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Life Begins When the Sea Lion Is Ashore: Microhabitat Use by a Louse Living on a Diving Mammal Host

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Life Begins When the Sea Lion Is Ashore: Microhabitat Use by a Louse Living on a Diving Mammal Host Bulletin of Entomological Research, Page 1 of 9 doi:10.1017/S0007485311000794 © Cambridge University Press 2012 Life begins when the sea lion is ashore: microhabitat use by a louse living on a diving mammal host M.S. Leonardi1*, E.A. Crespo1, D.G. Vales1, M. Feijoo2, J.A. Raga3 and F.J. Aznar3 1Laboratorio de Mamíferos Marinos, Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, PC U9120ACV, Puerto Madryn, Argentina: 2Laboratorio de Evolución, Facultad de Ciencias, Universidad de la República. Casillas 12106, PC 11400, Montevideo, Uruguay: 3Unidad de Zoología Marina, Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universidad de Valencia, PC 46071 Valencia, España Abstract Among Anoplura, the family Echinophthiriidae includes species that infest pinnipeds and otters. Previous evidence obtained from pinnipeds infested by echinophthiriids, specifically from seals, indicates that flippers are the preferred infestation sites, while lice from fur seals select areas in the pelage. We studied habitat selection of Antarctophthirus microchir on South American sea lion pups (Otaria flavescens Shaw, 1800) from Patagonia, Argentina, during the austral summer of 2009. We found a clear pattern of habitat selection: eggs are laid on the dorsal surface; nymphs 1 hatch there and then migrate to the belly, where they develop into adults and copulate; and then ovigerous females return to the dorsal surface. On the one hand, nymphs 1 are characterised by their low locomotory ability; therefore, the fact that they migrate as soon as they hatch suggests a clear pressure leading to microhabitat restriction. On the other hand, the described pattern of microhabitat selection seems to respond to the physiological requirements of each stage, which vary according to the physiological process considered, e.g. oviposition, morpho- genesis, hatching and development. Accordingly, it appears that A. microchir would prefer the host’s ventral area for development and copulation and the dorsal area for oviposition. However, the causes of this pattern are not clear, and many factors could be involved. Considering that sea lion pups periodically soak at high tides, and that prolonged immersion and very high humidity are known to be lethal for lice eggs, selecting the dorsal area would be advantageous for oviposition because it dries much faster. Furthermore, because humidity should be retained for longer periods on the ventral surface of the pup, wetter conditions on the sea lion would prevent desiccation of the nymphs in the very arid environment where O. flavescens breeds. Keywords: habitat selection, sucking lice, Echinophthiriidae, Antarctophthirus microchir, South American sea lion, Otaria flavescens, Patagonia, Argentina (Accepted 2 December 2011) *Author for correspondence Fax: (+54) 2965 451543 E-mail: [email protected] 2 M.S. Leonardi et al. Table 1. Features of the three families of Pinnipedia concerning diversity, geographical distribution, lice fauna and biological traits that could influence habitat selection by lice (Kim, 1985; Durden & Musser, 1994; Berta et al., 2006; Mostmant Liwanag, 2008 and references therein). Family Otariidae (fur seals and sea lions) Phocidae (true seals) Odobenidae (walrus) (14 spp.) (18 spp.) (1 sp.) Diversity Fur seals (9 spp.): genera Arctocephalus Genera Mirounga (2 spp.) Monachus spp. Odobenus rosmarus (8 spp.) and Callorhinus (1 sp.) (2 spp.); Leptonychotes (1 sp.); Lobodon Sea lions (5 spp): genera Phocarctos (1 sp.); Ommatophoca (1 sp.); Hydrurga (1 sp.); Neophoca (1 sp.); Eumetopias (1. sp.) Halichoerus (1 sp.); Cystophora (1 sp.); Zalophus (1 sp.) and Otaria (1 sp.); Erignathus (1 sp.); Pagophilus (1 sp.) (1 sp.); Histriophoca (1 sp.) and Phoca (5 spp.) Geographical Pacific Ocean, Antarctic and Polar and sub-polar regions; Paleartic Arctic Ocean and sub-Arctic seas distribution sub-Antarctic waters; South temperate seas (Pusa, Phoca); Atlantic (A. australis, A. pusillus, temperate and tropical seas O. flavescens) (Monachus); antitropical in Pacific and Atlantic oceans (Mirounga) Lice species Proechinophthirus fluctus (on Lepidophthirus macrorhini (on Mirounga); Antarctophthirus trichechi Callorhinus, Eumetopias); P. zumpti L. piriformis (on Monachus), (on two species of Arctocephalus); Echinophthirius horridus Antarctophthirus callorhini (on (on Halichoerus, Cystocephora, Callorhinus); A. microchir (on all sea Erignathus, Pagophilus and Phoca); lion species) Antarctophthirus ogmorhini (on Leptonychotes and Hydrurga); A. mawsoni (on Ommatophoca) and A. lobodontis (on Lobodon) Pelage Fur seals: high-density, air-trapping, Low-density, wettable fur with short Only short and sparse guard hairs non-wettable fur with long guard guard hairs and underhairs hairs and underhairs Sea lions: medium-density, wettable fur with short guard hairs and underhairs Insulation Fur seals: air layer Mainly bubbler (fur important in pups) Bubbler Sea lions: mainly blubber Skin At or near to body temperature At or near to ambient temperature At or near to ambient temperature temperature Flippers Can be brought beneath body Cannot be brought beneath body Can be brought beneath body Dorsal side with sparse hair, ventral Dense hair on both sides Hairless side naked Terrestrial Support on all four limbs, thrust By vertical undulations of the trunk Body supported in large part by the locomotion produced by both fore- and hind Belly. Combined movement of flippers hind limbs with a lunge in which the chest is raised by forelimbs Introduction A. mawsoni). A further species of echinophthiriid, Latagophthirus rauschi, has been described from river otters, Lice (order Phthiraptera) are the only insects that have Lontra canadensis, in North America (Kim, 1985). become obligate and permanent parasites throughout Echinophthiriids have developed unique morphological their entire life cycles, living as ectoparasites on the host’s adaptations to cope with the amphibious lifestyle of their surface (Kim, 1985; Bush et al., 2001). Among the sucking lice hosts. All species possess (i) tibia-tarsi of second and third (Anoplura), the family Echinophthiriidae is the only family pairs of legs strongly adapted to apprehension; (ii) a whose species have adapted to survive on pinnipeds (Durden membranous abdomen that could increase the efficiency of & Musser, 1994), a mammalian group that includes fur seals gas exchange, particularly underwater; and (iii) abdominal and sea lions (Otariidae), walruses (Odobenidae) and true spiracles with a sophisticated closing device that apparently seals (Phocidae); table 1 summarises the main differences preserves atmospheric air and prevents flooding during the among pinniped families. Currently, the Echinophthiriidae host’s immersions (Kim, 1975). Other adaptations, however, consist of 12 species distributed in five genera (table 1): seem to have evolved as a specific response to the different Proechinophthirus include two species infesting fur seals and insulation mechanisms of their hosts. Fur seals have devel- sea lions, whereas species of Lepidophthirus (two species) oped a dense long-haired fur that creates a layer of trapped and Echinophthirius (monotypic) occur in true seals. air when the animal is submerged (table 1). This insulation Antarctophthirus is the most diversified and less host-specific mechanism generates a virtually ‘terrestrial’ environment for genus, with six recognised species infecting fur seals species of Proechinophthirus, e.g. Proechinophthirus fluctus on (A. callorhini), sea lions (A. microchir), walruses (A. trichechi) northern fur seals and Callorhinus ursinus (Kim, 1975). and Antarctic true seals (A. lobodontis, A. ogmorhini and However, sea lions, true seals and walruses rely more on Life begins when the sea lion is ashore 3 blubber for insulation and have a less dense and wettable largely qualitative and/or based on small sample sizes, they pelage (table 1). Accordingly, echinophthiriids infesting these show two broad patterns of microhabitat selection. First, pinnipeds are exposed to truly aquatic conditions, and this the four echinophthiriid species infesting true seals tend to apparently results in further morphological adaptations. In concentrate mainly on the host’s hind flippers, whereas the species of Antarctophthirus, Lepidophthirus and Echinophthirius, two species infecting the fur seal have broad distributions that spines have been modified into scales that cover the whole change with the age of the host; however, hind flippers are not body surface and may serve as a plastron or as a protective the preferred microhabitat for any species (table 2). Second, surface for their very thin cuticle (Hinton, 1976; Murray, 1976; regardless of their taxonomic position, at least the three species Mehlhorn et al., 2002). infesting true seals from polar and sub polar regions also use Differences between pinnipeds, specifically between non- hind flippers as the oviposition site (no data are available for wettable (fur seals) and wettable (other pinnipeds), also seem the species infecting fur seals, see table 2). Murray & Nicholls to influence the life history strategies of their lice. It has been (1965) and Murray et al.(1965) suggested that hind flippers suggested that Proechinophthirus fluctus and Antarctophthirus are highly vascularised areas that would represent a food-rich callorhini, which infect the northern fur seal (Callorhinus habitat and are also a place for heat dissipation, thus providing ursinus), a host species with a non-wettable pelage (see a suitable
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