Chapter 11 Living Together: the Parasites of Marine Mammals1

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Chapter 11 Living Together: the Parasites of Marine Mammals1 Chapter 11 Living together: the parasites of marine mammals1 F. JAVIER AZNAR, JUAN A. BALBUENA, MERCEDES FERNÁNDEZ and J. ANTONIO RAGA Department of Animal Biology, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Dr. Moliner 50, 46100 Burjassot (Valencia), Spain, E-mail: [email protected] 1. INTRODUCTION The reader may wonder why, within a book of biology and conservation of marine mammals, a chapter should be devoted to their parasites. There are four fundamental reasons. First, parasites represent a substantial but neglected facet of biodiversity that still has to be evaluated in detail (Windsor, 1995; Hoberg, 1997). Perception of parasites among the public are negative and, thus, it may be hard for politicians to justify expenditure in conservation programmes of such organisms. However, many of the reasons advanced for conserving biodiversity or saving individual species also apply to parasites (Marcogliese and Price, 1997; Gompper and Williams, 1998). One fundamental point from this conservation perspective is that the evolutionary fate of parasites is linked to that of their hosts (Stork and Lyal, 1993). For instance, the eventual extinction of the highly endangered Mediterranean monk seal Monachus monachus would also result in that of its host-specific sucking louse Lepidophthirus piriformis (Figure 1B). Second, parasites cause disease, which may have considerable impact on 1 Order of authorship is alphabetical and does not reflect unequal contribution Marine Mammals: Biology and Conservation, edited by Evans and Raga, Kluwer Academic/Plenum Publishers, 2001 385 386 Parasites of marine mammals marine mammal populations (Harwood and Hall, 1990). Scientists have come to realise this particularly after the recent die-offs caused by morbilliviruses (Domingo et al., this volume). However, these epizootic outbreaks represent the most dramatic, but by no means the only, example of parasite-induced mortality in marine mammal populations (see Section 3 below). Third, parasites are elegant markers of contemporary and historical ecological relationships, providing information on host ecology, biogeography and phylogeny (Gardner and Campbell, 1992; Brooks and McLennan, 1993; Hoberg, 1996, 1997). From the perspective of conservation and management, parasites have proved especially useful as biological tags for host social structure, movements and other ecological aspects of marine mammal populations (Balbuena et al., 1995). Finally, some parasites of marine mammals have public health and economic importance (Oshima and Kliks, 1987). For instance, the nematode Anisakis simplex uses fish and squid as intermediate hosts to infect cetaceans. Consumption of raw or lightly-cooked seafood can result in human infections, causing a severe clinical condition known as anisakidosis. In addition, recent studies have shown that A. simplex in fish fillets can produce allergic reactions in humans (Fernández de Corres et al., 1996; Armentia et al., 1998). Besides, parasites of marine mammals cause important losses to the fish processing industry. Costs resulting from the removal of larvae of the sealworm Pseudoterranova decipiens from cod fillets alone were estimated to be in excess of CAD 29 million in 1982 in Atlantic Canada (Burt, 1994). In this chapter, we review different aspects of the biology of marine mammal parasites, organising the concepts under four main sections: (1) the parasite diversity, (2) the interaction between host and parasite populations, (3) the origin and evolution of the parasite faunas and (4) the structure of parasite communities. There are obvious limitations of space and, therefore, we just can outline major ideas and provide selected examples that illustrate the conceptual framework. The chapter is not intended as a major review of the old literature and so readers keen to trace back the history of ideas to their very beginning should look up the references provided herein. 2. PARASITE DIVERSITY Biodiversity results from the complex interaction of phylogeny, ecology, geography and history as determinants of the evolution and distribution of organisms (Hoberg, 1997). In this section, we present the outcome of this interaction, i.e., a descriptive outline of patterns of association between marine mammals and their parasites. The processes leading to the observed 11. Aznar et al. 387 patterns will be treated with some detail in the Sections 4 and 5. It is important to distinguish between generalist organisms that can occur not only in marine mammals but in many other habitats (e.g., Clostridium botulinum, Escherichia coli) from those which have arisen specifically in these hosts. The latter are more meaningful from the biodiversity perspective. We consider here the term ‘parasite’ in its widest sense (Price, 1980) and, for convenience, we divide this section in one part devoted to microparasites (e.g., viruses, bacteria, protozoons) and another, to macroparasites (commonly helminths and arthropods) (see Anderson, 1993, for a definition of these concepts). For completeness, other symbiotic associations, such as phoresis or commensalism are also included. As a cautionary note, bear in mind that the differences in coverage of micro- and macroparasites of marine mammals reflect the degree to which both groups have been studied. Studies of metazoan parasites of sea mammals date back to linnean times, and gained momentum in the last 50 years, particularly thanks to the work of Soviet helminthologists (Delyamure, 1955; Delyamure and Skriabin, 1985). In contrast, research on micro-organisms is a fairly recent addition to the field of marine mammal parasitology. For instance, not a single virus had been isolated from any marine mammal prior to 1968, and information on viral diseases was scanty until the 80s (Lauckner, 1985a). In addition, the data presented herein are influenced by the degree of sampling effort of the host groups, and, therefore, they do not necessarily reflect an even, complete representation of the richness and diversity of parasites in marine mammals. 2.1 Microparasites Virological studies of marine mammals are currently in progress. Visser et al. (1991) reported 12 different viruses belonging to 10 families, isolated from wild and captive pinnipeds; van Bressem et al. (1999) have recorded 9 virus families in some 25 cetaceans species, and Duignan et al. (1995) recently found morbillivirus antibodies in sirenians (Table 1). We will focus on the genus Morbillivirus (family Paramyxoviridae) because this is one of the viral groups most studied, and several types show a specific relationship with marine mammal hosts. The first morbillivirus of marine mammals was isolated in 1988 and was christened phocine distemper virus (PDV). The PDV caused mass mortality in the North Sea populations of harbour seals Phoca vitulina and, to a lesser extent, grey seals Halichoerus grypus (Domingo et al., this volume). Since then, other morbilliviruses have been discovered in other marine mammals, causing high mortality (Osterhaus et 388 Parasites of marine mammals al., 1998; Domingo et al., this volume). Particularly, two types are known in cetaceans: the porpoise morbillivirus (PMV) and the dolphin morbillivirus (DMV), which are considered as strains of the same species (Kennedy, 1998; Domingo et al., this volume; van Bressem et al., 1999). Table 1. Occurrence of virus, bacterium and protozoan families in marine mammals. Host group Pinnipedia Cetacea Sirenia Sea otter References Viruses Adenoviridae x x 1, 2 Caliciviridae x x 1, 2 Coronaviridae x 1 Hepadnaviridae x 2, 3 Herpesviridae x x 1, 2 Orthomyxoviridae x x 1, 2 Papovaviridae x 2 Paramyxoviridae x x ? 1, 2, 4, 5, 28 Picornaviridae x x 1 Poxviridae x x 1, 2 Retroviridae x 1 Rhabdoviridae x x 1, 2 Bacteria Bacteroidaceae x 6 Corynebacteriaceae x 7, 8 Enterobacteriaceae x x 6, 7, 9, 10, 11 Leptospiraceae x ? 7, 12 Micrococcaceae x x x 9, 7, 13, 28 Mycobacteriaceae x x 13, 14, 15 Neisseriaceae x x 7, 9 Nocardiaceae x 7 Pasteurellaceae x x ? 6, 7, 9, 11, 16, 28 Pseudomonadaceae x x x 7, 9, 13 Streptococcaceae x 7, 17, 18 Vibrionaceae x x 6, 7, 9, 19 Abiotrophia* x 20 Alcaligenes* x 7 Arcanobacterium* x 21 Brucella* x x 22 Cetobacterium* x 23 Clostridium* x ? 6, 7, 10, 28 Erysipelothrix* x x 7, 9 Mycoplasma* x 24, 25 Protozoa Eimeriidae x x 7, 13, 26 Sarcocystidae x x x 7, 9, 26, 27 *Incertae sedis. References: 1 Visser et al. (1991), 2 van Bressem et al. (1999), 3 Bossart et al. (1990), 4 Duignan et al. (1995), 5 Kennedy (1998), 6 Baker et al. (1998), 7 Lauckner (1985b), 8 Pascual-Ramos et al. (1998), 9 Dailey (1985), 10 Baker and Ross (1992), 11 Foster et al. (1998), 12 Gulland et al. (1996), 13 Lauckner (1985c), 14 Romano et al. (1995), 15 Thorel et 11. Aznar et al. 389 al. (1998), 16 Foster et al. (1996), 17 Goh et al. (1998), 18 Swenshon et al. (1998), 19 Fujioka et al. (1988), 20 Lawson et al. (1999), 21 Pascual-Ramos et al. (1997), 22 Jahans et al. (1997), 23 Foster et al. (1995), 24 Giebel et al. (1991), 25 Ruhnke and Madoff (1992), 26 Beck and Forrester (1988), 27 Domingo et al. (1992), 28 Lauckner (1985a). Genomic and antigenic data suggest that the PDV is closely related to the canine distemper virus (CDV) of land carnivores, whereas the PMV- DMV seems more similar to morbilliviruses of ruminants (Visser, 1993; Barrett et al., 1993; Kennedy, 1998). This should not be viewed as a result of parallel evolution (i.e., co-evolution, see Section 4) between the hosts and their viruses. Given the differences in the rate of evolutionary diversification between mammals and viruses, it seems more likely that common viral ancestors were able to infect phylogenetically related taxa because these are biologically similar (Visser, 1993). Bacteria of about 30 genera have been isolated in marine mammals (Table 1 and references therein). Howard et al. (1983), Lauckner (1985a, 1985b, 1985c), Dailey (1985) and Dunn (1990) have reviewed the bacterial infections of both wild and captive marine mammals. The majority of these bacteria are widely distributed in many environments.
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