Integrative and Comparative Biology Integrative and Comparative Biology, Volume 52, Number 2, Pp

Integrative and Comparative Biology Integrative and Comparative Biology, volume 52, number 2, pp. 235–244 doi:10.1093/icb/ics081 Society for Integrative and Comparative Biology SYMPOSIUM Effects of Oceanic Salinity on Body Condition in Sea Snakes François Brischoux,1,*,† Virginie Rolland,‡ Xavier Bonnet,* Matthieu Caillaud§ and Richard Shineô *Centre d’Etudes Biologiques de Chize´, CEBC-CNRS UPR 1934, 79360 Villiers en Bois, France; †Department of Biology, University of Florida, Gainesville, FL 32611, USA; ‡Department of Biological Sciences, PO Box 599, State University, Jonesboro, AR 72467, USA; §IFREMER Nouvelle Cale´donie, LEADNC, Campus IRD, BP 2059, 98846 Noumeá Cedex, Nouvelle Cale´donie, France; ôSchool of Biological Sciences A08, University of Sydney, Sydney, NSW 2006, Australia From the symposium ‘‘New Frontiers from Marine Snakes to Marine Ecosystems’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2012 at Charleston, South Carolina. 1E-mail: [email protected] Downloaded from Synopsis Since the transition from terrestrial to marine environments poses strong osmoregulatory and energetic challenges, temporal and spatial fluctuations in oceanic salinity might influence salt and water balance (and hence, body condition) in marine tetrapods. We assessed the effects of salinity on three species of sea snakes studied by mark– http://icb.oxfordjournals.org/ recapture in coral-reef habitats in the Neo-Caledonian Lagoon. These three species include one fully aquatic hydrophiine (Emydocephalus annulatus), one primarily aquatic laticaudine (Laticauda laticaudata), and one frequently terrestrial laticaudine (Laticauda saintgironsi). We explored how oceanic salinity affected the snakes’ body condition across various temporal and spatial scales relevant to each species’ ecology, using linear mixed models and multimodel inference. Mean annual salinity exerted a consistent and negative effect on the body condition of all three snake species. The most terrestrial taxon (L. saintgironsi) was sensitive to salinity over a short temporal scale, corresponding to the duration of a typical marine foraging trip for this species. In contrast, links between oceanic salinity and body condition in the fully aquatic E. annulatus and the highly aquatic L. laticaudata were strongest at a long-term (annual) scale. The sophisticated by guest on July 20, 2012 salt-excreting systems of sea snakes allow them to exploit marine environments, but do not completely overcome the osmoregulatory challenges posed by oceanic conditions. Future studies could usefully explore such effects in other secondarily marine taxa such as seabirds, turtles, and marine mammals. success (e.g., Pinaud et al. 2005; Weimerskirch Introduction et al. 2010). In several taxa, environmentally induced Secondarily marine, air-breathing vertebrates provide variation in such traits ultimately influences popula- robust model systems with which to explore the tion dynamics (Forcada et al. 2006; Rolland et al. complex effects of bio-physical parameters of the 2009). Understanding such links can enhance our oceanic environment across a range of temporal ability to predict biotic responses to environmental and spatial scales. Research over the past two decades perturbations (Jenouvrier et al. 2009; Wolf et al. has revealed strong links between environmental 2010). parameters (e.g., sea surface temperature, primary Although simply documenting empirical links production, sea-ice extent, El Ninõ or La Ninã between environmental variation and population re- events, and fisheries offtake) on population parame- sponses is useful, an understanding of the proximate ters such as abundance (e.g., Baez et al. 2011), mechanisms that cause such links provides a stronger growth rates (e.g., Quillfeldt et al. 2007), survival (and more general) basis for accurate prediction (e.g., Rolland et al. 2010), breeding probabilities (Helmuth et al. 2005; Kearney and Porter 2009). In (e.g., Jenouvrier et al. 2003), breeding success (e.g., most cases, such mechanisms will include several Leaper et al. 2006; Lee 2011), and aspects of individ- intermediate steps between the physical properties ual behavior, such as spatial ecology and foraging of the marine environment and their ultimate effects Advanced Access publication June 18, 2012 ß The Author 2012. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. 236 F. Brischoux et al. on individuals, or populations, of predators. All spe- the degree of reliance on marine versus terrestrial cies of secondarily marine vertebrates use the oceanic habitats varies extensively among species within environment to forage, so that the effects of physical these lineages. Hydrophiines are totally aquatic, oceanic parameters on apex predators likely are me- whereas laticaudines are amphibious (Heatwole diated by intermediate trophic levels (Pinaud et al. 1999). Within the laticaudines (sea kraits), some 2005). Even apparently direct effects, such as those of taxa use terrestrial habitats more frequently than currents, fronts, or the extent of sea-ice on the at-sea do others (Greer 1997; Bonnet et al. 2005; Lane distribution of seabirds or marine mammals, may in and Shine 2011a, 2011b), and laticaudine species fact be mediated by the distribution of trophic re- vary in their ability to tolerate saline conditions (as sources (Bost et al. 2009). measured by dehydration rates in seawater) (Lilly- Clearly, however, not all impacts of environmental white et al. 2008). Maintaining osmotic balance variables on organismal function work through in- seems to pose a physiological challenge to marine termediate steps such as shifts in availability of food; snakes, and some species require access to fresh or some environmental effects act directly on the indi- brackish water for their survival (Bonnet and vidual organism (Tomanek and Somero 2000; Brischoux 2008; Lillywhite et al. 2008). Finally, salin- Helmuth et al. 2002). For example, water tempera- ity likely influenced the evolutionary transition to ture directly affects body temperatures (and thus marine life in snakes and currently constrains the Downloaded from metabolic rates) of ectothermic vertebrates and, diversity and geographic distributions of sea snakes hence, influences the duration of their dives (Priest (Brischoux et al. 2012). and Franklin 2002; Storey et al. 2008; Pratt and This combination of traits renders the elapid sea Franklin 2010); and substantially modifies the snakes a powerful model system with which to ex- energy budgets of endothermic divers (de Leeuw plore the effects of salinity on marine vertebrates. http://icb.oxfordjournals.org/ 1996; Butler and Jones 1997; Gre´millet et al. 2001). Salinity might affect sea snakes through two path- Although typically overlooked (but see Gutie´rrez ways: (1) the energetic costs of excreting excess salt et al. 2011; Brischoux et al. 2012), salinity poses a (Peaker and Linzell 1975; Gutie´rrez et al. 2011) and major physiological challenge to air-breathing marine (2) dehydration due to water loss from the body to vertebrates. Since seawater is hyperosmotic to body the surrounding seawater (Lillywhite et al. 2008). fluids, marine species gain salt and lose water across Both of these processes should influence a snake’s permeable surfaces (Schmidt-Nielsen 1983). Drinking body mass (through utilization of body reserves for of seawater (e.g., during prey capture) imposes a the former and due to water loss for the latter) and, by guest on July 20, 2012 supplementary salt-load (Costa 2002; Houser et al. hence, its body condition (mass relative to body 2005). Thus, most marine vertebrates must regulate length, sensu Bonnet and Naulleau [1995]). We their osmotic balance (Schmidt-Nielsen 1983). thus explored the effect of salinity on the body con- Excreting excess salt through specific structures dition of three species of sea snakes (a hydrophiine (salt glands in nonmammalian vertebrates [Peaker sea snake, Emydocephalus annulatus, and two laticau- and Linzell 1975], reniculate kidneys, and elongated dine sea kraits, Laticauda laticaudata and Laticauda nephrons in marine mammals [Ortiz 2001]) can saintgironsi) from populations that we have regularly entail significant energetic costs (Schmidt-Nielsen surveyed through mark–recapture studies since 2002 1983; Ortiz 2001; Gutie´rrez et al. 2011). on the coral reefs of New Caledonia. Since these Dehydration due to osmotic loss of water to a species differ in their degree of reliance on oceanic saline medium is another risk faced by marine ver- habitats (see earlier), we adopted two complementary tebrates (Lillywhite et al. 2008). Taken together, these approaches. First, we used a large time-scale analysis elements suggest that oceanic salinity may impose to compare inter-annual variation in body condition significant energetic and hydric costs to air-breathing to concurrent variation in oceanic salinity. Second, vertebrates. we used a finer-scaled approach to explore potential Herein, we test the hypothesis that salinity may effects of salinity at temporal and spatial scales rele- impose costs to marine tetrapods, using three species vant to each species’ ecology. of sea snakes from the family Elapidae as our study system. Two independent phylogenetic transitions Materials and Methods from terrestrial to marine life have occurred within Study

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