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.     

Moving in two worlds: aquatic and terrestrial locomotion in sea snakes (Laticauda colubrina,Laticaudidae)

Yellow‐lipped sea kraits (Laticauda colubrina) are amphibious in their habits. We measured their locomotor speeds in water and on land to investigate two topics: (1) to what degree have adaptations to increase swimming speed (paddle‐like tail etc.) reduced terrestrial locomotor ability in sea kraits?; and (2) do a sea krait’s sex and body size influence its locomotor ability in these two habitats, as might be expected from the fact that different age and sex classes of sea kraits use the marine and terrestrial environments in different ways? To estimate ancestral states for locomotor performance, we measured speeds of three species of Australian terrestrial elapids that spend part of their time foraging in water. The evolutionary modifications of Laticauda for marine life have enhanced their swimming speeds by about 60%, but decreased their terrestrial locomotor speed by about 80%. Larger snakes moved faster than smaller individuals in absolute terms but were slower in terms of body lengths travelled per second, especially on land. Male sea kraits were faster than females (independent of the body‐size effect), especially on land. Prey items in the gut reduced locomotor speeds both on land and in water. Proteroglyphous snakes may offer exceptional opportunities to study phylogenetic shifts in locomotor ability, because (1) they display multiple independent evolutionary shifts from terrestrial to aquatic habits, and (2) one proteroglyph lineage (the laticaudids) displays considerable intraspecific and interspecific diversity in terms of the degree to which they use terrestrial vs. aquatic habitats.     

Habitat selection by sea kraits (Laticauda spp.) at coastal sites of Orchid Island, Taiwan

Three species of amphibious sea kraits (Laticauda spp.) spend variable time at sea and require fresh water for water balance. Both the rate of cutaneous evaporative water loss and the extent of terrestriality are known to differ among them. Laticauda semifasciata has the greatest rate of water loss and the least extent of terrestriality, whereas L. colubrina exhibits the reverse and L. laticaudata is intermediate. These sea kraits tend to be more abundant at places where there are sources of fresh water, but other factors also influence their distribution. To further clarify the habitat requirements, we investigated the abundance of each species of sea krait at six different habitats and the availability of each type of habitat on Orchid Island, Taiwan. The six habitats were high coral reef without fresh water (HR) and with fresh water (HRF); low coral reef without fresh water (LR) and with fresh water (LRF); sand or gravel coast, which has no coral reef, without fresh water (NR) and with fresh water (NRF). The extent of safety judged from the relative availability of retreat sites, from high to low, was HR, LR, and NR among these habitats. More than 75% of individuals counted for each species were found in HRF. We found no sea kraits in NRF and NR. The most available habitat was LR, but no L. laticaudata or L. semifasciata were found in this habitat. We found 3.3% and 16.7% of L. colubrina in LR and HR, respectively. For L. colubrina, the second abundant habitat was HR, whereas for L. laticaudata and L. semifasciata, the second abundant habitat was LRF. We conclude that both safety (availability of retreat sites) and fresh water are important to the habitat selection of sea kraits. Compared with other species, L. colubrina is characterized by a greater extent of terrestrial habit and possibly greater variety of access to sources of fresh water.     

Abundance of sea kraits correlates with precipitation

Recent studies have shown that sea kraits (Laticauda spp.)--amphibious sea snakes--dehydrate without a source of fresh water, drink only fresh water or very dilute brackish water, and have a spatial distribution of abundance that correlates with freshwater sites in Taiwan. The spatial distribution correlates with sites where there is a source of fresh water in addition to local precipitation. Here we report six years of longitudinal data on the abundance of sea kraits related to precipitation at sites where these snakes are normally abundant in the coastal waters of Lanyu (Orchid Island), Taiwan. The number of observed sea kraits varies from year-to-year and correlates positively with previous 6-mo cumulative rainfall, which serves as an inverse index of drought. Grouped data for snake counts indicate that mean abundance in wet years is nearly 3-fold greater than in dry years, and this difference is significant. These data corroborate previous findings and suggest that freshwater dependence influences the abundance or activity of sea kraits on both spatial and temporal scales. The increasing evidence for freshwater dependence in these and other marine species have important implications for the possible impact of climate change on sea snake distributions.     

Phylogenetic relationships within laticaudine sea snakes (Elapidae)

The sea snake subfamily Laticaudinae consists of a single genus with eight named species, based on morphological characters. We used microsatellite and mitochondrial DNA (mtDNA) data to clarify the adaptive radiation of these oviparous sea snakes in the South Pacific, with special reference to New Caledonia and Vanuatu. A mitochondrial DNA data set (ND4 gene 793 bp) was obtained from 345 individuals of the five species of Laticauda sp. sea snakes endemic to the region. Maximum likelihood and Bayesian approaches yielded the same optimal tree topology, identifying two major clades (yellow-banded and blue-banded sea snakes). Although all laticaudine sea snakes rely on small islands as oviposition sites, the two lineages differ in their use of marine vs. terrestrial habitats. A highly aquatic species (Laticauda laticaudata) shows a strong pattern of genetic isolation by distance, implying that the patchy distribution of terrestrial habitats has had little impact on gene flow. The more terrestrial clade (Laticauda colubrina, Laticauda frontalis, Laticauda guineai, Laticauda saintgironsi) shows stronger geographic differentiation in allelic frequencies, associated with island groups rather than with geographic distance. Microsatellites and mtDNA suggest that L. frontalis (restricted to Vanuatu) represents a recent founder-induced speciation event, from allopatric migrants of the New Caledonian taxon L. saintgironsi. A major divergence in speciation patterns between the two major clades of laticaudine snakes thus correlates with (and perhaps, is driven by) differences in the importance of terrestrial habitats in the species' ecology.     

Terrestrial locomotion in sea snakes: the effects of sex and species on cliff-climbing ability in sea kraits (Serpentes, Elapidae, Laticauda)

Ecomorphological theory predicts a match between an organism's environment and its locomotor abilities, such that animals function most effectively under the conditions they experience in nature. However, amphibious species must simultaneously optimize performance in two different habitats posing incompatible demands on locomotor morphology and physiology. This situation may generate a mismatch between environment and locomotor function, with performance optimized only for the more important habitat type; alternatively, selection may fine-tune locomotor abilities for both types of challenges. Two species of sea kraits in New Caledonia offer an opportunity to examine this question: Laticauda laticaudata is more highly aquatic than L. colubrina , and males are more terrestrial than females within each taxon. We examined an aspect of locomotor performance that is critical to coming ashore on steep-walled rocky islets: the ability to climb steep cliffs. We also measured the muscular strength of these animals, a character that is likely critical to climbing performance. Laticauda colubrina was heavier-bodied and stronger (even relative to its body mass) than the more aquatic L. laticaudata ; and within each species, males were heavier-bodied and stronger than females. The same patterns were evident in cliff-climbing ability. Thus, the ability of different species and sexes of sea kraits to climb steep cliffs correlates with their body shape even though these primarily aquatic animals use terrestrial habitats only rarely.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 433–441.     

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.     

Sexual divergence in diets and morphology in Fijian sea snakes Laticauda colubrina (Laticaudinae)

In the Fiji Islands, female yellow‐lipped sea kraits (Laticauda colubrina) grow much larger than males, and have longer and wider heads than do conspecific males of the same body length. This morphological divergence is accompanied by (and may be adaptive to) a marked sex divergence in dietary habits. Adult female sea kraits feed primarily on large conger eels, and take only a single prey item per foraging bout. In contrast, adult males feed upon smaller moray eels, and frequently take multiple prey items. Prey size increases with snake body size in both males and females, but the sexes follow different trajectories in this respect. Female sea kraits consume larger eels relative to predator head size and body length than do males. Thus, the larger relative head size of female sea kraits is interpreted as an adaptation to consuming larger prey items. Our results are similar to those of previous studies on American water snakes (natricines) and Australian file snakes (acrochordids), indicating that similar patterns of sex divergence in dietary habits and feeding structures have evolved convergently in at least three separate lineages of aquatic snakes.     

Comparison of freshwater discrimination ability in three species of sea kraits (Laticauda semifasciata, L. laticaudata and L. colubrina)

Three species of amphibious sea kraits (Laticauda spp.) require drinking freshwater to regulate water balance. The extent of terrestriality is known to differ among them. Species with higher extent of terrestriality would drink freshwater accumulated on land, whereas less terrestrial species would rely totally on freshwater that runs into the sea. Consequently, we predicted that the latter species might have a better ability to follow the flow of freshwater or lower salinity water in the sea than the former. We investigated the freshwater discrimination ability of three sea krait species, using a Y-maze apparatus. We found that Laticauda semifasciata and Laticauda laticaudata, less terrestrial species, followed freshwater significantly more frequently than seawater, whereas Laticauda colubrina, more terrestrial species, unbiasedly selected freshwater and seawater. This result supports our prediction and suggests that less terrestrial sea kraits more efficiently access freshwater sources in the sea than highly terrestrial sea kraits. It is likely that behavioral rehydration systems vary among sea kraits in relation to their terrestrial tendency.     

First records of sea snakes (Elapidae: Hydrophiinae) diving to the mesopelagic zone (>200 m)

Viviparous sea snakes (Elapidae: Hydrophiinae) are fully marine reptiles distributed in the tropical and subtropical waters of the Indian and Pacific Oceans. Their known maximum diving depth ranges between 50 and 100 m and this is thought to limit their ecological ranges to shallow habitats. We report two observations, from industry‐owned remotely operated vehicles, of hydrophiine sea snakes swimming and foraging at depths of approximately 250 m in the Browse Basin on Australia's North West Shelf, in 2014 and 2017. These observations show that sea snakes are capable of diving to the dim‐lit, cold‐water mesopelagic zone, also known as the ‘twilight’ zone. These record‐setting dives raise new questions about the thermal tolerances, diving behaviour and ecological requirements of sea snakes. In addition to significantly extending previous diving records for sea snakes, these observations highlight the importance of university‐industry collaboration in surveying understudied deep‐sea habitats.     

Reproductive isolating mechanisms between two sympatric sibling species of sea snakes

Mechanisms that maintain species isolation within sympatric congeners have attracted analysis in many kinds of organisms, but not in snakes. We studied two sibling species of amphibious sea snakes (Laticauda colubrina and L. frontalis) on the island of Efate, in the Pacific Ocean republic of Vanuatu. The two taxa are almost identical morphologically, except that L. colubrina grows much larger than L. frontalis. No natural hybrids have been reported, and geographic distributions of the two taxa suggest the possibility of sympatric speciation. Our fieldwork shows that the two taxa are often syntopic and overlap in breeding seasons. Behavioral studies in outdoor arenas show that the separation between these two taxa is maintained by species-specific cues that control male courtship. Males of both species courted conspecific females but not heterospecific females. The proximate mechanism driving this separation involves chemical cues. Adult females of both taxa possess distinctive lipids in the skin. Males directed courtship behavior (chin-pressing) to hexane-extracted samples of lipids from conspecific but not heterospecific females. Males of the dwarf species (L frontalis) were more selective courters than were those of the larger taxon (L. colubrina), perhaps because a preference for courting larger females means that L. colubrina males would be unlikely to court L. frontalis-sized (i.e., small) females even in the absence of pheromonal barriers.     

Fine scale site fidelity in sea kraits: implications for conservation

The shores of coral reef islands are major sites for biodiversity, but unfortunately they are also subject to strong anthropogenic disturbances. Indeed vast arrays of organisms live exclusively in these very narrow and well structured zones, many others depend on the rich and diverse micro-habitats for essential part of their life cycle (to reproduce, forage, etc.). Sea kraits are sea snakes that depend on the shore of coral islets; they forage at sea but digest, reproduce and rest on land. They have been killed in extremely large numbers in many places, causing local extinctions. In the current study we demonstrate through recapture and translocation studies that these snakes exhibit a strong and fine-scale fidelity for particular segments of the shore. Consequently, these specific areas should be under strong protection, as it the case for the breeding beaches used by marine mammals, birds or turtles.     

Effects of oceanic salinity on body condition in sea snakes

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-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 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.     

Microsatellite loci for laticaudine sea kraits

We report the development of 11 polymorphic microsatellite loci (three dinucleotides, one trinucleotide and seven tetranucleotides) that are useful for the detection of population subdivision and the study of philopatry, migration and mating biology in laticaudine sea kraits Laticauda saintgironsi and Laticauda laticaudata. Five loci are highly polymorphic and amplify reliably in both L. saintgironsi and L. laticaudata. An additional three are useful in L. saintgironsi and another three in L. laticaudata.     

Amino acid sequences of two novel long-chain neurotoxins from the venom of the sea snake Laticauda colubrina.

From the venom of a population of the sea snake Laticauda colubrina from the Solomon Islands, a neurotoxic component, Laticauda colubrina a (toxin Lc a), was isolated in 16.6% (A280) yield. Similarly, from the venom of a population of L. colubrina from the Philippines, a neurotoxic component, Laticauda colubrina b (toxin Lc b), was obtained in 10.0% (A280) yield. The LD50 values of these toxins were 0.12 microgram/g body wt. on intramuscular injection in mice. Toxins Lc a and Lc b were each composed of molecules containing 69 amino acid residues with eight half-cystine residues. The complete amino acid sequences of these two toxins were elucidated. Toxins Lc a and Lc b are different from each other at five positions of their sequences, namely at positions 31 (Phe/Ser), 32 (Leu/Ile), 33 (Lys/Arg), 50 (Pro/Arg) and 53 (Asp/His) (residues in parentheses give the residues in toxins Lc a and Lc b respectively). Toxins Lc a and Lc b have a novel structure in that they have only four disulphide bridges, although the whole amino acid sequences are homologous to those of other known long-chain neurotoxins. It is remarkable that toxins Lc a and Lc b are not coexistent at the detection error of 6% of the other toxin. Populations of Laticauda colubrina from the Solomon Islands and from the Philippines have either toxin Lc a or toxin Lc b and not both of them.     

Long-term field study of sea kraits in New Caledonia: fundamental issues and conservation

This short review focuses on the findings associated with a long-term field study on two species of sea kraits in New Caledonia. Since 2002, more than 30 sites in the lagoon have been sampled, and in most places mark-recapture was implemented. We collected detailed data on more than 14,000 marked individuals (>6000 recaptures) and used different techniques (stable isotopes, bio-logging, analyses of diet). The objective was fundamental: to examine how amphibious snakes cope with both terrestrial and aquatic environments. As access to abundant food is likely the main evolutionary driver for the return transition toward the sea in marine tetrapods, foraging ecology was an important part of the research and novel information was obtained on this subject. Rapidly however, field observations revealed the potential interest of sea kraits for conservation issues. Our results show that these snakes are useful bio-indicators of marine biodiversity; they also provide a useful signal to monitor levels of contamination by heavy metals in the lagoon, and more generally as a means of studying the functioning of reef ecosystems. Importantly, anecdotal observations (e.g., a krait drinking during rain) provided unsuspected physiological insights of general importance to fundamental problems and conservation. One of the lessons of this long-term study is that key results emerged in an unexpected way, but all were dependent on intensive field work.     

Fingerprint correspondence of hemoglobins and the relationships of sea snakes.

1. Peptide fingerprints of tryptic digests of the globins of sea snake species of Hydrophis, Pelamis, Aipysurus, Laticauda and the terrestrial elapid Naja were compared. 2. Globin divergence, as estimated from peptide fingerprints, paralleled closely transferrin divergence, as measured immunologically. 3. Taxonomic affinities, suggested by the fingerprint data, are concordant with McDowell's taxonomic system for sea snakes with the following exceptions: (a) Laticauda shows a closer affinity to the true sea snakes than to the terrestrial elapid Naja. (b) Sea snakes appear to be more widely divergent from terrestrial elapids than his scheme suggests.     

Conflicts between feeding and reproduction in amphibious snakes (sea kraits,Laticauda spp.)

If reproduction impairs an organism's ability to perform other fitness‐related activities, natural selection may favour behavioural adjustments to minimize these conflicts. This is presumably the reason why many animals are anorexic during the breeding season. We studied amphibious sea snakes, a group whose ecology facilitates teasing apart the causal links between reproduction and feeding. In both Laticauda laticaudata and L. saintgironsi in New Caledonia, adult females cease feeding as their eggs develop. The advantages of foregoing feeding do not relate to thermoregulation (because foraging does not entail lower body temperatures), nor are they attributable to physical constraints on abdominal volume (because in a snake's linear body, there is little overlap between the stomach and the oviducts). Instead, female sea kraits appear to cease feeding because their bodily distension impedes locomotor ability, rendering them less effective at foraging and more vulnerable to aquatic predators.     

Phylogeny of Australasian venomous snakes (Colubroidea, Elapidae, Hydrophiinae) based on phenotypic and molecular evidence

Scanlon, John D. & Lee, Michael S. Y. (2004). Phylogeny of Australasian venomous snakes (Colubroidea, Elapidae, Hydrophiinae) based on phenotypic and molecular evidence. — Zoologica Scripta , 33 , 335–366.
Phylogenetic relationships among Hydrophiinae (Australasian and marine elapid snakes) are inferred using 87 characters from external, skeletal, hemipenial and internal anatomy, ecology, and chromosomes as well as available sequences of two mitochondrial genes (cytochrome b and 16S rRNA). Parsimony analysis of the combined data retrieves many widely accepted clades; while observed bootstrap or branch (Bremer) support for these is often weak, most have never been corroborated previously by a rigorous numerical analysis. Sea kraits ( Laticauda ) and Solomon Islands elapids are basal to the remaining hydrophiines (Australian terrestrial forms and hydrophiin sea snakes). The latter clade includes three main lineages: a large-bodied oviparous lineage, a small-bodied oviparous lineage, and a viviparous lineage (which also includes the hydrophiin sea snakes, strongly reaffirmed as monophyletic). While the Solomons retain a relictual fauna, New Guinea has less endemism and has been invaded multiple times by Australian lineages, so there is no clear 'stepping stone' pattern supporting a northern (Asian, rather than Gondwanan) biogeographical origin.     

The influence of natural selection and sexual selection on the tails of sea-snakes (Laticauda colubrina)

Many phenotypic traits perform more than one function, and so can influence organismal fitness in more than one way. Sexually dimorphic traits offer an exceptional opportunity to clarify such complexity, especially if the trait involved is subject to natural as well as sexual selection, and if the sexes differ in ecology as well as reproductive behaviour. Relative tail length in sea-snakes fulfils these conditions. Our field studies on a Fijian population of yellow-lipped sea kraits ( Laticauda colubrina ) show that relative tail lengths in male sea kraits have strong consequences for individual fitness, both via natural and sexual selection. Males have much longer tails (relative to snout-vent length) than do females. Mark-recapture studies revealed a trade-off between growth and survival: males with relatively longer tails grew more slowly, but were more likely to survive, than were shorter-tailed males. A male snake's tail length relative to body length influenced not only his growth rate and probability of survival, but also his locomotor ability and mating success. Relative tail length in male sea kraits was thus under a complex combination of selective forces. These forces included directional natural selection (through effects on survival, growth and swimming speed) as well as stabilizing natural selection (males with average-length tails swam faster) and stabilizing sexual selection (males with average-length tails obtained more matings). In contrast, our study did not detect significant selection on relative tail length in females. This sex difference may reflect the fact that females use their tails primarily for swimming, whereas males also must frequently use the tail in terrestrial locomotion and in courtship as well as for swimming.