Sea Snake Research Articles

Sea snakes lose their stripes to deal with pollution

Melanin pigment in darkened skin binds to pollutants and helps animals rid themselves of chemicals.

A new subspecies of sea snake, Hydrophis platurus xanthos, from Golfo Dulce, Costa Rica.

We describe a distinctive new subspecies of sea snake from the occasionally anoxic inner-basin waters of Golfo Dulce, Costa Rica, based on combined data garnered between 2010 and 2017 for 154 specimens, 123 free-ranging and 31 museum-held. The yellow sea snake, Hydrophis platurus xanthos Bessesen & Galbreath, subsp. n., is diagnosed by a notably smaller body size and nearly uniform yellow coloration, which contrasts with the black and yellow striae and tail spots or bands typical of the species. Within the modest geographic range (circa 320 km2), nearly all specimens possess both diagnostic character states. Bathymetrics appear to restrict genetic flow between this allopatric population and conspecifics in the broader Eastern Pacific. In perspicuous contrast to typical H. platurus, H. p. xanthos shows no association with drift lines, and feeds at night in turbulent waters, assuming a sinusoidal ambush posture never previously reported for the species. This evolutionarily significant unit (ESU) warrants taxonomic recognition and active protection.

Contribution of citizen science to improve knowledge on marine biodiversity in the Gulf Region

Monitoring marine biodiversity is costly and practical solutions have to be implemented to identify species and their preferred habitats, particularly in this era of rapid global change. Citizen science has proven to be effective and with high potential for monitoring efforts, and has been extensively applied to biodiversity. We have used the citizen science approach to engage the general public and stakeholders to contribute improving the current knowledge of sea snake biodiversity in Qatar and the Gulf Region. Logistic regression analysis using demographic data from interview surveys conducted in Qatar has indicated that the people having seen more sea snakes are older than 30years and are Qatari citizens and/or fishermen from India.Of the ten species of sea snakes listed in the literature to be present in the Gulf Region, most of them have been reported for Qatar, Bahrain, United Arab Emirates and Saudi Arabia. However, the number of species present is often assumed based on their occurrence within the Arabian Gulf rather than on actual captures and appropriate identification. The creation of marine reference biological scientific collections to properly identify the species and make accurate biodiversity inventories is an urgent priority for the countries in the Gulf region. To this end, contributions by stakeholders and the general public for this study have proven to be very useful. However a larger networking with local and international scientists and stakeholders is still needed to adequately survey the country’s current biodiversity, identify research priorities and eventually provide the scientific input needed to assist biodiversity management related to renewable resource management and marine conservation in the Arabian Gulf Region.

Venom proteome of the yellow-lipped sea krait, Laticauda colubrina from Bali: Insights into subvenomic diversity, venom antigenicity and cross-neutralization by antivenom

The venom proteome of Laticauda colubrina (Bali, Indonesia) was elucidated by nano-ESI-LCMS/MS of the venom reverse-phase HPLC fractions. Altogether 31 distinct forms of proteins were identified and clustered into three toxin families: three-finger toxin (3FTX, 66.12% of total venom proteins), phospholipase A2 (PLA2, 33.26%) and cysteine-rich secretory protein (CRiSP, 0.05%). The 3FTX were α-neurotoxins (five long neurotoxins, LNTX, 48.87%; two short neurotoxins, SNTX, 16.94%) and a trace amount of two cytotoxins (CTX, 0.31%). PLA2 were present with a large diversity of homologues (≥20 forms), however none was annotated to the lethal proteoform reported previously. The venom is highly lethal in mice (LD50=0.10μg/g) and this is driven primarily by the SNTX and LNTX (LD50=0.05–0.13μg/g), since the PLA2 proteins were non-lethal up to 2μg/g (20-time the venom LD50). The SNTX and LNTX were effectively cross-neutralized by the heterologous Sea Snake Antivenom (SSAV, Australian product) (potency=0.27mg toxin per ml antivenom, and 0.40mg/ml, respectively), corroborating the cross-neutralization of the whole venom (potency=1.09mg/ml) and its antigenic immunoreactivity toward SSAV. Furthermore, compared with earlier studies, the present work reveals geographical variation of venom composition for L. colubrina which may have implication for the evolution and conservation of the species. Biological significanceLaticauda colubrina (yellow-lipped sea krait) is a widely distributed, semi-aquatic venomous snake species. The venom proteome at the level of protein family is unsophisticated and consistent with its restricted prey selection. Nonetheless, the subproteomic findings revealed geographical variability of the venom for this widely distributed species. In contrast to two previous reports, the results for the Balinese L. colubrina venom showed that LNTX Neurotoxin a and Neurotoxin b were co-existent while the PLA2 lethal subtype (PLA-II) was undetected by means of LCMS/MS and by in vivo assay. This is an observable trait of L. colubrina considered divergent from specimens previously studied for the Philippines and the Solomon Islands. The stark geographical variation might be reflective of trophic adaptation following evolutionary arms race between the snake and the prey (eels) in different localities. The preferred trait would likely propagate and remain significant within the geographical population, since the strong behaviour of site fidelity in the species would have minimized gene flow between distant populations. Meanwhile, the in vivo neutralization study verified that the efficacy of the heterologous Sea Snake Antivenom (Australian product) is attributable to the cross-neutralization of SNTX and LNTX, two principal lethal toxins that made up the bulk of L. colubrina venom proteins. The findings also implied that L. colubrina, though could be evolutionarily more related to the terrestrial elapids, has evolved a much streamlined, neurotoxin- and PLA2-predominated venom arsenal, with major antigenicity shared among the true sea snakes and the Australo-Papuan elapids. The findings enrich our current understanding of the complexity of L. colubrina venom and the neutralizing spectrum of antivenom against the principal toxins from this unique elapid lineage.

Northward dispersal of sea kraits (Laticauda semifasciata) beyond their typical range.

Marine reptiles are declining globally, and recent climate change may be a contributing factor. The study of sea snakes collected beyond their typical distribution range provides valuable insight on how climate change affects marine reptile populations. Recently, we collected 12 Laticauda semifasciata (11 females, 1 male) from the waters around southern South Korea—an area located outside its typical distribution range (Japan, China including Taiwan, Philippines and Indonesia). We investigated the genetic origin of Korean specimens by analyzing mitochondrial cytochrome b gene (Cytb) sequences. Six individuals shared haplotypes with a group found in Taiwan-southern Ryukyu Islands, while the remaining six individuals shared haplotypes with a group encompassing the entire Ryukyu Archipelago. These results suggest L. semifasciata moved into Korean waters from the Taiwan-Ryukyu region via the Taiwan Warm Current and/or the Kuroshio Current, with extended survival facilitated by ocean warming. We highlight several contributing factors that increase the chances that L. semifasciata establishes new northern populations beyond the original distribution range.

Postmortem examination of Australian sea snakes ( Hydrophiinae): Anatomy and common pathologic conditions.

There is limited published information about disease in wild sea snakes and no standardized guideline for postmortem examination of sea snakes. Identifying causes of morbidity and mortality of marine vertebrate species has been pivotal to understanding disease factors implicated in stranding events and assisting with the formulation of conservation plans. Additionally, postmortem findings can provide valuable information on life history traits and the ecology of these reclusive species. Sick, moribund, or dead sea snakes are intermittently washed ashore along Australian and international beaches and provide an opportunity to examine a subset of the population and identify causes of population decline. We present an illustrated description of sea snake anatomy and describe a systematic approach to postmortem examination of sea snakes. We describe common pathologic conditions identified from clinical and postmortem examinations of stranded Australian sea snakes from southeast Queensland. Notable pathologic conditions include traumatic injury, inflammatory conditions, parasitic infections, and neoplasia.

Temporal and spatial activity‐associated energy partitioning in free‐swimming sea snakes

Summary Partitioning energy between critical basal functions and activity‐associated behaviours is a primary determinant of animal survival. Consequently, habitat selection is likely to be driven by the efficiency with which resources can be acquired from a heterogeneous energy landscape. Determining how energy partitioning is achieved across temporal and spatial scales is particularly challenging in aquatic animals due to the logistical limitations in estimating field metabolic rates (FMR) while simultaneously examining habitat choice. Here, acoustic telemetry using accelerometers alongside bimodal respirometry were used to correlate vectorial dynamic body acceleration (VeDBA) with oxygen consumption rates () of sea snakes (Hydrophis curtus and Hydrophis elegans) across an ecologically relevant temperature range. Subsequently, VeDBA of free‐roaming snakes was used to estimate activity‐associated FMR within a near‐shore environment over diel, seasonal and spatial scales. Diel changes in activity explained short‐term patterns in FMR, whereas seasonal changes in water temperature drove long‐term patterns. Spatial analyses demonstrated that activity‐associated FMR was elevated in productive seagrass and mudflat habitats, indicative of a concentration of foraging efforts. Our findings illustrate for the first time how sea snakes partition activity‐associated FMR across time and space, providing an approach by which we can monitor the impacts of, and vulnerabilities to, natural and anthropogenic disturbances like warming and trawl fisheries. A lay summary is available for this article.

How the Cobra Got Its Flesh-Eating Venom: Cytotoxicity as a Defensive Innovation and Its Co-Evolution with Hooding, Aposematic Marking, and Spitting.

The cytotoxicity of the venom of 25 species of Old World elapid snake was tested and compared with the morphological and behavioural adaptations of hooding and spitting. We determined that, contrary to previous assumptions, the venoms of spitting species are not consistently more cytotoxic than those of closely related non-spitting species. While this correlation between spitting and non-spitting was found among African cobras, it was not present among Asian cobras. On the other hand, a consistent positive correlation was observed between cytotoxicity and utilisation of the defensive hooding display that cobras are famous for. Hooding and spitting are widely regarded as defensive adaptations, but it has hitherto been uncertain whether cytotoxicity serves a defensive purpose or is somehow useful in prey subjugation. The results of this study suggest that cytotoxicity evolved primarily as a defensive innovation and that it has co-evolved twice alongside hooding behavior: once in the Hemachatus + Naja and again independently in the king cobras (Ophiophagus). There was a significant increase of cytotoxicity in the Asian Naja linked to the evolution of bold aposematic hood markings, reinforcing the link between hooding and the evolution of defensive cytotoxic venoms. In parallel, lineages with increased cytotoxicity but lacking bold hood patterns evolved aposematic markers in the form of high contrast body banding. The results also indicate that, secondary to the evolution of venom rich in cytotoxins, spitting has evolved three times independently: once within the African Naja, once within the Asian Naja, and once in the Hemachatus genus. The evolution of cytotoxic venom thus appears to facilitate the evolution of defensive spitting behaviour. In contrast, a secondary loss of cytotoxicity and reduction of the hood occurred in the water cobra Naja annulata, which possesses streamlined neurotoxic venom similar to that of other aquatic elapid snakes (e.g., hydrophiine sea snakes). The results of this study make an important contribution to our growing understanding of the selection pressures shaping the evolution of snake venom and its constituent toxins. The data also aid in elucidating the relationship between these selection pressures and the medical impact of human snakebite in the developing world, as cytotoxic cobras cause considerable morbidity including loss-of-function injuries that result in economic and social burdens in the tropics of Asia and sub-Saharan Africa.

Importance of Shallow Tidal Habitats as Refugia from Trawl Fishing for Sea Snakes

Abstract Sea snakes are an important component of bycatch in commercial and small-scale trawl fisheries in tropical waters and are highly vulnerable to fishing-related mortality. Extensive boat-based surveys were conducted to investigate the assemblage and abundance of sea snakes within a protected shallow coastal bay adjacent to productive trawl fishing grounds. Spine-Bellied Sea Snakes, Hydrophis curtus (previously Lapemis curtus), and Elegant Sea Snakes, Hydrophis elegans, were the most commonly encountered species. Based on the age structure of these two species, the bay was used primarily by juveniles. Temporal trends in age structure and sex ratios showed that H. curtus may use Cleveland Bay as a nursery ground, with gravid females entering the bay in summer months to give birth. In contrast, H. elegans appears to use the bay more consistently through the year, with ∼30% of individuals being adults. This study also showed that shallow tidal habitats, too shallow for trawl fishing, are regularly used...

Evidence for Control of Cutaneous Oxygen Uptake in the Yellow-Lipped Sea KraitLaticauda colubrina(Schneider, 1799)

Abstract Some sea snakes and sea kraits (family Elapidae) can dive for upward of two hours while foraging or feeding, largely because they are able to absorb a significant percentage of their oxygen demand across their skin surfaces. Although cutaneous oxygen uptake is a common adaptation in marine elapids, whether its uptake can be manipulated in response to conditions that might alter metabolic rate is unclear. Our data strongly suggest that Yellow-Lipped Sea Kraits, Laticauda colubrina (Schneider, 1799), can modify cutaneous uptake in response to changing pulmonary oxygen saturation levels. When exposed to stepwise 20% decreases in aerial oxygen saturation from 100% to 40%, Yellow-Lipped Sea Kraits spent more time emerged but breathed less frequently. A significant graded increase in cutaneous uptake was seen between 100% and 60% saturation, likely attributable to subcutaneous capillary recruitment. The additional increase in oxygen uptake between 60% and 40% was not significant, indicating capillary r...

Hydrostatin-TL1, an Anti-Inflammatory Active Peptide from the Venom Gland of Hydrophis cyanocinctus in the South China Sea.

Tumor necrosis factor (TNF)-α is a pleiotropic cytokine with intense pro-inflammatory and immunomodulatory properties, and anti-TNF-α biologics are effective therapies for various inflammatory diseases such as inflammatory bowel disease (IBD) and sepsis. Snake venom, as a traditional Chinese medicine, has been used in the treatment of inflammatory diseases in China for centuries. In this research, we constructed a venom gland T7 phage display library of the sea snake Hydrophis cyanocinctus to screen bioactive compounds that antagonize TNF-α and identified a novel nine-amino-acid peptide, termed hydrostatin-TL1 (H-TL1). In enzyme-linked immunosorbent assay (ELISA) and surface plasmon resonance (SPR) analyses, H-TL1 inhibited the interaction between TNF-α and TNF receptor 1 (TNFR1). Further, H-TL1 attenuated the cytotoxicity of TNF-α in L929 cells as determined by the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) assay. H-TL1 also decreased the mRNA expression of TNF-α/TNFR1 downstream targets and suppressed the phosphorylation of well-characterized proteins of downstream signal transduction pathways in HEK-293 cells. In vivo data demonstrated that H-TL1 protects animals against dextran sodium sulfate (DSS)-induced acute colitis and lipopolysaccharide (LPS)-induced acute shock. Given its significant anti-inflammatory activity in vitro and in vivo, H-TL1 is a potential peptide for the development of new agents to treat TNF-α-associated inflammatory diseases.

Rapid Radiations and the Race to Redundancy: An Investigation of the Evolution of Australian Elapid Snake Venoms.

Australia is the stronghold of the front-fanged venomous snake family Elapidae. The Australasian elapid snake radiation, which includes approximately 100 terrestrial species in Australia, as well as Melanesian species and all the world’s true sea snakes, may be less than 12 million years old. The incredible phenotypic and ecological diversity of the clade is matched by considerable diversity in venom composition. The clade’s evolutionary youth and dynamic evolution should make it of particular interest to toxinologists, however, the majority of species, which are small, typically inoffensive, and seldom encountered by non-herpetologists, have been almost completely neglected by researchers. The present study investigates the venom composition of 28 species proteomically, revealing several interesting trends in venom composition, and reports, for the first time in elapid snakes, the existence of an ontogenetic shift in the venom composition and activity of brown snakes (Pseudonaja sp.). Trends in venom composition are compared to the snakes’ feeding ecology and the paper concludes with an extended discussion of the selection pressures shaping the evolution of snake venom.

Chinese sea snake (Laticauda semifasciata) misidentified as slender-necked sea snake in previous published account in Korea

Recent ocean warming near the Korean peninsula and our lack of knowledge of an important vertebrate group, the sea snakes, encouraged us to clarify this part of Korea’s regional fauna. We re-examined photographs that had been used to report the slender-necked sea snake (Hydrophis melanocephalus) in 1995. We discovered it was misidentified. To determine the correct identity of the sea snake, we studied 13 original photographs taken at the collecting site in Sooyoung Bay, Busan-si, in 1995 and determined the snake to be Laticauda semifasciata based on enlarged ventral scales, definitive for Laticaudinae sea snakes, and internasal scales, pale blue body color, divided rostral scale, and evident “V”-shaped stripes on the body trunk, definitive for L. semifasciata. Therefore, the snake caught 30 years ago in Korean waters should be considered the first record of a Laticaudinae sea snake in Korean waters. L. semifasciata is listed as near threatened setting the stage for urgently needed studies of sea snakes in Korea and supporting those currently underway.

Sea snakes (Elapidae, Hydrophiinae) in their westernmost extent: an updated and illustrated checklist and key to the species in the Persian Gulf and Gulf of Oman.

The Persian Gulf is known as the westernmost distribution limit for sea snakes, except for Hydrophis platurus (Linnaeus, 1766) that reaches southeastern Africa. Previous identification guides for sea snakes of the Persian Gulf and its adjacent waters in the Gulf of Oman were based on old data and confined mostly to written descriptions. Therefore, a series of field surveys were carried out in 2013 and 2014 through Iranian coastal waters of both gulfs to provide a comprehensive sampling of sea snakes in the area. This paper presents an illustrated and updated checklist and identification tool for sea snakes in the Persian Gulf and Gulf of Oman, which are based on new material and a review of the literature. This checklist includes ten species of marine hydrophiines, of which one, Microcephalophis cantoris (Günther, 1864), is a new record for the area. All specimens examined herein are deposited and available at the Zoological Museum of Shahid Bahonar University of Kerman, Kerman province, Iran.

The toxinology of sea snakes: A systematic review

The toxinology of sea snakes: A systematic review

Oceanic circulation models help to predict global biogeography of pelagic yellow-bellied sea snake.

It is well recognized that most marine vertebrates, and especially tetrapods, precisely orient and actively move in apparently homogeneous oceanic environments. Here, we investigate the presumptive role of oceanic currents in biogeographic patterns observed in a secondarily marine tetrapod, the yellow-bellied sea snake (Hydrophis [Pelamis] platurus). State-of-the-art world ocean circulation models show how H. platurus, the only pelagic species of sea snake, can potentially exploit oceanic currents to disperse and maintain population mixing between localities that spread over two-thirds of the Earth's circumference. The very close association of these snakes with surface currents seems to provide a highly efficient dispersal mechanism that allowed this species to range extensively and relatively quickly well beyond the central Indo-Pacific area, the centre of origin, abundance and diversity of sea snakes. Our results further suggest that the pan-oceanic population of this species must be extraordinarily large.

Venomic Analysis of the Poorly Studied Desert Coral Snake, Micrurus tschudii tschudii, Supports the 3FTx/PLA₂ Dichotomy across Micrurus Venoms.

The venom proteome of the poorly studied desert coral snake Micrurus tschudii tschudii was unveiled using a venomic approach, which identified ≥38 proteins belonging to only four snake venom protein families. The three-finger toxins (3FTxs) constitute, both in number of isoforms (~30) and total abundance (93.6% of the venom proteome), the major protein family of the desert coral snake venom. Phospholipases A2 (PLA2s; seven isoforms, 4.1% of the venom proteome), 1–3 Kunitz-type proteins (1.6%), and 1–2 l-amino acid oxidases (LAO, 0.7%) complete the toxin arsenal of M. t. tschudii. Our results add to the growing evidence that the occurrence of two divergent venom phenotypes, i.e., 3FTx- and PLA2-predominant venom proteomes, may constitute a general trend across the cladogenesis of Micrurus. The occurrence of a similar pattern of venom phenotypic variability among true sea snake (Hydrophiinae) venoms suggests that the 3FTx/PLA2 dichotomy may be widely distributed among Elapidae venoms.

Revisiting Notechis scutatus venom: on shotgun proteomics and neutralization by the “bivalent” Sea Snake Antivenom

Recent advances in proteomics enable deep profiling of the compositional details of snake venoms for improved understanding on envenomation pathophysiology and immunological neutralization. In this study, the venom of Australian tiger snake (Notechis scutatus) was trypsin-digested in solution and subjected to nano-ESI-LCMS/MS. Applying a relative quantitative proteomic approach, the findings revealed a proteome comprising 42 toxin subtypes clustered into 12 protein families. Phospholipases A2 constitute the most abundant toxins (74.5% of total venom proteins) followed by Kunitz serine protease inhibitors (6.9%), snake venom serine proteases (5.9%), alpha-neurotoxins (5.6%) and several toxins of lower abundance. The proteome correlates with N. scutatus envenoming effects including pre-synaptic and post-synaptic neurotoxicity and consumptive coagulopathy. The venom is highly lethal in mice (intravenous median lethal dose=0.09μg/g). BioCSL Sea Snake Antivenom, raised against the venoms of beaked sea snake (Hydrophis schistosus) and N. scutatus (added for enhanced immunogenicity), neutralized the lethal effect of N. scutatus venom (potency=2.95mg/ml) much more effectively than the targeted H.schistosus venom (potency=0.48mg/ml). The combined venom immunogen may have improved the neutralization against phospholipases A2 which are abundant in both venoms, but not short-neurotoxins which are predominant only in H. schistosus venom. SignificanceA shotgun proteomic approach adopted in this study revealed the compositional details of the venom of common tiger snake from Australia, Notechis scutatus. The proteomic findings provided additional information on the relative abundances of toxins and the detection of proteins of minor expression unreported previously. The potent lethal effect of the venom was neutralized by bioCSL Sea Snake Antivenom, an anticipated finding due to the fact that the Sea Snake Antivenom is actually bivalent in nature, being raised against a mix of venoms of the beaked sea snake (Hydrophis schistosus) and N. scutatus. However, it is surprising to note that bioCSL Sea Snake Antivenom neutralized N. scutatus venom much more effectively compared to the targeted sea snake venom by a marked difference in potency of approximately 6-fold. This phenomenon may be explained by the main difference in the proteomes of the two venoms, where H. schistosus venom is dominated by short-neurotoxins in high abundance – this is a poorly immunogenic toxin group that has been increasingly recognized in the venoms of a few cobras. Further investigations should be directed toward strategies to improve the neutralization of short-neurotoxins, in line with the envisioned production of an effective pan-regional elapid antivenom.

The evolution of scale sensilla in the transition from land to sea in elapid snakes

Scale sensilla are small tactile mechanosensory organs located on the head scales of many squamate reptiles (lizards and snakes). In sea snakes and sea kraits (Elapidae: Hydrophiinae), these scale organs are presumptive scale sensilla that purportedly function as both tactile mechanoreceptors and potentially as hydrodynamic receptors capable of sensing the displacement of water. We combined scanning electron microscopy, silicone casting of the skin and quadrate sampling with a phylogenetic analysis to assess morphological variation in sensilla on the postocular head scale(s) across four terrestrial, 13 fully aquatic and two semi-aquatic species of elapids. Substantial variation exists in the overall coverage of sensilla (0.8–6.5%) among the species sampled and is broadly overlapping in aquatic and terrestrial lineages. However, two observations suggest a divergent, possibly hydrodynamic sensory role of sensilla in sea snake and sea krait species. First, scale sensilla are more protruding (dome-shaped) in aquatic species than in their terrestrial counterparts. Second, exceptionally high overall coverage of sensilla is found only in the fully aquatic sea snakes, and this attribute appears to have evolved multiple times within this group. Our quantification of coverage as a proxy for relative ‘sensitivity’ represents the first analysis of the evolution of sensilla in the transition from terrestrial to marine habitats. However, evidence from physiological and behavioural studies is needed to confirm the functional role of scale sensilla in sea snakes and sea kraits.

First Record of Laticauda semifasciata (Reptilia: Squamata: Elapidae: Laticaudinae) from Korea

The Chinese sea snake Laticauda semifasciata (Reinwardt in Schlegel, 1837) is newly reported from Korean waters based on three specimens collected from Jeju Island, Korea, in August, September, and November 2015. This is the first time that the genus Laticauda and subfamily Laticaudinae has been reported from Korean waters. The subfamily Laticaudinae has ventrals that are four to five times wider than the adjacent dorsals, which are unlike the ventrals that are similar or up to two times wider than adjacent dorsals in the subfamily Hydrophiinae. Laticauda semifasciata is distinct from other species because it has three prefrontals and its rostrals are horizontally divided into two. As the result of this report, four species (L. semifasciata, Hydrophis (Pelamis) platurus, Hydrophis cyanocinctus, and H. melanocephalus) of sea snakes have been reported in Korean waters.