Coleman M. Sheehy

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.

Water exchange and permeability properties of the skin in three species of amphibious sea snakes (Laticauda spp.).

SUMMARY Evolutionary transitions between different environmental media such as air and water pose special problems with respect to skin permeability because of the dramatic changes in the driving gradients and nature of water exchange processes. Also, during the transitional periods prior to complete adaptation to a new medium, the skin is exposed to two very different sets of environmental conditions. Here, we report new data for transepidermal evaporative water loss (TEWL) and cutaneous resistance to evaporative water loss (Rs) of sea snakes that are transitional in the sense of being amphibious and semi-terrestrial. We investigated three species of sea kraits (Elapidae: Laticaudinae) that are common to Orchid Island (Lanyu), Taiwan. Generally, Rs of all three species is lower than that characteristic of terrestrial/xeric species of snakes measured in other taxa. Within Laticauda, Rs is significantly greater (TEWL lower) in the more terrestrial species and lowest (TEWL highest) in the more aquatic species. Previously reported losses of water from snakes kept in seawater exhibit a reversed trend, with lower rates of loss in the more aquatic species. These data suggest selection for adaptive traits with respect to increasing exposure to the marine environment. Thus, a countergradient of traits is reflected in decreased TEWL in aerial environments and decreased net water efflux in marine environments, acting simultaneously in the three species. The pattern for TEWL correlates with ultrastructural evidence for increased lipogenesis in the stratum corneum of the more terrestrial species. The skin surfaces of all three species are hydrophobic. Species differences in this property possibly explain the pattern for water efflux when these snakes are in seawater, which remains to be investigated.

Pitviper Scavenging at the Intertidal Zone: An Evolutionary Scenario for Invasion of the Sea

ABSTRACT It is difficult for terrestrial vertebrates to invade the sea, and little is known about the transitional evolutionary processes that produce secondarily marine animals. The utilization of marine resources in the intertidal zone is likely to be an important first step for invasion. An example of this step is marine scavenging by the Florida cottonmouth snakes (Agkistrodon piscivorus conanti) that inhabit Gulf Coast islands. These snakes principally consume dead fish that are dropped from colonial nesting bird rookeries, but they also scavenge beaches for intertidal carrion, consuming dead fish and marine plants, and occasionally enter seawater. Thus, allochthonous marine productivity supports the insular cottonmouth population through two pathways, and one of these pathways connects the snakes directly to the sea. The trophic ecology and behaviors of this unusual snake population suggest a requisite evolutionary scenario for the successful transition of vertebrates from a terrestrial to a marine existence.

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.

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.

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 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 (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 mMol/kg, mean hematocrit was , 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.

A NEW SPECIES OF ISCHNOCNEMA (ANURA: LEPTODACTYLIDAE) FROM LA PAZ, BOLIVIA

We describe a new species of Ischnocnema from upper montane rainforest in La Paz, Bolivia. Unlike its congeners, the new species possesses notched ungual flaps, a short dorsolateral fold, and a small axillary gland. The new species resembles I. sanctaecrucis and is the third species of Ischnocnema known from Bolivia.

Identification and Description of the Tadpole of the Parachuting Frog Rhacophorus catamitus from Southern Sumatra, Indonesia

Abstract The Indonesian parachuting frog Rhacophorus catamitus is endemic to the mountains of southern Sumatra. Herein, we describe the larval morphology of this species based on several developmental stages. Tadpoles were collected from localities that ranged in elevation from 1,068–1,680 m in montane primary and secondary growth rainforest habitats. We matched larvae to an adult paratype and a referred specimen using mitochondrial DNA. The tadpole of R. catamitus has a conspicuous black tail tip and a larval morphology similar to most congeners. Characteristics of this body plan include a ventral oral disc, jaw sheaths, several labial tooth rows, dorsolaterally positioned eyes, a single sinistral spiracle, and a median anal tube. All specimens (N = 28) have a large suctorial oral disc with 9–11 tooth rows (6–8 anterior, 3 posterior) that we hypothesize is an adaptation for life in fast-flowing streams. At least two size cohorts of R. catamitus larvae were collected in June 1996, suggesting that this species may breed either continuously or opportunistically throughout the year.

Patterns of Genetic Differentiation Among Populations of Smilisca fodiens

Abstract The Trans-Mexican Volcanic Belt and surrounding areas contain substantial biological diversity. The mountains that make up the Trans-Mexican Volcanic Belt are a hypothesized biogeographic barrier for the terrestrial fauna found in the region. Several phylogeographic studies have provided genetic evidence in support of this historical narrative; however, the species examined represent a small percentage of the diversity found in this part of Mexico. Thus, additional studies are needed to identify concordant phylogeographic patterns and infer the historic species composition of particular ecoregions. In this study we investigated genetic variation in the Lowland Burrowing Treefrog, Smilisca fodiens, a species that occurs on both sides of the Trans-Mexican Volcanic Belt. We used mitochondrial (12S and 16S ribosomal subunits; 1039 base pairs [bp]) and nuclear (tyrosinase precursor; 513 bp) DNA to perform phylogenetic analyses on frogs from several localities in Mexico. Mitochondrial DNA supported two well-defined clades that correspond to populations found north and south of the Trans-Mexican Volcanic Belt, respectively. These analyses of matrilineal lineages also found higher levels of genetic diversity south of the Trans-Mexican Volcanic Belt. Although our nuclear DNA analysis did not reveal a phylogeographic split at the Trans-Mexican Volcanic Belt, we observed higher genetic variation among our southern samples, similar to the mitochondrial analyses. Our results are consistent with studies in other sympatric taxa that propose the Trans-Mexican Volcanic Belt as a biogeographic barrier. Additionally, our results suggest recent northern range expansion of S. fodiens. We suggest retaining S. fodiens as a single species until future work can clarify the amount and direction of gene flow between the mitochondrial clades.