Thirst and drinking in North American watersnakes (Nerodia spp.).

We quantified drinking behavior in three species of North American watersnakes: Nerodia clarkii, which is a marine or brackish water amphibious species, and Nerodiafasciata and Nerodiataxispilota, both freshwater amphibious species. All three species have relatively small and similar thresholds of dehydration (TH, approximately -4% loss of body mass) that elicit thirst and drinking of fresh water. These species have higher thirst sensitivity than several species of hydrophiine and laticaudine sea snakes, which are characterized by much lower TH (greater dehydration, -9% to <-20%). Nerodia clarkii, which is often found in coastal oceanic water, refused to drink seawater, but drank fresh water when dehydrated. In separate trials involving dehydration of N. clarkii and N. fasciata that were concurrently fed fish at regular intervals, snakes eventually refused to eat at TH of approximately -12% of original body mass, but resumed eating after they were allowed to drink fresh water and rehydrate. The drinking behaviors of Nerodia corroborate previous data on the importance of fresh water for drinking, and they complement growing evidence that dietary water does not itself mitigate dehydration in snakes. These new data increase understanding of water relationships in the context of evolutionary transitions from land to sea, and they emphasize the importance of fresh water resources in the conservation of coastal and marine species of reptiles.

Pelagic sea snakes dehydrate at sea.

Secondarily marine vertebrates are thought to live independently of fresh water. Here, we demonstrate a paradigm shift for the widely distributed pelagic sea snake, Hydrophis (Pelamis) platurus, which dehydrates at sea and spends a significant part of its life in a dehydrated state corresponding to seasonal drought. Snakes that are captured following prolonged periods without rainfall have lower body water content, lower body condition and increased tendencies to drink fresh water than do snakes that are captured following seasonal periods of high rainfall. These animals do not drink seawater and must rehydrate by drinking from a freshwater lens that forms on the ocean surface during heavy precipitation. The new data based on field studies indicate unequivocally that this marine vertebrate dehydrates at sea where individuals may live in a dehydrated state for possibly six to seven months at a time. This information provides new insights for understanding water requirements of sea snakes, reasons for recent declines and extinctions of sea snakes and more accurate prediction for how changing patterns of precipitation might affect these and other secondarily marine vertebrates living in tropical oceans.

Gravity and the evolution of cardiopulmonary morphology in snakes.

Physiological investigations of snakes have established the importance of heart position and pulmonary structure in contexts of gravity effects on blood circulation. Here we investigate morphological correlates of cardiopulmonary physiology in contexts related to ecology, behavior and evolution. We analyze data for heart position and length of vascular lung in 154 species of snakes that exhibit a broad range of characteristic behaviors and habitat associations. We construct a composite phylogeny for these species, and we codify gravitational stress according to species habitat and behavior. We use conventional regression and phylogenetically independent contrasts to evaluate whether trait diversity is correlated with gravitational habitat related to evolutionary transitions within the composite tree topology. We demonstrate that snake species living in arboreal habitats, or which express strongly climbing behaviors, possess relatively short blood columns between the heart and the head, as well as relatively short vascular lungs, compared to terrestrial species. Aquatic species, which experience little or no gravity stress in water, show the reverse - significantly longer heart-head distance and longer vascular lungs. These phylogenetic differences complement the results of physiological studies and are reflected in multiple habitat transitions during the evolutionary histories of these snake lineages, providing strong evidence that heart-to-head distance and length of vascular lung are co-adaptive cardiopulmonary features of snakes.

Variation of organ position in snakes.

The complex and successful evolutionary history of snakes produced variation in the position and structure of internal organs. Gravity strongly influences hemodynamics, and the impact on structure and function of the cardiovascular system, including pulmonary circulation, is well established. Therefore, we hypothesized that interspecific variation in the position of the heart and vascular (faveolar) lung should exceed that of other internal organs that are less sensitive to gravity. We examined the position of selected internal organs in 72 snakes representing 5 families and 13 species including fully aquatic and scansorial/arboreal species, representing the extremes of gravitational influence. Tests for differences of variance and coefficients of variation largely confirm that interspecific variation in position of the heart and vascular lung generally exceed those of other organs that we measured, particularly posterior organs. The variance of heart position generally exceeded that of more posterior organs, was similar to that of the anterior margin of the vascular lung, and was exceeded by that of the posterior margin of the vascular lung (variance ratio = 0.23). The gravity-sensitive vascular lung exhibited the greatest variation of any organ. Importantly, these findings corroborate previous research demonstrating the influence of gravity on cardiopulmonary morphology. Snakes offer useful model systems to help understand the adaptation of organs to a spectrum of conditions related to diversity of behavior and habitat across a broad range of related taxa.

Drinking by sea snakes from oceanic freshwater lenses at first rainfall ending seasonal drought.

Acquisition of fresh water (FW) is problematic for FW-dependent animals living in marine environments that are distant from sources of FW associated with land. Knowledge of how marine vertebrates respond to oceanic rainfall, and indeed the drinking responses of vertebrates generally following drought, is extremely scant. The Yellow-bellied Sea Snake (Hydrophis platurus) is the only pelagic species of squamate reptile and ranges across the Indo-Pacific oceans, having one of the largest geographic distributions of any vertebrate species. It requires FW and dehydrates at sea during periods of drought. Here we report drinking behaviors of sea snakes precisely at the transition from dry to wet season when rainfall first impacted the ocean following 6 months of seasonal drought. We show that the percentage of sea snakes that voluntarily drank FW in the laboratory when captured over eight successive days decreased from 80% to 13% before and after rainfall commenced, respectively. The percentage of snakes that drank immediately following capture exhibited a significant linear decline as the earliest rains of the wet season continued. Drinking by snakes indicates thirst related to dehydration, and thus thirsty snakes must have dehydrated during the previous six months of drought. Hence, the progressive decline in percentage of thirsty snakes indicates they were drinking from FW lenses associated with the first rainfall events of the wet season. These data reinforce the importance of accessing oceanic FW from precipitation, with implications for survival and distribution of pelagic populations that might be subjected to intensifying drought related to climate change.

Dehydration and drinking behavior of the marine file snake Acrochordus granulatus.

Dehydration and drinking behaviors were investigated in the little file snake (Acrochordus granulatus) collected from marine populations in the Philippines and in Australia. File snakes dehydrate in seawater and do not drink seawater when dehydrated in air and offered seawater to drink. Dehydrated file snakes drink freshwater, and the threshold of dehydration for first drinking response is a deficit of -7.4% ± 2.73% (mean ± SD) of original body mass. The thirst mechanism in this species is more sensitive than that recently studied in sea snakes. The volume of water ingested increases with increasing dehydration. Mean plasma osmolality was 278.89 ± 33.17 mMol/kg, mean hematocrit was 59% ± 5.45%, and both decreased in snakes that drank freshwater following acclimation in seawater. Snakes always drank freshwater at the water's surface, testing water with tongue flicks between each swallowing of water. Some snakes ingested large volumes of freshwater, approaching 50% of body mass. Visual observations and measurements of osmolality in plasma and stomach fluids suggest that water is taken up from the gut and dilutes body fluids slowly over the course of 48 h or longer. Eighty percent of snakes that were collected during the dry season (following >4 mo of drought) in Australia drank freshwater immediately following their capture, indicating that snakes were dehydrated in their marine environment even when known to have been feeding at the time. Snakes kept in seawater maintained a higher state of body condition when freshwater was periodically available. These results support a growing conclusion that diverse taxa of marine snakes require environmental sources of freshwater to maintain water balance, contrary to earlier belief. Identifying the freshwater requirements of secondarily marine vertebrates is important for better understanding how they maintain water balance in marine habitats, especially with respect to conservation in changing environments.

Preliminary insights into the phylogeography of the yellow-bellied sea snake, Pelamis platurus.

The yellow-bellied sea snake, Pelamis platurus (Elapidae, Hydrophiinae), has the largest distribution of any snake species, and patterns related to its distribution and regional color variation suggest there is population structuring in this species. Here, we use mitochondrial (ND4, Cyt-b) and nuclear (RAG-1) DNA to (1) test whether genetic variation is associated with local variation in color pattern, and (2) assess whether large-scale patterns of genetic variation are correlated with geographic distribution across the Pacific Ocean. We found low levels of genetic variation and shallow population structure that are correlated with local variation in color pattern and with geographic distribution. The low levels of genetic divergence indicate a relatively high rate of gene flow throughout the Pacific region and/or a recent expansion of range, both of which could be attributable to the passive drifting of these snakes on oceanic surface currents. The mtDNA data conform closely to a model of past exponential population growth, and this may have been associated with the species' large eastward and westward expansion of range. The pattern of low nucleotide and high haplotype diversity suggests that this population growth occurred in the relatively recent past. Data from drifting buoys can potentially act as informative models for predicting patterns of drifting in Pelamis and for generating additional testable hypotheses relating to its population structure and biogeography. Future studies should employ nuclear microsatellite markers to investigate population structure in this species at a finer scale. The exploitation of oceanic currents as a novel and highly efficient dispersal mechanism has likely facilitated gene flow throughout the Pacific Ocean in this uniquely pelagic species of sea snake, resulting in a distribution spanning over half of the earth's circumference.

Marine snake epibiosis: a review and first report of decapods associated with Pelamis platurus.

Under circumstances in which area for settlement is limited, the colonization of living substrata may become a highly valuable strategy for survival of marine invertebrates. This phenomenon, termed epibiosis, results in spatially close associations between two or more living organisms. Pelamis platurus, the yellow-bellied sea snake, is the only exclusively pelagic marine snake and its propensity for foraging along ocean slicks facilitates its colonization by pelagic epibionts. Herein, we report epibionts associated with P. platurus inhabiting the waters off the northwestern Pacific coast of Costa Rica. These associations include the first records of decapod epibionts from any marine snake. Decapod epibionts were found on 18.9% of P. platurus, and size of snake (total length) had a significant positive effect on the frequency and intensity of epibiosis. We discuss the spatial and ecological mechanisms that facilitate these interactions, as well as the suite of factors that either promote or deter epibiosis and ultimately dictate the frequency and intensity of these interactions. Finally, we provide a review of marine snake epibiosis. The intention of this review is to (1) provide contemporary researchers with a single, accessible reference to all known reports of epibionts associated with marine snakes and (2) discuss what is currently known with respect to diversity of epibionts from marine snakes.

Dehydration and drinking responses in a pelagic sea snake.

Recent investigations of water balance in sea snakes demonstrated that amphibious sea kraits (Laticauda spp.) dehydrate in seawater and require fresh water to restore deficits in body water. Here, we report similar findings for Pelamis platurus, a viviparous, pelagic, entirely marine species of hydrophiine ("true") sea snake. We sampled snakes at Golfo de Papagayo, Guanacaste, Costa Rica and demonstrated they do not drink seawater but fresh water at variable deficits of body water incurred by dehydration. The threshold dehydration at which snakes first drink fresh water is -18.3 ± 1.1 % (mean ± SE) loss of body mass, which is roughly twice the magnitude of mass deficit at which sea kraits drink fresh water. Compared to sea kraits, Pelamis drink relatively larger volumes of water and make up a larger percentage of the dehydration deficit. Some dehydrated Pelamis also were shown to drink brackish water up to 50% seawater, but most drank at lower brackish values and 20% of the snakes tested did not drink at all. Like sea kraits, Pelamis dehydrate when kept in seawater in the laboratory. Moreover, some individuals drank fresh water immediately following capture, providing preliminary evidence that Pelamis dehydrate at sea. Thus, this widely distributed pelagic species remains subject to dehydration in marine environments where it retains a capacity to sense and to drink fresh water. In comparison with sea kraits, however, Pelamis represents a more advanced stage in the evolutionary transition to a fully marine life and appears to be less dependent on fresh water.

Sea snakes (Laticauda spp.) require fresh drinking water: implication for the distribution and persistence of populations.

Dehydration and procurement of water are key problems for vertebrates that have secondarily invaded marine environments. Sea snakes and other marine reptiles are thought to remain in water balance without consuming freshwater, owing to the ability of extrarenal salt glands to excrete excess salts obtained either from prey or from drinking seawater directly. Contrary to this long-standing dogma, we report that three species of sea snake actually dehydrate in marine environments. We investigated dehydration and drinking behaviors in three species of amphibious sea kraits (Laticauda spp.) representing a range of habits from semiterrestrial to very highly marine. Snakes that we dehydrated either in air or in seawater refused to drink seawater but drank freshwater or very dilute brackish water (10%-30% seawater) to remain in water balance. We further show that Laticauda spp. can dehydrate severely in the wild and are far more abundant at sites where there are sources of freshwater. A more global examination of all sea snakes demonstrates that species richness correlates positively with mean annual precipitation within the Indo-West Pacific tropical region. The dependence of Laticauda spp. on freshwater might explain the characteristically patchy distributions of these reptiles and is relevant to understanding patterns of extinctions and possible future responses to changes in precipitation related to global warming. In particular, metapopulation dynamics of the Laticauda group of sea snakes are expected to change in relation to projected reductions of tropical dry-season precipitation.