapocephalus , and Tetrabothrius ; only the latter two have representatives in baleen whales). The diphyllobothriids belong to the genera Diphyllobothrium (infect-ing toothed whales, more rarely baleen whales), Diplogonoporus(in baleen whales and the sperm whale, Physeter macrocephalus ), Hexagonoporus (in the sperm whale), and Plicobothrium (typical from pilot whales, Globicephala spp., rarely in other dolphins). In general, tapeworms of marine homeotherms use zooplanktonic crus-taceans as fi rst intermediate hosts. In some tetrabothriids, euphasiids (the krill) act as intermediate hosts and fi sh as transport hosts. In con-trast, the known cycles of members of the Diphyllobothriidae involve copepods and fi sh as intermediate hosts. Cetaceans and some pinni-peds also harbor larvae (plerocercoids and merocercoids) of the fam-ily Phyllobothriidae worldwide. Recent studies have revealed two types of plerocercoid (termed as “ small ” and “ large ” ) in the digestive tract. Likewise two types of merocercoid, classically designated as Phyllobothrium delphini and Monorygma grimaldii , occur in the blub-ber and mesenteries, respectively. A detailed study of these larvae in cetaceans from the Mediterranean, based on morphological, molecu-lar, and ecological data, suggests that “ large ” plerocercoids, P. delphiniand M. grimaldii represent different species, whereas the “ small ” ple-rocercoid is a previous stage of M. grimaldii . The adult stage of these tapeworms is not known but all these larvae are closely related to phyl-lobothriids infecting large sharks that feed on cetaceans. Apparently, cetaceans are intermediate hosts of these tapeworms, raising interest-ing questions about the evolution of the life cycles of tetraphyllideans ( Aznar et al. , 2007 ).

Among the nematodes, the family Anisakidae is probably the most successful in terms of potential for colonizing hosts in many environ-ments. Different studies have revealed the existence of several com-plexes of sibling species. The anisakids occurring in cetaceans belong to the genera Pseudoterranova , Contracaecum and Anisakis , although only species of the latter are found mainly in cetaceans, hence their vernacular name of “ whaleworm. ” Eight species of Anisakis have been reported in at least 35 species of marine cetaceans. Whaleworms occur in the stomach, mainly in the forestomach. The larvae can attach to the stomach walls in aggregates and provoke ulcers. The life cycle is well documented. The eggs, shed in the feces, hatch and release the free-living larvae that are subsequently ingested by planktonic crusta-ceans. Apparently, the parasite is then ready to infect cetaceans (e.g., mysticetes). However, the larvae are usually transmitted to fi sh and

squid feeding on infected crustaceans, and most cetaceans become eventually infected by consuming these pray. The worms molt to the adult stage and mate in the stomach of cetaceans, where the cycle is closed when the female nematodes release the fertilized eggs ( Dailey, 2005 ). The large histozoic nematodes of Crassicaudidae (about 11 spe-cies exclusive of cetaceans) occur in the kidneys and urogenital organs, placenta, mammary glands, muscles, and pterygoid sinuses, some-times causing extensive damage. Species of Crassicauda infect both whales and dolphins, whereas the up to 9-m-long Placentonema gigan-tissima dwells in the placenta of sperm whales (Geraci and St. Aubin, 1987). Life cycles are largely unknown. It has been speculated that C. boopis might infect fi n whale calves either by ingestion of larvae shed in their mothers ’ urine or by transplacental transmission ( Dailey, 2005 ). Pseudaliids (about 17 species exclusive to toothed whales) are distributed among the genera Pseudostenurus , Pharurus , Torynurus , Stenurus , Halocercus , Pseudalius , and Skrjabinalius . They occur mainly in the lungs, air sinuses, and heart of phocoenids and mono-dontids, secondarily delphinids. Prenatal transmission of Halocercus in common bottlenose dolphins has been suggested. However, indirect transmission through the food web is probably the main route of infec-tion for most species ( Dailey, 2005 ).

Only species from two genera of acanthocephalans (family Polymorphidae) reproduce in the intestine and occasionally in the stomach of marine mammals. These worms are closely allied to forms infecting aquatic birds. Whales and dolphins are the typical hosts for Bolbosoma (some nine species). Pelagic euphasiids and copepods are thought to act as intermediate hosts, and fi sh as transport hosts (Raga and Gulland, in press). A few members of Corynosoma have speci-ated in cetaceans, but the bulk of diversity in this genus is found in pinnipeds (see later).

Cetaceans harbor a specifi c and rather diverse fauna of parasitic and nonparasitic crustaceans; interestingly, such associations are rare in sirenians, and do not occur on pinnipeds. Whale lice (Cyamidae, about 26 species) have diversifi ed extensively among dolphins and whales, becoming one of the few groups of parasitic amphipods. Whale lice attach to the skin (especially on natural openings, wounds, and scars), feeding mostly on epidermal tissue. The life cycle takes place completely on the hosts and transmission is by bodily contact ( Raga, 1997 ). Copepods of the genus Pennella (family Pennellidae) are primarily parasites of fi sh. However, about six species have successfully colonized cetaceans. Their life cycle is complex: after two free-swim-ming stages, they develop, mate, and attain sexual maturity on squid and then females seek a suitable defi nitive host, e.g., cetaceans, where they burrow on the host’s body (mainly on the back and belly) to get their head anchored, and subsequently feed on blood and body fl uids.

B. Sirenians Four species of Coccidia have been reported in sirenians: Eimeria

manatus , E. nodulosa , and T. gondii in the West Indian manatee (Trichechus manatus ) and E. trichechi in the Amazonian manatee (T. inunguis ). The species of Eimeria have been detected as oocysts in feces. Nothing is known about their life cycles, but the oocyst of E. nodulosa bears peculiar nodules that are thought to serve for attachment to aquatic vegetation. Thus the cycle might be direct (Raga and Gulland, in press).

The fauna of metazoan parasites in manatees and dugongs is restricted to digeneans and nematodes, but it is fairly diversi-fi ed relative to the number of extant host species, and very specifi c. Except Nudacotyle undicola , which belongs to a genus typical from land mammals, all species and genera recorded so far (3 species

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of nematodes belonging to 2 genera; 22 species of digeneans in 16 genera) are exclusive to sirenians (three out of six families also are). Interestingly, the dugong ( Dugong dugon ) exhibits a distinct and richer helminth fauna than the manatees (17 vs 7 species). This difference might simply result from corresponding differences in research effort. However, dugongs inhabit the Tropical Pacifi c, whose richer marine fauna may offer a larger selection of intermediate hosts and, perhaps more importantly, dugongs have remained longer in the marine habitat of ancestral sirenians. In contrast, the manatees moved and adapted to freshwater habitats, which probably resulted in the loss of some ances-tral marine parasites ( Beck and Forrester, 1988 ; Dailey, 2001 ).

The parasites of sirenians occur in a variety of sites within the host. The roundworms Paradujardinia halicoris and Heterocheilusspp. inhabit the stomach, more rarely the small intestine. Flukes exhibit a notable morphological diversity, e.g., Taprobanella bicau-data , and are found in diverse locations. Species of Paramphistomidae (4), Rhabdiopoeidae (4), and Nudacotylidae (1) and most of the Opisthotrematidae (6) occur in different sites in the digestive system, including the stomach, pyloric ceca, duodenum, ileum, colon, pan-creas, and liver. In some cases they form cysts, e.g., Faredifex clavata(Rhabdiopoeidae) or Lankatrema mannarense (Opisthotrematidae). In contrast, species of Opisthotrema (2), Cochleotrema (2), and Pulmonicola (1) dwell in the ear system or the lungs, whereas Labicola elongata (Labicolidae) occurs in the upper lip of dugongs ( Lauckner, 1985a ; Dailey, 2001 ). The life cycles have not been determined for any of these parasites. Some authors have suggested that the nema-todes of sirenians use crustaceans as intermediate hosts that would be consumed incidentally while feeding on vegetation. Other pro-pose that the eggs might be ingested directly when the hosts feed on contaminated vegetation. Similar conjectures have been advanced for digeneans. Chiorchis fabaceus is thought to infect manatees through the incidental ingestion of snails containing metacercariae (larvae), whereas the cercariae of Lankatrematoides gardneri use a mollusk as an intermediate host, and perhaps then the larvae escape and encyst on aquatic vegetation, where they wait to infect dugongs ( Beck and Forrester, 1988 ).

C. Pinnipeds The most common protozoons found in pinnipeds are coccid-

ians. Species of Eimeria have been detected in the intestine of seals, sometimes causing severe disorders. Eimeria phocae is typical from harbor seals ( Phoca vitulina ) in the northwestern Atlantic. Although its life cycle is still unclear, experimental evidence shows that oocysts sporulate in feces if incubated in air but not if suspended in seawa-ter, suggesting that transmission occurs on land. Another six spe-cies of Eimeria occur in Weddell seals ( Leptonychotes weddelli ) and crabeater seals ( Lobodon carcinophagus ). Species of Sarcocystishave been reported in harbor seals in California, northern fur seals (Callorhinus ursinus ) in Alaska, Hawaiian monk seals ( Monachus schauinslandi ), and leopard seals ( Hydrurga leptonyx ) in Antarctica. Isospora miroungae and Cystoisospora israeli have been described in young Antarctic southern elephant seals ( Mirounga leonina ) and South African fur seals ( Arctocephalus pusillus ), respectively. Toxoplasmosis due to T. gondii has been observed in harbor seals, California sea lions ( Zalophus californianus ), ringed seals ( Pusa hispida ), spotted seals ( Phoca largha ), and walruses ( Odobenus rosmarus ) (Raga and Gulland, in press). Experimental infections in gray seals ( Halichoerus grypus ) have demonstrated that oocysts of this parasite can establish viable infection in seals, and that oocysts are probably acquired in sur-face water runoffs and sewer discharges (see also below). Likewise,

harbor seals, ringed seals, spotted seals, and walruses have been found to be seropositive to N. caninum ( Dubey et al ., 2003 ). In addition to coccidians, fl agellates of Giardia spp. have been detected in feces from ringed seals, harp seals ( Pagophilus groenlandicus ), gray seals, and a harbor seal from the arctic, subarctic, and eastern coasts of Canada, and in California sea lions in northern California. It has been suggested that seals and sea lions could serve as reservoirs for Giardiaspp. but little is known about the transmission of this parasite in the sea ( Dailey, 2005 ).

Flukes are represented by eight families. Within the Brachycladiidae (formerly Campulidae) four species of the genus Orthosplanchnus infect arctic and subarctic phocids, and walruses, whereas O. antarcticus occurs in Antarctic seals. Zalophotrema hepaticum is associated with California sea lions in the northeastern Pacifi c. Brachyclaidiids of pinnipeds live in the bile ducts, gall bladder, and rarely, the intestine. The family Heterophyidae is widespread in pinnipeds, particularly in the Northern Hemisphere. About 12 intes-tinal species have been recorded so far, belonging to Cryptocotyle , Phagicola , Rossicotrema , Galactosomum , Mesostphanus, Heterophy-opsis, Pricetrema , and Phocitrema. Species of the two latter genera are associated more specifi cally with pinnipeds (in the Pacifi c region). Nothing is known of the life cycles of these heterophyids. Inferences made from other species strongly suggest that a gastropod would function as fi rst and various species of fi sh as second intermedi-ate hosts. Five species of opistorchiids from the genera Opistorchis , Metorchis , and Pseudamphistomum inhabit the bile ducts of seals from the Northern Hemisphere. Their life cycles are unknown, but, from other opistorchiids, it might be inferred that fi sh act as second intermediate hosts. Microphallids (three species) from the genera Microphallus and Maritrema are intestinal fl ukes. Microphallus orien-talis has been reported in immense numbers in walruses and bearded seals ( Erignathus barbatus ) from the Barents Sea. The majority of microphallid larvae encyst in benthic crustaceans, which may explain their occurrence in seals that feed on bottom invertebrates. Finally, Ogmogaster antarcticus (Notocotylidae) is known from Weddell and crabeater seals ( Lauckner, 1985b ). These hosts likely become infected when feeding on benthic invertebrates (see earlier discussion).

The tapeworm fauna of pinnipeds is rich. The majority of species belong to the family Diphyllobothriidae (37 species out of 48 in marine mammals). Of these species, those of Diphyllobothrium form the major component, being distributed in pinnipeds worldwide ( Lauckner, 1985b ). In contrast, species of Baylisia , Baylisiella , and Glandicephalusare exclusive to Antarctic seals, and those of Diplogonoporus to boreal pinnipeds. Insights of the life cycles of diphyllobothriids have already been discussed above. One genus of Tetrabothriidae, Anophryocephalus (seven species) is associated with arctic and subarc-tic pinnipeds. Euphasiids and fi sh appear to be intermediate and trans-port hosts, respectively, in the life cycle ( Lauckner, 1985b ).

Pinnipeds harbor a diverse nematode fauna that comprises six families: Ancylostomatidae (2 species), Dipetalonematidae (2), Trichinellidae (1 – 2), Filaroididae (4), Crenosomatidae (1), and Anisakidae (14). To a great extent, this parasite fauna is related to taxa found in land carnivores. Thus, the cycle of some groups is land-dependent and resembles that of their terrestrial counterparts. For instance, the eggs and the fi rst three larval stages of Uncinaria spp. (Ancylostomatidae) develop on the soil of otariid rookeries. Third-stage larvae infect adult hosts by boring the skin (especially in the fl ippers) and migrate to host tissues, particularly the ventral blub-ber and mammary glands. Larvae use the milk of adult female seals to infect the pups, where worms become adults in the intestine. Transmission occurs only during the breeding period; infective

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larvae overwinter on the rookery until the arrival of the hosts (Raga and Gulland, in press). The heartworm, Acanthocheilonema (�Dipetalonema) spirocauda (Dipetalonematidae), likely requires an arthropod vector (a louse) to trigger development and to transmit the microfi laria to North Atlantic seals, although this mode of transmis-sion has yet to be proven. Transplacental or transmammary transmis-sion to pups has been also suggested to occur. Species of Trichinella(Trichinellidae) are typical tissue parasites of terrestrial mammals. However, as discussed in the next section, a natural cycle of trichinosis involving pinnipeds seems to exist in the Arctic (Raga and Gulland, in press). With regard to nematodes with aquatic cycles, experiments have demonstrated that the lungworm Parafi laroides decorus (Filaroididae) infects fi sh that consume excrements of Californian sea lions contami-nated with the larvae. These fi sh are, in turn, preyed upon by the sea lions. Recent experimental studies of the lungworm Otostrongylus circumlitus (Crenosomatidae), a species infecting boreal seals, have shown that fi sh seem to act as intermediate hosts ( Dailey, 2005 ). By far the most widespread nematode group in seals is the Anisakidae, dwelling in the stomach and duodenum. Pinnipeds are primary hosts for species of Pseudoterranova and Phocascaris , whereas species of Contracaecum appear primarily in aquatic birds, although some spe-cies occur in phocids and otariids. In addition, Anisakis simplex may occasionally mature in some phocids, particularly in the gray seal. The life cycle of the sealworm, Pseudoterranova decipiens , is the best known. Experiments have shown that the sealworm can infect a wide variety of invertebrates. Under natural conditions, however, it utilizes only benthic and epibenthic organisms as intermediate and transport hosts. The free-living larva emerging from the egg has negative buoy-ancy and adheres to the substrate by its tail. This behavior favors inges-tion by benthic copepods, which, in turn, are consumed by benthic macroinvertebrates. At this point, the larvae have molted twice and are ready to infect seals, but benthophagous fi sh, or their demersal preda-tors, can be used as transport hosts, enhancing transmission ( Aznar et al. , 2001 ).

Acanthocephalans of the genus Corynosoma (Polymorphidae, some 20 species in pinnipeds) exhibit a protracted history of associa-tion with pinnipeds. They have a cosmopolitan distribution, appear-ing in the intestine of most species of seals and sea lions, and the walrus. The complete life cycle for C. strumosum and C. pseudoha-manni has been inferred from fi eld collections. Nearshore amphi-pods acquire the cystacanth larvae, which, following ingestion, encyst in the body cavity of several fi sh species and await seals to prey on these fi sh. Species of Bolbosoma have also been reported inciden-tally in Arctic seals ( Lauckner, 1985b ).

Two main arthropod groups are associated with pinnipeds: suck-ing lice (Echinophthiriidae) and mites (Halarachnidae). The entire life cycle of sucking lice is spent on the seals and, therefore, they rely on bodily contact for transmission. Echinophthiriids (four genera, nine species) are associated with all major pinniped groups (otariids, odo-benids, phocids) worldwide. They are physiologically adapted to the particular hosts ’ amphibious conditions and are transmitted on land ( Lauckner, 1985b ). Mites (six species) inhabit the respiratory tract and belong to two genera: Halarachne (in phocids) and Orthohalarachne(in otariids and odobenids). The life cycle takes place in the same indi-vidual host and comprises four stages: a larva, two nymphal stages, and the adult. Transmission occurs on land when active larvae are trans-ferred by nose contact or are sneezed from the nostrils of infested ani-mals. Acari also have some representatives in pinnipeds. Dermacentor rosmari (Ixodidae) appears between the fi ngers of walruses, especially in the hind legs, in the Arctic waters of Russia; nymphal stages are not known. Demodex zalophi (Demodicidae) occurs in the hair follicles

of the fl ippers and genital region of California sea lions. Each follicle usually contains one female and four males. All stages of development take place in the hair follicle, usually in the distal portion of the duct of the sebaceous gland ( Lauckner, 1985b ).

D. Sea Otter Three protozoan species have been reported in the sea otter

(Enhydra lutris ): T. gondii , N. caninum , and Sarcocystis neurona . These species are terrestrial and thus their occurrence in the sea otter and other marine mammals (see above) is intriguing. Recent studies reveal that between 40 and 70% of sea otters analyzed in the North American Pacifi c coast are seropositive to T. gondii . Apparently, oocysts in cat feces are washed into the sea through freshwater runoff. It is assumed that otters are infected either by feeding on fi lter-feeding invertebrates that retain the oocysts or by direct ingestion in sea water (see above). Interestingly, the most common strain of T. gondii infect-ing sea otters, and some pinnipeds, has not been described in terres-trial hosts. Concerning S. neurona , experimental studies have shown that sea otters can support the development of mature sporocysts that are infectious to competent defi nitive hosts ( Miller et al. , 2002 ; Dubey et al. , 2003 ; Kreuder et al ., 2003 ).

Some 20 metazoan parasite species have been reported from sea otters throughout their range. Most are acquired directly from sympat-ric pinnipeds, for instance, Orthosplanchnus fraterculus , Pricetrema zalophi , Phocitrema fusiforme , Diplogonoporus sp., Diphyllobothrium phocarum , Pseudoterranova decipiens , P. azarasi , Corynosoma stru-mosum , C. villosum , and Halarachne miroungae or from cetaceans (Anisakis sp. larvae). Other parasites appear to derive from seabirds, such as the microphallid digeneans Microphallus pirum , M. nicolli , and Plenosoma minimum , and three acanthocephalan species of Profi licollis (Polymorphidae) occurring as immature. Apparently, the only parasite specifi c to the sea otter is Corynosoma enhydri , the largest species in this genus ( Lauckner, 1985c ; Margolis et al ., 1997 ; Mayer et al ., 2003 ).

E. Polar Bear Polar bears ( Ursus maritimus ) have been relatively little analyzed

for parasites. In wild animals, Trichinella spp. (Trichinellidae) rep-resent the most frequent records. Three cestode species, D. latum , Bothriocephalus sp., and Taenia ursi-maritimus have also been reported ( Dailey, 2001 ).

II. Patterns and Processes in Host–Parasite Associations

To understand how marine mammals and their parasites have become associated, we have to fi rst discuss the principles that regu-late the outcomes of host – parasite interactions. The evolutionary fate of every parasite species depends on that of its hosts. If parasites are able to track their hosts ’ evolution, host and parasite phylogenies will match exactly, resulting in a perfect cospeciation pattern. However, if parasites speciate or go extinct whereas their hosts do not, or if hosts speciate but parasites do not, incongruences between both phyloge-nies will occur. Another fundamental reason for incongruence is host switching (also called “ host capture ” ), i.e., parasites colonize new hosts through ecological mechanisms. Host switching deserves more detailed comments because of its importance for the development of parasite faunas in marine mammals ( Fig. 2 ) ( Aznar et al ., 2001 ).

In order to successfully colonize a new host, the parasite has to encounter the host and be compatible with it. Encounters depend

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on behavioral, ecological, or biogeographical factors. For instance, the transmission of digeneans of sirenians appears to be linked to either sea vegetation or the organisms associated to it. Therefore, the chances of transmission to fi sh-eating marine mammals will be small indeed. If contact occurs, the new host can be “ right ” or “ wrong ” depending on compatibility, i.e., those morphological, physiological, or immunological factors that either allow or preclude that a given para-site becomes established, matures, or reproduces in/on the newly con-tacted host. Since most parasites of marine mammals use food webs for transmission, they cannot exert strong selection on host compati-bility, thus ending in both “ right ” and “ wrong ” hosts. For instance, spe-cies of Corynosoma are mainly associated with pinnipeds worldwide, but their larvae frequently end up in sympatric seabirds or cetaceans. However, for unknown physiological and/or immunological reasons, these larvae rarely mature in these nonpinniped hosts.

When encounters with “ wrong ” hosts are fortuitous, their ecological and evolutionary signifi cance is minimal. For example, sea otters from California seldom acquire larvae of Polymorphus spp. from aquatic birds. However, if encounters repeat predictably throughout time, true accommodation or speciation of parasites in initially “ wrong ” hosts can be promoted, providing that parasites are eventually able to over-come the compatibility fi lter. This is obviously easier as the target host is phylogenetically closer to the original host. However, the probability of encounter is always of paramount importance. This explains why, for instance, carnivorous marine mammals have more parasitic taxa in com-mon with fi sh-eating seabirds than with sirenians ( Fig. 2 ).

A typical case of accommodation is that of the ecological fac-ultative hosts, i.e., suitable hosts for a parasite species that origi-nated elsewhere ( Hoberg and Adams, 2000 ). For example, the tapeworm Anophryocephalus ochotensis originated in the Steller sea lion (Eumetopias jubatus ) due to colonization of seals by Anophryocephalusspp. However, A. ochotensis also infects and reproduces now in sympat-ric northern fur seals ( Hoberg, 1995 ). Facultative hosts are particularly important when they sustain a signifi cant portion of a parasite population.

A. General Hypothesis on the Origin of Associations

Based on the above concepts, we can elaborate a general hypoth-esis on the origin of host – parasite associations. Let us consider the ter-restrial ancestors of each marine mammal group (cetaceans, sirenians, pinnipeds, the sea otter, and the polar bear). These ancestors certainly harbored parasites in a variable number, but the subsequent host tran-sitions from land to sea likely posed a barrier for these terrestrial par-asites to track their hosts. In other words, parasites were compelled to either precisely adjust their life cycle and/or physiology to the new environment or face extinction. There are beautiful examples of such biological adjustment (e.g., the life cycle of U. lucasi explained above), but many parasite extinctions should have occurred, particularly in the two marine mammal groups (cetaceans and sirenians) that eventually severed their ties with land ( Aznar et al ., 2001 ; see also Hoberg and Adams, 2000 ; Hoberg and Klassen, 2002 ).

PholeterTetrabothrius

Pennella Ogmogaster

Nudacotyle

PricetremaPhocitremaMicrophallusPseudoterranova

UncinariaDipetalonemaCapillaria

SarcoptesDemodexDermacentor

Trichinella

Anisakis

Profilicollis

Contracaecum

OrthosplanchnusDiplogonoporus

Corynosoma

Diphyllobothrium

Taenia

CryptocotyleGalactosomumHeterophyopsisMaritremaMesorchis

MesostephanusMicrophallusPhagicolaRossicotrema

Figure 2 Genera of parasitic helminths and arthropods that are shared between marine mammals and between marine mammals and other hosts, i.e., terrestrial mammals (represented by a fox) and seabirds (represented by a gull). Complex patterns of putative colonization involving terrestrial mammals, pinnipeds, fi sh-eating seabirds, and the sea otter occur in the coastal realm. Pinnipeds also share arthropods and nematodes of terrestrial origin with other mammals. Cetaceans share a smaller number of genera apparently because of the lack of coevolutionary elements of terrestrial origin and their pelagic habits, which would hamper colonization events. Sirenians are isolated from other marine mammals because of their herbivorous diet. Fish are phylogenetically too apart for most parasite exchanges between them and mammals to be successful (see the text for details) .

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When the ancestors of sea mammals made it to the sea, they became literally immersed in an ocean of infective stages of marine parasites. Then the mechanisms favoring host switching began to work. Some host captures involved marine mammals and parasites from nonmammalian hosts. However, due to compatibility limita-tions, these episodes should have been rare as compared to the para-site exchange between marine mammals themselves. An example can illustrate the intricacies of colonization events. The Brachycladiidae, a family of digeneans occurring in marine mammals worldwide, are the putative sister group of fl ukes using fi sh as defi nitive hosts. Apparently, the brachycladiid ancestors amplifi ed a cycle that for-merly ended up in these fi sh by adding a new step where fi sh preda-tors (some unknown ancestor of toothed whales) became the new defi nitive hosts. This initial host switch opened the possibility for brachycladiids of subsequent coevolution (host tracking) of toothed whales and, of course, of new host-switching events. Not surpris-ingly, the latter involved other marine mammals. Baleen whales and pinnipeds apparently acquired brachycladiids from toothed whales, and sea otters from pinnipeds ( Aznar et al ., 2001 ).

It is therefore likely that most parasite taxa infecting cetaceans have a marine origin, whereas coevolved products from land have remained in hosts with a permanent or close contact with this realm. The evidence available indicates that the arthropods and intesti-nal helminths of cetaceans probably rose from marine ancestors, whereas a sizeable part of parasites of pinnipeds has a clear terres-trial affi liation. To test this prediction thoroughly, we need robust phylogenetic hypotheses dealing with all parasite taxa.

B. Parasite Exchange in Ecological Scenarios We have learned from the above discussion that the distribution

of parasites in marine mammals can be largely understood from pat-terns of exchange, either past or present day, within communities of marine vertebrates. This section analyzes with more detail some major features of these patterns within each specifi c ecosystem.

1. Terrestrial Ecosystem According to the previous discussion, we would expect that most monoxenous parasites disappeared when the terrestrial ancestors of cetaceans entered the aquatic environ-ment. Whale lice, coming from free-living amphipods, are among the few aquatic forms that rely exclusively on direct transmission. However, some parasites of pinnipeds, sea otters, and polar bears, derived putatively from terrestrial counterparts, have cycles con-strained to develop on land ( Aznar et al ., 2001 ). Most of these land parasites have monoxenous life cycles and many are host specifi c. For instance, echinophthiriid lice and halarachnid mites likely coevolved with the ancestor(s) of pinnipeds and are largely restricted to these hosts today. In this context, the occurrence of Halarachne miroun-gae in sea otters should be regarded as fortuitous. Another interest-ing example is that of Trichinella spp. These extremely generalist parasites occur worldwide in terrestrial carnivores and other mam-mals. Bearded and ringed seals, walruses, and polar bears are known to serve as hosts of these nematodes in the Arctic. The infections can evi-dently be traced to a terrestrial origin, but patterns of transmission are intricate and have not been proven defi nitively. Crustaceans and birds have been suggested to acquire Trichinella spp. larvae when feeding on mammal carcasses. Then, seals would be infected by direct ingestion of these crustaceans or while feeding on grounds contaminated with bird feces ( Lauckner, 1985b ). The nematode might then be transmit-ted to polar bears and some walruses that feed on seals. Polar bears could also acquire Trichinella independently by consuming carrion of other mammals. Perhaps, no other example of terrestrial infections in

marine mammals is as intriguing as that of coccidians. For T. gondii , runoff water contaminated with cat excrements has been proposed as the most likely route of transmission, given that felids are the only known hosts that can excrete environmentally resistant oocysts and in high numbers ( Miller et al ., 2002 ; Dubey et al ., 2003 ). By contrast, the routes of infection of N. caninum and Sarcocystis spp. in the marine realm are still largely unknown ( Dubey et al ., 2003 ).

2. Freshwater Ecosystems River dolphins, Baikal seals ( Pusa sibirica ), and manatees ( Trichechus spp.) have a comparatively poor and specifi c helminth fauna. Since these hosts have secondarily colo-nized freshwater habitats, an interesting question is what kind of par-asite fauna they are expected to harbor. Parasites may have followed these hosts from the marine realm or may have colonized them in freshwater habitats. The species of Hunterotrema and Peritrachelius(�Anisakis ) insignis infecting the Amazonian river dolphin ( Inia geof-frensis ) seem to exemplify ancestral associations of marine origin. In contrast, many other parasites should have been acquired after freshwater colonization. For instance, the congeners of the fl uke Nudacotyle undicola from West Indian manatees infect freshwa-ter and terrestrial mammals. Likewise, Baikal seals are infected with Diphyllobothrium dendriticum , a typical freshwater tapeworm occur-ring in aquatic birds and land mammals. Ruffetrema indirae in the Indian river dolphin ( Platanista gangetica ) provides another example, given that relatives of this fl uke infect terrestrial birds and mammals. In this instance, however, infections seem accidental because worms are apparently unable to produce viable eggs, although it might well represent a case of incipient colonization of a new host.

Some other parasites have an uncertain origin. The digenean Chiorchis fabaceus and nematodes of the genus Heterocheilus are common to species of manatees from both freshwater and coastal habitats, but the origin of these associations is currently unknown. Likewise, the nematode Contracaecum lobulatum is exclusive to Indian river dolphins, and species of Contracaecum are typical of fi sh-eating aquatic birds, pinnipeds, and cetaceans. Where might C.lobulatum have come from, a marine or a freshwater habitat?

3. Coastal Ecosystems Coasts constitute probably the most important realm in terms of historical and current parasite exchange between carnivorous marine mammals, and between these hosts and other vertebrates ( Hoberg and Adams, 2000 ; Hoberg and Klassen, 2002 ). Perhaps the best example of rich parasite exchange in coastal waters is provided by the parasite fauna of sea otters, which is almost entirely made up of parasites from either sympatric pinnipeds or sea-birds ( Margolis et al ., 1997 ). The infl ux of parasites through coastal food webs puts many parasites in contact with incidental hosts, in which, depending on the compatibility fi lter, parasites are able or not to reproduce at ecological time. Examples of apparent failure are, e.g., P. decipiens in sea otters, A. simplex in many seals, or most Corynosoma spp. in nonpinniped hosts. In contrast, some parasites are notoriously unspecifi c with respect to the choice of their fi nal hosts: heterophyid, opistorchiid, and microphallid digeneans found typically in terrestrial mammals or aquatic birds infect and repro-duce in pinnipeds and the sea otter (rarely coastal cetaceans) in ner-itic and littoral waters ( Lauckner, 1985b ). Most of these records are occasional, but in the Caspian seal ( Pusa caspica ) they represent an important portion of the helminth fauna: many species occur also in sympatric aquatic birds or terrestrial carnivores.

There are also many examples of recent accommodation or specia-tion of parasites in new hosts (although, in most cases, we are not certain of which were the donor and the target hosts). For instance, the brach-ycladiid Orthosplanchnus fraterculus infects and reproduces readily in

Parasites828

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walruses, bearded seals, and sea otters, which share a similar diet on ben-thic invertebrates (sea otters probably acquired this fl uke from pinnipeds) ( Margolis et al ., 1997 ). Likewise, diet similarity seems to be responsible for the occurrence of Ogmogaster antarcticus in fi n whales, blue whales, Weddell seals, and crabeater seals in Antarctic waters. There are also many examples of apparent parasite speciation associated with recent colonization in the coastal environment. Species of Corynosoma in ceta-ceans (e.g., C. cetaceum in dolphins from the Southern Hemisphere), otters ( C. enhydri in sea otters), and seabirds ( C. shackletoni in the Gentoo penguin, Pygoscelis papua ) appear to constitute independent host-switching events from Corynosoma of pinnipeds.

Finally, some cases represent more archaic colonization events followed by secondary diversifi cation within the new association. It is postulated that the genera Anophryocephalus (Tetrabothriidae) and Orthosplanchnus (Brachycladiidae), typical from pinnipeds of the arctic and subarctic waters, arose during the Quaternary from ances-tors infecting toothed whales ( Hoberg and Adams, 2000 ; Aznar et al ., 2001 ). After the initial host capture, a complex history of parasite diversifi cation apparently occurred associated to pinnipeds themselves. One of the most striking examples is that of Contracaecum spp. in pin-nipeds: there is phylogenetic evidence that boreal seals and austral ota-riids acquired species of Contracaecum from seabirds independently.

4. Pelagic Ecosystems Despite the appearance of continuity between coastal and oceanic domains, the parasitic fauna of pelagic marine mammals is distinctive and comparatively poorer than that of coastal hosts. Several factors appear to contribute to this singularity. First, some parasitic groups are underrepresented. The diversity of dige-neans is probably constrained because they almost exclusively require gastropods or bivalves as fi rst intermediate hosts, which are abundant in coastal but not in pelagic waters. Indeed the Brachycladiidae are among the few fl ukes with representatives in pelagic marine mammals. Second, the probability of parasite exchange is decreased (e.g., there is little chance for terrestrial infl uence). Third, infective stages are much more “ diluted ” in the pelagic environment ( Hoberg and Adams, 2000 ;Hoberg and Klassen, 2002) . Transmission rates are thus lowered, also reducing the likelihood of host captures.

Some parasitic groups infecting marine mammals are predomi-nantly pelagic and probably originated in this ecosystem. Except for species of the genus Anophryocephalus , most tetrabothriid cestodes occur in pelagic birds and cetaceans ( Hoberg, 1995 ). Seabirds have been considered as initial hosts for ancestral tetrabothriids, from which these tapeworms would have switched to cetaceans (sea-birds, dolphins, and whales share the genus Tetrabothrius ). There are two other interesting cases of host switching. First, pelagic ceta-ceans seem to have acquired species of Pennella from oceanic fi sh. Even, there are records of the same species, P. crassicornis , parasi-tizing both cetaceans and fi shes. However, females of Pennella can actively select their defi nitive hosts, in contrast to the majority of examples discussed thus far. How did this host switch to cetaceans happen? Second, some species of Phyllobothrium and Monorygma(Cestoda) appear to use cetaceans (mostly pelagic) as intermediate hosts ( Aznar et al ., 2007 ). Evidently, a shift in the ancestral life cycle of these tapeworms had to occur as other relatives within the class Tetraphyllidea use only invertebrates and fi sh.

III. Effects and Applications A. Parasitosis

The severity of the parasite-induced damage is related to the type of parasite, its abundance, the host’s health status, and the

concurrence of other pathogenic agents. The effects of parasites usu-ally have little relevance on host health, such as local reactions pro-duced by, for instance, the proboscis of Bolbosoma or Corynosoma.Sometimes, the lesions can be more important, such as ulcers and hemorrhages caused by species of Anisakis and Pseudoterranova , and on occasion, parasites can compromise the health of its host and even lead to its death. For instance, Nasitrema spp. can cause neuropathies that have been related to both single and mass strand-ings. Likewise, lungworms of cetaceans and pinnipeds cause bron-chitis and pneumonia that may result in death, particularly among the youngest individuals. Sometimes, the direct action of the para-site might not be severe, but propitiates more serious viral, bacterial, and other parasite infections, e.g., sucking lice may transmit heart-worms while feeding on their hosts ( Dailey, 2005 ; Raga and Gulland, in press).

Sometimes, parasites represent a major cause of mortality in marine mammal populations. For instance, encephalitis by T. gon-dii and intestinal perforation caused by Profi licollis spp. accounts for about 38% of the total mortality of southern sea otters off California ( Kreuder et al ., 2003 ). Indeed, parasites might contribute signifi -cantly to marine mammal population dynamics by affecting either host reproduction or survival. For instance, many females in a herd of Atlantic white-sided dolphins ( Lagenorhynchus acutus ) suffered from mastitis caused by Crassicauda nematodes. The parasites dam-aged the secretory tissue, affecting the quality and quantity of the milk, which would ultimately compromise the survival of the calves and the reproductive output of the herd (Geraci and St. Aubin, 1987). In other instances, parasites can lead to direct mortality. Crassicauda spp. causes cranial damage in pantropical spotted dol-phins ( Stenella attenuata ) from the eastern Tropical Pacifi c. A study of dolphins caught in a tuna purse-seine fi shery showed an increase of lesions among individuals up to 5 years old. In contrast, in animals older than 8 years, lesions diminished by 12.3% annually. Assuming that the lesions were irreversible, that there were no reinfections, and that dolphins with lesions had the same probability of being caught as those without, the mortality rate attributable to the para-site was estimated as 1.1%. Since the annual natural mortality rate for the Pacifi c spotted dolphin population is 10 – 13%, the study sug-gests that Crassicauda spp. accounts for 11 – 14% of that rate.

In some cases, parasites might actually regulate marine mammal populations. A density-dependent relationship between parasite-induced mortality and population size has been shown for the hook-worm U. lucasi in northern fur seals from the North Pacifi c. These nematodes constitute the most important mortality factor among newborns by causing diarrhea, anemia, and intense intestinal hemor-rhages. The population size of pups born in St. Paul Island (Alaska) peaked around 1940 and declined more or less steadily until the present. Data of hookworm mortality from previous surveys showed a decrease in pup numbers, which means that recent mortality is less than in the past. These data suggest a density-dependent relation-ship and, therefore, a possible regulatory effect.

B. Economic and Public Health Importance The parasites of marine mammals can infect valuable animals in

aquaria, causing lesions and diseases. For this reason, expensive pro-phylactic measures must be used routinely. The most important eco-nomic impact, however, is due to anisakid nematodes whose larvae occur in commercial fi sh and squid. These larvae also have public health repercussions (see Box 1) but, from an economic perspective, the problem is cosmetic, rendering the fi sh unappealing to consumers.

Parasites 829

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to features of the host and the ecosystem. Despite some limitations, marine mammal parasites have proven themselves as biological indica-tors of phylogeny, local migration, distribution, disease, stock identity, and social behavior of their hosts.

Regarding host behavior, differences in the occurrence of two whale lice (Cyamidae) species on sperm whales were interpreted as evidence of spatial segregation between the bulls and the rest of the population off South Africa. Assuming that males leave their natal herd at attainment of sexual maturity, parasite information sug-gested that this should occur at 12 m of length. This prediction was validated later on by analyses of gonadal tissue. Another example is the comparison of intestinal helminth abundance between pods of long-fi nned pilot whales ( Globicephala melas ) in the North Atlantic. Monte Carlo simulations revealed that adult males were more dif-fi cult to allocate into their pods than other individuals. This sug-gests male exchanges between pods, a conclusion that agrees with genetic studies that adult males do not breed within their natal pods ( Balbuena et al ., 1995 ).

Parasites transmitted through the food web have also provided information on past and present host feeding grounds. This has served to reveal geographical differences between areas for Antarctic whales, spotted seal, populations on both sides of the North Pacifi c, inshore and offshore forms of bottlenose dolphins in both the east coast of the United States and Peru, and geographical segregation of franciscana ( Pontoporia blainvillei ) south and north of the La Plata River Estuary, between Argentina and Uruguay ( Aznar et al ., 2001 ).

Finally, marine mammals can be used to evaluate the risk of human infections of protozoan pathogens. In particular, since sea otters are nearshore predators that share the same environment and some food items with humans, the ongoing studies of transmission and spatial dynamics of T. gondii in this species may prove useful to tackle toxoplasmosis of marine origin in humans ( Miller et al ., 2002 ; Dubey et al ., 2003 ).

See Also the Following Articles Health ■ Stock Identity ■ Whale Lice

References Aznar , F. J. , Fognani , P. , Balbuena , J. A. , Pietrobelli , M. , and Raga , J. A.

( 2006 ). Distribution patterns of Pholeter gastrophilus (Digenea) in the stomach of four odontocete species: the role of the host digestive physiology . Parasitology 133 , 369 – 380 .

Aznar , F. J. , Agust í , C. , Littlewood , D. T. J. , Raga , J. A. , and Olson , P. D. ( 2007 ). Insight into the role of cetaceans in the life cycle of the tet-raphyllideans (Platyhelminthes: Cestoda) . Int. J. Parasitol. 37 , 243 – 255 .

Aznar , F. J. , Balbuena , J. A. , Fern á ndez , M. , and Raga , J. A. ( 2001 ). Living together: the parasites of marine mammals . In “ Marine Mammals: Biology and Conservation ” ( P. G. H. Evans , and J. A. Raga , eds ) . Kluwer Academic/Plenum Publishers , New York .

Balbuena , J. A. , Aznar , F. J. , Fern á ndez , M. , and Raga , J. A. ( 1995 ). The use of parasites as indicators of social structure and stock identity of marine mammals . In “ Whales, Seals, Fish and Man ” ( A. S. Blix , L. Wall ø e. , and Ø . Ulltang , eds ) , pp. 133 – 139 . Elsevier Science , Amsterdam .

Beck , C. , and Forrester , D. J. ( 1988 ). Helminths of the Florida manatee, Trichechus manatus latirostris , with a discussion and summary of the parasites of sirenians . J. Parasitol. 74 , 628 – 637 .

Box 1 Main parasitic zoonoses

Trichinosis occurs mainly among people from the Arctic due to the consumption of raw or undercooked meat, particu-larly of polar bear, walrus, and some seals. Larvae of Trichinellaspecies are found in the striate muscle of many mammals, encapsulated inside individual nurse cells. When the mus-cles are ingested by another mammal, the larvae are released into the small intestine, where they penetrate the mucosa and develop to adult stage. The females give birth to numerous lar-vae, which migrate through the circulatory system to the skel-etal muscles. The damage to the host is due to both penetration of adult females in the mucosa, migration of juveniles, and penetration in the muscle and nurse cell formation. Infections in humans can be fatal. Traditional arctic dishes based on seal meat, such as igunaq, nikku, raw frozen sausage, and poorly cooked sausage represent a potential source of infection for people (Raga and Gulland, in press).

Diphyllobotriosis is caused by tapeworms of the genera Diphyllobothrium and Diplogonoporus . Human infections occur by ingestion of plerocercoids (larval stages) encysted in fi sh muscles. These larvae can develop into the adult stage in the human intestine. Usually the infections are not severe, but sometimes can lead to pernicious anemia due to B12 vitamin defi cit. Cases of marine transmitted diphyllobothriosis are particularly common in Japan and Peru due to the ingestion of raw fi sh dishes such as ceviche ( Lauckner, 1985b ; Oshima and Kliks, 1987 ).

Anisakidosis is produced by anisakid nematodes, particu-larly those of the genus Anisakis . Infections in humans occur when the larvae are eaten with either raw or lightly cooked fi sh or squid. The larvae cannot develop to the adult stage in the digestive tract of humans, but can make considerable damage to the gastric or intestinal wall. They may produce ulcers and eventually peritonitis and other severe pathologies. Although anisakidosis has been traditionally common in Asian countries, especially in Japan, the popularity of raw fi sh dishes, as sushi, has spread human infections worldwide ( Oshima and Kliks, 1987 ; Smith, 1999 ). Allergic reactions due to antigens released by the worms in the fi sh have been reported both among con-sumers and workers in fi sh processing plants. This places the problem of anisakidosis under a whole new light because some of the antigens are thermostable (Moneo et al ., 1997). Thus, common prophylactic methods, such as cooking or freezing that kill the larvae and prevent infections are not useful to avoid allergies.

In 1982, the losses caused by P. decipiens in eastern Canada were val-ued $20 million, only in processing of cod fi llets ( Aznar et al ., 2001 ).

The parasites with repercussions on public health are those that can infect humans with food (Box 1), when animals consume meat from marine mammals or, more frequently, raw fi sh or squid con-taining living infective stages.

C. Natural Tags Many parasites are useful natural markers of biological and envi-

ronmental phenomena because their transmission is linked intimately

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Dailey , M. D. ( 1985 ). Diseases of mammalia: cetacea . In “ Diseases of Marine Animals ” ( O. Kinne , ed. ) , vol. 4 , pp. 805 – 847 . Biologische Anstalt Helgoland , Hamburg , Part 2 .

Dailey , M. D. ( 2001 ). Parasitic diseases . In “ Marine Mammal Medicine ” ( L. A. Dierauf , and F. M. D. Gulland , eds ) , 2nd ed. , pp. 357 – 379 . CRC Press , Boca Raton, FL .

Dailey , M. D. ( 2005 ). Parasites of marine mammals . In “ Marine Parasitology ” ( K. Rohde , ed. ) , pp. 408 – 414 . CSIRO Publishing , Victoria .

Dubey , J. P. , et al . (12 authors) ( 2003 ). Toxoplasma gondii , Neosporacaninum , Sarcocystis neurona , and Sarcocystis canis -like infections in marine mammals . Vet. Parasitol. 116 , 275 – 296 .

Geraci , J. R. , and St. Aubin , D. J. ( 1987 ). Effects of parasites on marine mammals . Int. J. Parasitol. 17 , 407 – 414 .

Hoberg , E. P. ( 1995 ). Historical biogeography and modes of speciation across high-latitude seas of the Holartic: concepts for host – parasite coevolution among the Phocini (Phocidae) and Tetrabothriidae (Eucestoda) . Can. J. Zool. 73 , 45 – 57 .

Hoberg , E. P. , and Adams , A. ( 2000 ). Phylogeny, history and biodiver-sity: understanding faunal structure and biogeography in the marine realm . Bull. Scand. Soc. Parasitol. 10 , 19 – 37 .

Hoberg , E. P. , and Klassen , G. J. ( 2002 ). Revealing the faunal tapestry: coevolution and historical biogeography of hosts and parasites in marine systems . Parasitology 125 , 3 – 22 .

Kreuder , C. , et al . (9 authors) ( 2003 ). Patterns of mortality in southern sea otters ( Enhydra lutris nereis ) from 1998 – 2001 . J. Wildl. Dis. 39 , 495 – 509 .

Lauckner , G. ( 1985 a ). Diseases of mammalia: sirenia . In “ Diseases of Marine Animals ” ( O. Kinne , ed. ) , vol. 4 , pp. 795 – 803 . Biologische Anstalt Helgoland , Hamburg , Part 2 .

Lauckner , G. ( 1985 b ). Diseases of mammalia: pinnipedia . In “ Diseases of Marine Animals ” ( O. Kinne , ed. ) , vol. 4 , pp. 683 – 793 . Biologische Anstalt Helgoland , Hamburg , Part 2 .

Lauckner , G. ( 1985 c ). Diseases of mammalia: carnivora . In “ Diseases of Marine Animals ” ( O. Kinne , ed. ) , vol. 4 , pp. 645 – 682 . Biologische Anstalt Helgoland , Hamburg , Part 2 .

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Parental Behavior JANET MANN

Parental behavior in pinnipeds, sirenia, sea otters ( Enhydra lutris ), polar bears ( Ursus maritimus ), and cetaceans shares several features: paternal care is virtually absent, gestation and

lactation periods are typically long, females give birth to and nurse one offspring at a time (polar bears excepted), and many marine mam-mals fast during the early stages of lactation. In sum, marine mammal mothers invest extensively and exclusively in single offspring; this arti-cle reviews the diversity and nature of that investment.

Marine mammal maternal strategies vary in important respects. Polar bears, sea otters, and all three families of pinnipeds — Odobenidae (walrus, Odobenus rosmarus ), Phocidae (earless or “ true seals ” ), and Otariidae (eared seals, sea lions, fur seals) — give birth on land or ice. Twenty-three species of pinnipeds breed on land and 13 breed on ice. Cetacean and sirenian females give birth in the water; this pattern favors precocial swimming and diving. Among many pin-nipeds, maternal care is largely restricted to milk transfer, whereas the prolonged association characteristic of many cetaceans, sirenians, otters, polar bears, and some pinnipeds also involves protection and potentially extensive information transfer.

I. Feeding, Lactation, and Patterns of Association

Lactation strategies in marine mammals generally depend on trade-offs among foraging, predation risk, and reproduction. This trade-off is exemplifi ed by many marine mammal species that fast during the early stages of lactation. That females forgo feeding by breeding on land (i.e., pinnipeds) or in warm coastal waters (i.e., baleen whales) suggests that benefi ts, such as reduced predation risk and rapid energy transfer from mother to offspring, outweigh the costs of fasting. Larger bodied mammals can withstand fasting for longer periods than smaller, thus able to afford longer fasting periods devoted to offspring care. Fasting and lactation coincide in many marine mammal species and only rarely in terrestrial mammals. Early-weaning marine mammals tend to have milk that is high in fat, investing heavily in offspring for a shorter period. Late-weaning marine mammals tend to have lower fat milk (although still much higher than for terrestrial mammals). This pat-tern is generally true for comparisons between phocids and otariids, or toothed and baleen whales ( Oftedal, 1997 ; Table I ). Other factors, such as the development of pup or calf foraging skills, also contribute to late weaning ages and prolonged association (see Section IV ).

Phocids tend to fast and remain near the rookery until their pup is weaned; they rely on fat stores to nurse offspring. Phocid maternal strategies are generally characterized as fasting. A few phocids feed during lactation, notably the harp ( Pagophilus groenlandicus ), harbor (Phoca vitulina ), ringed ( Pusa hispida ), and Weddell ( Leptonychotesweddellii ) seals. Most remarkable is the hooded seal ( Cystophoracristata ), which breeds on pack ice and nurses her pup for only 4 days, transferring approximately 748,000 J or 178,657 kcal to the pup in that time ( Oftedal et al ., 1993 ).

Predator and prey distributions are likely to infl uence breeding habitat (i.e., pack ice, fast ice, beach, cave, and water) and lactation length. The relationship between breeding habitat and lactation length has been diffi cult to test using the comparative method because species breeding in similar habitats tend to be close phylogenetically.