Marine Snakes Research Articles

Marine snake fossil prompts reclassification of ancient species

Marine snake fossil prompts reclassification of ancient species

Into the Deep: Diving Record for the Dice Snake Natrix tessellata (Laurenti, 1768) in Lake Orta, NW Italy

Many snakes live close to water, with several groups displaying morphological, physiological, or behavioral adaptions to aquatic environments. Although marine snakes have been found at depths beyond 200 m, freshwater snakes are rarely reported at depths larger than a few meters. Here we report freshwater depth records for the dice snake Natrix tessellata, an aquatic snake belonging to the family Natricidae. Dice snake was observed at depths down to 17 m, including in habitats below the thermocline, in Lake Orta (Northern Italy). These observations open new perspectives related to the biology and physiology of Palearctic freshwater snakes belonging to the family Natricidae.

The adaptive significance of large size at birth in marine snakes.

Evolutionary shifts from one habitat type to another can clarify selective forces that affect life-history attributes. Four lineages of snakes (acrochordids and three clades within the Elapidae) have invaded marine habitats, and all have larger offspring than do terrestrial snakes. Predation by fishes on small neonates offers a plausible selective mechanism for that shift, because ascending to breathe at the ocean surface exposes a marine snake to midwater predation whereas juvenile snakes in terrestrial habitats can remain hidden. Consistent with this hypothesis, snake-shaped models moving through a coral-reef habitat in New Caledonia attracted high rates of attack by predatory fishes, and small models (the size of neonatal terrestrial snakes) were attacked more frequently than were large models (the size of neonatal sea snakes). Vulnerability to predatory fishes may have imposed strong selection for increased offspring size in marine snakes.

Polyphyly of the Dinurinae Looss, 1907 (Digenea: Hemiuridae) and resurrection of the Mecoderinae Skrjabin & Guschanskaja, 1954 based on novel collection of Tubulovesicula laticaudi Parukhin, 1969 from marine elapid snakes in Sri Lanka.

With one exception, the only known hemiurid trematodes that do not use teleost fishes as definitive hosts instead occur in marine elapid snakes. These comprise six species across four genera and three subfamilies, and so presumably indicate at least three independent invasions of marine snakes from teleost fishes. Here, one of these taxa, Tubulovesicula laticaudi Parukhin, 1969 (= T. orientalis Chattopadhyaya, 1970 n. syn.) is reported from Sri Lanka, collected from Shaw's sea snake Hydrophis curtus (Shaw) (Elapidae: Hydrophiinae: Hydrophinii), the annulated sea snake H. cyanocinctus Daudin and the yellow sea snake H. spiralis (Shaw) off Nayaru in the Bay of Bengal, and from H. spiralis in Portugal Bay, Gulf of Mannar. Novel molecular data, for COI mtDNA and ITS2 and 28S rDNA, are the first for a species of Tubulovesicula Yamaguti, 1934. Nominally, Tubulovesicula belongs in the Dinurinae Looss, 1907, but in phylogenetic analyses based on 28S rDNA, our sequences for T. laticaudi resolved relatively distant from that for representatives of Dinurus Looss, 1907, the type-genus, rendering the subfamily polyphyletic. Tubulovesicula laticaudi resolved closest to data for the type-species of the Plerurinae Gibson & Bray, 1979, but that subfamily is also polyphyletic. These findings lead us to re-evaluate an alternative classification considered by Gibson & Bray (1979). We propose restricting the Dinurinae for forms with a permanent sinus-organ (Dinurus, Ectenurus Looss, 1907; Erilepturus Woolcock, 1935; Paradinurus Vigueras, 1958; Qadriana Bilqees, 1971) and resurrect the Mecoderinae Skrjabin & Guschanskaja, 1954 for forms with a temporary sinus-organ (Mecoderus Manter, 1940, Allostomachicola Yamaguti, 1958, Stomachicola Yamaguti, 1934 and Tubulovesicula).

Taxonomic revision of the giant marine snake genus Pterosphenus Lucas, 1898, based on new fossil material from the middle Eocene (Bartonian) Harudi Formation of Kachchh (Kutch) Basin, India

ABSTRACT Fossil snakes of the family Palaeophiidae are primarily known from rare, isolated vertebrae, leading to a poor understanding of the intra- and inter-columnar variation within a palaeophiid species. This leads to ambiguity in the taxonomic identity of these snakes, as in the case of the Eocene-age marine snakes of the genus Pterosphenus, in which the majority of species have been described by characters of problematic taxonomic value. Here, we propose a taxonomic revision of the genus based on an articulated to semi-articulated section of the vertebral column at the anterior to mid trunk-transition of Pterosphenus schucherti discovered from the middle Eocene (Bartonian) Harudi Formation, Kachchh (Kutch) Basin. The characters that separate Pterosphenus schucherti from ‘Pterosphenus schweinfurthi’ and ‘Pterosphenus biswasi,’ viz., the height of the pterapophysis and the anterior concavity of the zygosphene, have been found to be non-diagnostic, and the latter two species have been synonymized with the type species. Additionally, we utilized 2D and 3D landmark-based geometric morphometry to determine the morphometric affinity of palaeophiids amongst the alethinophidian snakes. The body size of the snake was estimated based on extant snakes with a morphometric affinity to Palaeophiidae. The cosmopolitan distribution of Pterosphenus schucherti is modelled based on the sea surface temperature (SST) constraints of the modern cosmopolitan snake Hydrophis platurus, and the known fossil localities of the species. The present findings provide crucial insights into the global paleoecological landscape of the Eocene, and the interactions of Pterosphenus schucherti with other palaeophiid snakes as well as the other Eocene fauna.

Uneven species occurrence and richness of lowland snakes (Serpentes, Squamata) in Terengganu, Peninsular Malaysia, with new locality records.

This study documents information on the composition, diversity, richness, and temporal occurrence of snakes at Sekayu's lowland forest (SLF), Terengganu, Peninsular Malaysia for the first time. The snakes recorded within the SLF were sampled opportunistically from 2013 to 2019, employing the Visual Encounter Survey method (VES) and L-shape pitfall traps with drift fences. Forty-six snake species from 37 genera belonging to the nine families were recorded, of which 11 were new records to Terengganu. Individual-based rarefaction and extrapolation curves were not reaching asymptote, indicating that additional species can be recorded at the study area. Non-parametric species richness estimators estimated and produced a range between 51 and 57 species. ACE was the best estimator based on the quantitative evaluation. All species showed some variations of occurrence patterns across months. Fourteen species were only encountered once across the sampling years, and interestingly 11 of them were only detected during the rainy season (late October to January). In general, the number of species richness, abundance, and rare species were high during this season. Species richness of snakes is high at SLF but sampling effort should be intensified, especially during these rainy months, to obtain a robust estimated snake species richness in SLF. Terengganu harbor considerably high species richness of snakes with a total of 71 species to date (excluding marine snakes), but snake diversity is still underestimated as only a few localities were surveyed in the past years, primarily at the northern part. Future surveys should be commenced at the central and southern parts of Terengganu to complement the current investigation.

Macroevolution in axial morphospace: innovations accompanying the transition to marine environments in elapid snakes.

Sea snakes in the Hydrophis-Microcephalophis clade (Elapidae) show exceptional body shape variation along a continuum from similar forebody and hindbody girths, to dramatically reduced girths of the forebody relative to hindbody. The latter is associated with specializations on burrowing prey. This variation underpins high sympatric diversity and species richness and is not shared by other marine (or terrestrial) snakes. Here, we examined a hypothesis that macroevolutionary changes in axial development contribute to the propensity, at clade level, for body shape change. We quantified variation in the number and size of vertebrae in two body regions (pre- and post-apex of the heart) for approximately 94 terrestrial and marine elapids. We found Hydrophis-Microcephalophis exhibit increased rates of vertebral evolution in the pre- versus post-apex regions compared to all other Australasian elapids. Unlike other marine and terrestrial elapids, axial elongation in Hydrophis-Microcephalophis occurs via the preferential addition of vertebrae pre-heart apex, which is the region that undergoes concomitant shifts in vertebral number and size during transitions along the relative fore- to hindbody girth axis. We suggest that this macroevolutionary developmental change has potentially acted as a key innovation in Hydrophis-Microcephalophis by facilitating novel (especially burrowing) prey specializations that are not shared with other marine snakes.

The banded colour patterns of sea snakes discourage attack by predatory fishes, enabling Batesian mimicry by harmless species.

The evolution of bright 'warning' colours in nontoxic animals often is attributed to mimicry of toxic species, but empirical tests of that hypothesis must overcome the logistical challenge of quantifying differential rates of predation in nature. Populations of a harmless sea snake species (Emydocephalus annulatus) in New Caledonia exhibit colour polymorphism, with around 20% of individuals banded rather than melanic. Stability in that proportion over 20 years has been attributed to Batesian mimicry of deadly snake species by banded morphs of the harmless taxon. This hypothesis requires that banded colours reduce a snake's vulnerability to predation. We tested that idea by pulling flexible snake-shaped models through the water and recording responses by predatory fish. Black and banded lures attracted similar numbers of following fish, but attacks were directed almost exclusively to black lures. Our methods overcome several ambiguities associated with experimental studies on mimicry in terrestrial snakes and support the hypothesis that banded colour patterns reduce a non-venomous marine snake's vulnerability to predation.

Diversity, distribution, and natural history of the marine snakes of Sri Lanka

Diversity, distribution, and natural history of the marine snakes of Sri Lanka

Range extension of Czeblukov’s true sea snake Hydrophis czeblukovi (Elapidae:Hydrophiinae) southwest to Exmouth Gulf, Western Australia

ABSTRACT Our understanding of the biology and ecology of many Australian marine snakes is inadequate to inform the conservation and management of their populations. Czeblukov’s true sea snake Hydrophis czeblukovi (Elapidae:Hydrophiinae) is an example of this, with an IUCN classification of “Data Deficient”. It is a wholly marine, ovoviviparous snake that is distinguishable by its dark colouration and unique pale banding forming dark pentagons on its dorsal surface and flanks. A recent biological survey in Exmouth Gulf, Western Australia found a recently dead H. czeblukovi specimen. This extends the species geographical range by approximately 300 kilometres southwest (minimum seaward distance). The stranding likely arose from the persistent onshore winds observed prior to the discovery or from self-stranding due to illness. This discovery brings the total number of marine snake species recorded from Exmouth Gulf to 11 out of ~24 known to occur in WA waters, which highlights the importance of this location for marine snake conservation. Here we compile the scarce knowledge for this data deficient species. We discuss the conservation implications of our findings in context of the dense industrial activity across the range of H. czeblukovi. We indicate the need for further research to inform conservation and management actions.

Marine Origin Ligands of Nicotinic Receptors: Low Molecular Compounds, Peptides and Proteins for Fundamental Research and Practical Applications.

The purpose of our review is to briefly show what different compounds of marine origin, from low molecular weight ones to peptides and proteins, offer for understanding the structure and mechanism of action of nicotinic acetylcholine receptors (nAChRs) and for finding novel drugs to combat the diseases where nAChRs may be involved. The importance of the mentioned classes of ligands has changed with time; a protein from the marine snake venom was the first excellent tool to characterize the muscle-type nAChRs from the electric ray, while at present, muscle and α7 receptors are labeled with the radioactive or fluorescent derivatives prepared from α-bungarotoxin isolated from the many-banded krait. The most sophisticated instruments to distinguish muscle from neuronal nAChRs, and especially distinct subtypes within the latter, are α-conotoxins. Such information is crucial for fundamental studies on the nAChR revealing the properties of their orthosteric and allosteric binding sites and mechanisms of the channel opening and closure. Similar data are provided by low-molecular weight compounds of marine origin, but here the main purpose is drug design. In our review we tried to show what has been obtained in the last decade when the listed classes of compounds were used in the nAChR research, applying computer modeling, synthetic analogues and receptor mutants, X-ray and electron-microscopy analyses of complexes with the nAChRs, and their models which are acetylcholine-binding proteins and heterologously-expressed ligand-binding domains.

Evolution and dispersal of snakes across the Cretaceous-Paleogene mass extinction

Mass extinctions have repeatedly shaped global biodiversity. The Cretaceous-Paleogene (K-Pg) mass extinction caused the demise of numerous vertebrate groups, and its aftermath saw the rapid diversification of surviving mammals, birds, frogs, and teleost fishes. However, the effects of the K-Pg extinction on the evolution of snakes—a major clade of predators comprising over 3,700 living species—remains poorly understood. Here, we combine an extensive molecular dataset with phylogenetically and stratigraphically constrained fossil calibrations to infer an evolutionary timescale for Serpentes. We reveal a potential diversification among crown snakes associated with the K-Pg mass extinction, led by the successful colonisation of Asia by the major extant clade Afrophidia. Vertebral morphometrics suggest increasing morphological specialisation among marine snakes through the Paleogene. The dispersal patterns of snakes following the K-Pg underscore the importance of this mass extinction event in shaping Earth’s extant vertebrate faunas.

Ecological Filtering and Exaptation in the Evolution of Marine Snakes.

AbstractConvergent evolution is often attributed to adaptation of form to function, but it can also result from ecological filtering, exaptation, or nonaptation. Testing among these possibilities is critical to understanding how and why morphological similarities emerge independently in multiple lineages. To address this challenge, we combined multiple preexisting phylogenetic methods to jointly estimate the habitats and morphologies of lineages within a phylogeny. We applied this approach to the invasions of snakes into the marine realm. We utilized a data set for 1,243 extant snake species consisting of newly compiled biome occupancy information and preexisting data on reproductive strategy, body mass, and environmental temperature and elevation. We find evidence for marine clades arising from a variety of aquatic and terrestrial habitats. Furthermore, there is strong evidence of ecological filtering for nonmarine ancestors that were already viviparous, had slightly larger-than-average body sizes, and lived in environments with higher-than-average temperatures and lower-than-average elevations. In aggregate, similarities among independent lineages of marine snakes result from a combination of exaptation and strong ecological filtering. Strong barriers to entry of new habitats appear to be more important than common adaptations following invasions for producing similarities among independent lineages invading a shared, novel habitat.

The sex life aquatic: sexually dimorphic scale mechanoreceptors and tactile courtship in a sea snake Emydocephalus annulatus (Elapidae: Hydrophiinae)

Abstract Evolutionary transitions from terrestrial to aquatic habitats involve major selective shifts in animal signalling systems. Entirely marine snakes face two challenges during underwater social interactions: (1) finding mates when pheromones are diffused by water currents; and, once a mate is located, (2) maintaining contact and co-ordinating mating when tactile cues are diminished by buoyancy force. We explore the potential tactile roles of scale protuberances in the mating of turtle-headed sea snakes [Emydocephalus annulatus (Hydrophiinae)] by investigating sexual dimorphism in museum specimens (N = 59). In addition to the previously noted rostral spine on the snout, we found that mature males have enlarged structures located on the chin (genial knobs) and near the cloaca (anal knobs). Ultrastructural data indicates that the rostral spine is comprised of thickened epidermal and dermal layers, similar to rugosities on the body, and likely provide stimulation to the female during prodding by the male. In contrast, the genial and anal knobs have dermally derived central cells indicative of enlarged scale mechanoreceptors (i.e. sensilla). We suggest that these mechanoreceptors are critical to mating success: genial knobs may help amorous males orient to the direction of female motion; whereas, and anal knobs likely give somatosensory feedback for cloacal alignment

Pluridens serpentis, a new mosasaurid (Mosasauridae: Halisaurinae) from the Maastrichtian of Morocco and implications for mosasaur diversity

Mosasaurids (Mosasauridae) were specialized marine lizards that evolved and radiated in the Late Cretaceous. Their diversity peaked in the Maastrichtian, with the most diverse faunas known from Morocco. Here we describe a new species of mosasaurid from this fauna. Pluridens serpentis sp. nov. is described based on two complete skulls and referred jaws. It is referred to Pluridens based on the elongate and robust jaws, small teeth, and specialized tooth implantation. Pluridens is referred to Halisaurinae based on the posteriorly expanded premaxilla, long premaxilla-maxilla suture, broad premaxillary facet on the maxilla, closed otic notch, and small, striated, hooked teeth. The orbits are reduced relative to other halisaurines while the snout is robust and flat with a broad, rounded tip. The jaws bear numerous small, hooked, snake-like teeth. Skulls imply lengths of 5–6 m; referred material suggests lengths of ≥9 m. Pluridens’ specialized morphology – especially the contrasting large size and small teeth - suggests a distinct feeding strategy. Small orbits imply that P. serpentis relied on nonvisual cues including touch and chemoreception during foraging, as in modern marine snakes. Numerous neurovascular foramina on the premaxillae are consistent with this idea. The small teeth suggest proportionately small prey. The dentary becomes massive and robust in the largest individuals, suggesting sexual selection and perhaps sexual dimorphism, with the mandibles possibly functioning for combat as in modern beaked whales and lizards. The new mosasaur emphasizes how Maastrichtian mosasaurids were characterized by high species richness, high functional diversity, and high endemism, i.e. geographic specialization. It appears mosasaurids continued diversifying until the end of the Cretaceous, just prior to the K-Pg extinction.

Ecophysiological steps of marine adaptation in extant and extinct non-avian tetrapods.

Marine reptiles and mammals are phylogenetically so distant from each other that their marine adaptations are rarely compared directly. We reviewed ecophysiological features in extant non-avian marine tetrapods representing 31 marine colonizations to test whether there is a common pattern across higher taxonomic groups, such as mammals and reptiles. Marine adaptations in tetrapods can be roughly divided into aquatic and haline adaptations, each of which seems to follow a sequence of three steps. In combination, these six categories exhibit five steps of marine adaptation that apply across all clades except snakes: Step M1, incipient use of marine resources; Step M2, direct feeding in the saline sea; Step M3, water balance maintenance without terrestrial fresh water; Step M4, minimized terrestrial travel and loss of terrestrial feeding; and Step M5, loss of terrestrial thermoregulation and fur/plumage. Acquisition of viviparity is not included because there is no known case where viviparity evolved after a tetrapod lineage colonized the sea. A similar sequence is found in snakes but with the haline adaptation step (Step M3) lagging behind aquatic adaptation (haline adaptation is Step S5 in snakes), most likely because their unique method of water balance maintenance requires a supply of fresh water. The same constraint may limit the maximum body size of fully marine snakes. Steps M4 and M5 in all taxa except snakes are associated with skeletal adaptations that are mechanistically linked to relevant ecophysiological features, allowing assessment of marine adaptation steps in some fossil marine tetrapods. We identified four fossil clades containing members that reached Step M5 outside of stem whales, pinnipeds, sea cows and sea turtles, namely Eosauropterygia, Ichthyosauromorpha, Mosasauroidea, and Thalattosuchia, while five other clades reached Step M4: Saurosphargidae, Placodontia, Dinocephalosaurus, Desmostylia, and Odontochelys. Clades reaching Steps M4 and M5, both extant and extinct, appear to have higher species diversity than those only reaching Steps M1 to M3, while the total number of clades is higher for the earlier steps. This suggests that marine colonizers only diversified greatly after they minimized their use of terrestrial resources, with many lineages not reaching these advanced steps. Historical patterns suggest that a clade does not advance to Steps M4 and M5 unless these steps are reached early in the evolution of the clade. Intermediate forms before a clade reached Steps M4 and M5 tend to become extinct without leaving extant descendants or fossil evidence. This makes it difficult to reconstruct the evolutionary history of marine adaptation in many clades. Clades that reached Steps M4 and M5 tend to last longer than other marine tetrapod clades, sometimes for more than 100 million years.

The unusual biology of marine file snakes with a perspective for the conservation of Acrochordus granulatus

Biodiversity and the function of tropical shallow-water marine environments are threatened by numerous anthropogenic factors, especially climate change, overharvesting of resources, and destruction of habitat. Marine snakes are important components of coastal shallow-water systems and should be considered as indicators of the health of coastal ecosystems such as mangroves. Acrochordid snakes (Acrochordidae: Acrochordus) represent a highly distinct evolutionary lineage with unusual adaptations to shallow water habitats and importance to biodiversity of tropical coastal regions. One of three congeneric species, Acrochordus granulatus (file snake), is an interesting and common inhabitant of coastal estuaries and mangroves in the Philippines. This paper reviews unusual attributes of A. granulatus and provides a perspective for its conservation in coastal habitats. Morphological, physiological, and behavioral characters of this snake are specialized for life in shallow-water marine environments such as mangroves. Unusual and specialized features confer abilities for prolonged submergence and include low metabolic rate, large capacity for oxygen storage, cutaneous gas exchange, nearly complete utilization of oxygen stores during aerobic submergence, intracardiac and cutaneous shunts for regulating blood flow, and reclusive behavior. Fresh water is required for water balance, and file snakes are dependent on rainfall in many habitats where they drink from freshwater lenses formed by precipitation on the surfaces of marine water. File snakes feed largely on fishes and are candidates as bio-indicators of the health of shallow-water coastal habitats. Attention should be given to threatening insults on coastal environments including climate change, habitat destruction, harvesting of resources, and other factors in need of research, monitoring, and plans for abatement. Importantly, conservation can be promoted by educating people about the docile behavior, unusual traits, and interesting ecology of A. granulatus. KEYWORDS: mangrove, shallow water, Acrochordidae, little file snake, conservation physiology, ecophysiology

New Environment, New Invaders-Repeated Horizontal Transfer of LINEs to Sea Snakes.

Although numerous studies have found horizontal transposon transfer (HTT) to be widespread across metazoans, few have focused on HTT in marine ecosystems. To investigate potential recent HTTs into marine species, we searched for novel repetitive elements in sea snakes, a group of elapids which transitioned to a marine habitat at most 18 Ma. Our analysis uncovered repeated HTTs into sea snakes following their marine transition. The seven subfamilies of horizontally transferred LINE retrotransposons we identified in the olive sea snake (Aipysurus laevis) are transcribed, and hence are likely still active and expanding across the genome. A search of 600 metazoan genomes found all seven were absent from other amniotes, including terrestrial elapids, with the most similar LINEs present in fish and marine invertebrates. The one exception was a similar LINE found in sea kraits, a lineage of amphibious elapids which independently transitioned to a marine environment 25 Ma. Our finding of repeated horizontal transfer events into marine snakes greatly expands past findings that the marine environment promotes the transfer of transposons. Transposons are drivers of evolution as sources of genomic sequence and hence genomic novelty. We identified 13 candidate genes for HTT-induced adaptive change based on internal or neighboring HTT LINE insertions. One of these, ADCY4, is of particular interest as a part of the KEGG adaptation pathway “Circadian Entrainment.” This provides evidence of the ecological interactions between species influencing evolution of metazoans not only through specific selection pressures, but also by contributing novel genomic material.

The life aquatic: an association between habitat type and skin thickness in snakes

Abstract An aquatic animal faces challenges not encountered by its terrestrial counterparts, promoting adaptive responses in multiple traits. For example, a thicker dermis might protect snakes when they are pushed against sharp objects by water currents, and might enable a snake to shed fouling organisms attached to its skin. We thus predicted that marine snakes should have thicker skin than terrestrial species, and that smaller sea snakes should have relatively thicker skin (because absolute, not relative, thickness determines vulnerability to fouling). Measurements of 192 snakes of 44 species supported those predictions. Many (but not all) sea snakes have skins 50% thicker than those of terrestrial and amphibious snake species, representing multiple independent evolutionary origins of thicker skin (in acrochordids, Laticauda sea kraits and both main clades of hydrophiine sea snakes). Marine snakes showed different allometries of skin thickness compared with their terrestrial counterparts; larger snakes had thicker skin within and among species of amphibious and terrestrial snakes, but larger aquatic snake species had thinner skin compared with smaller taxa. Interspecific variation in skin thickness was primarily due to increased collagen in the deep dermis, a physical barrier well suited to protecting against physical injury and to resisting penetration by epibionts.

“Beyond Primary Sequence”—Proteomic Data Reveal Complex Toxins in Cnidarian Venoms

Venomous animals can deploy toxins for both predation and defense. These dual functions of toxins might be expected to promote the evolution of new venoms and alteration of their composition. Cnidarians are the most ancient venomous animals but our present understanding of their venom diversity is compromised by poor taxon sampling. New proteomic data were therefore generated to characterize toxins in venoms of a staurozoan, a hydrozoan, and an anthozoan. We then used a novel clustering approach to compare venom diversity in cnidarians to other venomous animals. Comparison of the presence or absence of 32 toxin protein families indicated venom composition did not vary widely among the 11 cnidarian species studied. Unsupervised clustering of toxin peptide sequences suggested that toxin composition of cnidarian venoms is just as complex as that in many venomous bilaterians, including marine snakes. The adaptive significance of maintaining a complex and relatively invariant venom remains unclear. Future study of cnidarian venom diversity, venom variation with nematocyst types and in different body regions are required to better understand venom evolution.