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.

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.

Isotopic evidence concerning the habitat of Nautilus macromphalus in New Caledonia.

Modern nautilids (Nautilus and Allonautilus) have often been studied by paleontologists to better understand the anatomy and ecology of fossil relatives. Because direct observations of these animals are difficult, the analysis of light stable isotopes (C, O) preserved in their shells has been employed to reveal their habitat and life history. We aim to (1) reconstruct the habitat depth of Nautilus macromphalus and (2) decipher the fraction of metabolic carbon in its shell by analyzing oxygen and carbon isotopes (δ18O, δ13C) in the septa of two specimens in combination with analyses of water samples from the area. Additionally, we investigate whether morphological changes during ontogeny are reflected in the isotopic values of the shells. Results reveal that the patterns of change of δ18O and δ13C in the septa of N. macromphalus pre- and post-hatching are consistent with previous studies. Values of δ18Owater range from 0.7 to 1.4‰ (VSMOW), with a maximum value coincident with a salinity maximum at ~150 m. We use the temperature and δ18Owater profiles to calculate equilibrium values of δ18Oaragonite with depth. Comparing these values with the measured δ18O of the septa shows that the habitat depth of N. macromphalus is ~140 m pre-hatching and ~370 m post-hatching. Using δ13C of shell carbonate and published data on metabolic carbon, the fraction of metabolic carbon is reconstructed as ~21% and 14% pre- and post-hatching, respectively. The reconstructed depth pre-hatching is slightly shallower than in N. pompilius from the Philippines and Fiji, but the post-hatching depth is similar. However, it is important to emphasize that these estimates represent average over time and space because nautilus is a mobile animal. Lastly, the changes in morphological parameters and the changes in δ13C and δ18O during ontogeny do not coincide except at hatching and at the onset of maturity.

Divergence in life-history traits among three adjoining populations of the sea snake Emydocephalus annulatus (Hydrophiinae, Elapidae).

Life-history traits such as rates of growth, survival and reproduction can vary though time within a single population, or through space among populations, due to abiotically-driven changes in resource availability. In terrestrial reptiles, parameters such as temperature and rainfall generate variation in life-histories-but other parameters likely are more important in marine systems. We studied three populations of sea snakes (Emydocephalus annulatus) in adjacent bays in the IndoPacific archipelago of New Caledonia. The extreme philopatry of individual snakes allows us to unambiguously allocate each animal to one of the three populations. Although water temperatures and rainfall do not differ over this small scale, one site experiences more intense winds, restricting opportunities for foraging. Our 18-year mark-recapture dataset (> 1,200 snakes, > 2,400 captures) reveals significant divergence among populations in life-history traits. Survival rates and population densities were similar among sites, but snakes at the most wind-exposed site (Anse Vata) exhibited lower body condition, slower growth, less frequent production of litters, and smaller litters. Weather-driven variation in feeding rates thus may affect life-history traits of marine snakes as well as their terrestrial counterparts, but driven by different parameters (e.g., wind exposure rather than variation in temperatures or rainfall).

Frequency-dependent Batesian mimicry maintains colour polymorphism in a sea snake population.

Evolutionary theory suggests that polymorphic traits can be maintained within a single population only under specific conditions, such as negative frequency-dependent selection or heterozygote advantage. Non-venomous turtle-headed sea snakes (Emydocephalus annulatus) living in shallow bays near Noumea in New Caledonia exhibit three colour morphs: black, black-and-white banded, and an intermediate (grey-banded) morph that darkens with age. We recorded morph frequencies during 18 consecutive years of surveys, and found that the numbers of recruits (neonates plus immigrants) belonging to each morph increased in years when that morph was unusually rare in the population, and decreased when that morph was unusually common. Thus, morph frequencies are maintained by negative frequency-dependent selection. We interpret the situation as Batesian mimicry of highly venomous sea snakes (Aipysurus, Hydrophis, Laticauda) that occur in the same bays, and range in colour from black-and-white banded to grey-banded. Consistent with the idea that mimicry may protect snakes from attack by large fish and sea eagles, behavioural studies have shown that smaller fish species in these bays flee from banded snakes but attack black individuals. As predicted by theory, mimetic (banded) morphs are less common than the cryptically-coloured melanic morph.

Population dynamics of the sea snake Emydocephalus annulatus (Elapidae, Hydrophiinae).

For sea snakes as for many types of animals, long-term studies on population biology are rare and hence, we do not understand the degree to which annual variation in population sizes is driven by density-dependent regulation versus by stochastic abiotic factors. We monitored three populations of turtle-headed sea snakes (Emydocephalus annulatus) in New Caledonia over an 18-year period. Annual recruitment (% change in numbers) showed negative density-dependence: that is, recruitment increased when population densities were low, and decreased when densities were high. Windy weather during winter increased survival of neonates, perhaps by shielding them from predation; but those same weather conditions reduced body condition and the reproductive output of adult snakes. The role for density-dependence in annual dynamics of these populations is consistent with the slow, K-selected life-history attributes of the species; and the influence of weather conditions on reproductive output suggests that females adjust their allocation to reproduction based on food availability during vitellogenesis.

Sexual dimorphism in size and shape of the head in the sea snake Emydocephalus annulatus (Hydrophiinae, Elapidae).

In snakes, divergence in head size between the sexes has been interpreted as an adaptation to intersexual niche divergence. By overcoming gape-limitation, a larger head enables snakes of one sex to ingest larger prey items. Under this hypothesis, we do not expect a species that consumes only tiny prey items to exhibit sex differences in relative head size, or to show empirical links between relative head size and fitness-relevant traits such as growth and fecundity. Our field studies on the sea snake Emydocephalus annulatus falsify these predictions. Although these snakes feed exclusively on fish eggs, the heads of female snakes are longer and wider than those of males at the same body length. Individuals with wider heads grew more rapidly, reproduced more often, and produced larger litters. Thus, head shape can affect fitness and can diverge between the sexes even without gape-limitation. Head size and shape may facilitate other aspects of feeding (such as the ability to scrape eggs off coral) and locomotion (hydrodynamics); and a smaller head may advantage the sex that is more mobile, and that obtains its prey in narrow crevices rather than in more exposed situations (i.e., males).

Parental bleaching susceptibility leads to differences in larval fluorescence and dispersal potential in Pocillopora acuta corals.

Coral reef ecosystems are declining at an alarming rate. Increasing seawater temperatures and occurrence of extreme warming events can impair sexual reproduction in reef-building corals and inhibit the ability for coral communities to replenish and persist. Here, we investigated the role of photophysiology on the reproductive ecology of Pocillopora acuta coral colonies by focusing on the impacts of bleaching susceptibility of parents on reproduction and larval performance, during an El Niño Southern Oscillation event in Mo'orea, French Polynesia. Elevated temperature conditions at that time induced bleaching phenotypic differences among P. acuta individuals: certain colonies became pale (from the loss of pigments and/or decline in symbiont cell density), while others remained pigmented (normal/high symbiont cell density). More specifically, we studied the impact of parental phenotypes on offspring's fluorescence by counting released larvae and sorting them by fluorescence types, we assessed survival to thermal stress, recruitment success and post-recruitment survival of released larvae from each fluorescent phenotype, during summer months (February to April 2016). Our results showed that red and green fluorescent larvae released by P. acuta had distinct physiological performances: red fluorescent larvae exhibited a higher survival into the pelagic phase regardless temperature conditions, with lower capacity to settle and survive post-recruitment, compared to green larvae that settle within a short period. Interestingly, pale colonies released two-to seven-fold more red fluorescent larvae than pigmented colonies did. In the light of our results, photophysiological profiles of the brooding P. acuta parental colonies may modulate the fluorescence features of released larvae, and thus influence the dispersal strategy of their offspring, the green fluorescent larval phenotypes being more performant in the benthic than pelagic phase.

Swim with the tide: Tactics to maximize prey detection by a specialist predator, the greater sea snake (Hydrophis major).

The fitness of a predator depends upon its ability to locate and capture prey; and thus, increasing dietary specialization should favor the evolution of species-specific foraging tactics tuned to taxon-specific habitats and cues. Within marine environments, prey detectability (e.g., via visual or chemical cues) is affected by environmental conditions (e.g., water clarity and tidal flow), such that specialist predators would be expected to synchronize their foraging activity with cyclic variation in such conditions. In the present study, we combined behavioral-ecology experiments on captive sea snakes and their prey (catfish) with acoustic tracking of free-ranging sea snakes, to explore the use of waterborne chemical cues in this predator-prey interaction. In coral-reef ecosystems of New Caledonia, the greater sea snake (Hydrophis major) feeds only upon striped eel catfish (Plotosus lineatus). Captive snakes became more active after exposure to waterborne chemical cues from catfish, whereas catfish did not avoid chemical cues from snakes. Movement patterns of tracked snakes showed that individuals were most active on a rapidly falling tide, which is the time when chemical cues from hidden catfish are likely to be most readily available to a foraging predator. By synchronizing foraging effort with the tidal cycle, greater sea snakes may be able to exploit the availability of chemical cues during a rapidly falling tide to maximize efficiency in locating and capturing prey.

The behaviour of sea snakes (Emydocephalus annulatus) shifts with the tides.

Tidal cycles are known to affect the ecology of many marine animals, but logistical obstacles have discouraged behavioural studies on sea snakes in the wild. Here, we analyse a large dataset (1,445 observations of 126 individuals) to explore tidally-driven shifts in the behaviour of free-ranging turtle-headed sea snakes (Emydocephalus annulatus, Hydrophiinae) in the Baie des Citrons, New Caledonia. Snakes tended to move into newly-inundated areas with the rising tide, and became more active (e.g. switched from inactivity to mate-searching and courting) as water levels rose. However, the relative use of alternative habitat types was largely unaffected by tidal phase.

A new species of turtle-headed sea Snake (Emydocephalus: Elapidae) endemic to Western Australia.

We describe a new species of turtle-headed sea snake Emydocephalus orarius sp. nov. (Elapidae) from Western Australia's Coral Coast, Pilbara and Kimberley regions. Phylogenetic analysis of mitochondrial markers places the new species as the sister lineage to the two currently recognised species in Emydocephalus: E. annulatus from the Timor Sea reefs and Coral Sea, and E. ijimae from the Ryukyu Islands. Analysis of nuclear SNP data from the new species and E. annulatus from Australia and New Caledonia provides additional independent evidence of their evolutionary distinctiveness. The new taxon is usually morphologically diagnosable from its congeners using a combination of scalation and colour pattern characters, and appears to reach greater total lengths (>1 m in the new species versus typically ~80 cm in E. annulatus/E. ijimae). The new species is known largely from soft-bottomed trawl grounds, unlike E. annulatus and E.ijimae which usually inhabit coral reefs. The discovery of this new species brings the number of sea snake species endemic to Western Australia to six.

The ability of damselfish to distinguish between dangerous and harmless sea snakes.

In defence of their nests or territories, damselfish (Pomacentridae) attack even large and potentially dangerous intruders. The Indo-Pacific region contains many species of sea snakes, some of which eat damselfish whereas others do not. Can the fishes identify which sea snake taxa pose a threat? We recorded responses of damselfishes to natural encounters with five species of snakes in two shallow bays near Noumea, New Caledonia. Attacks by fishes were performed mostly by demersal territorial species of damselfish, and were non-random with respect to the species, size, sex and colouration of the snakes involved. The most common target of attack was Emydocephalus annulatus, a specialist egg-eater that poses no danger to adult fishes. Individuals of a generalist predator (Aipysurus duboisii) that were melanic (and thus resembled E. annulatus in colour) attracted more attacks than did paler individuals. Larger faster-swimming snake species (Aipysurus laevis, Laticauda saintgironsi) were watched but not attacked, or were actively avoided (Hydrophis major), even though only one of these species (A. laevis) eats pomacentrids. Attacks were more common towards female snakes rather than males, likely reflecting slower swimming speeds in females. In summary, damselfishes distinguish between sea snake species using cues such as size, colour and behaviour, but the fishes sometimes make mistakes.

Social-environmental drivers inform strategic management of coral reefs in the Anthropocene.

Without drastic efforts to reduce carbon emissions and mitigate globalized stressors, tropical coral reefs are in jeopardy. Strategic conservation and management requires identification of the environmental and socioeconomic factors driving the persistence of scleractinian coral assemblages-the foundation species of coral reef ecosystems. Here, we compiled coral abundance data from 2,584 Indo-Pacific reefs to evaluate the influence of 21 climate, social and environmental drivers on the ecology of reef coral assemblages. Higher abundances of framework-building corals were typically associated with: weaker thermal disturbances and longer intervals for potential recovery; slower human population growth; reduced access by human settlements and markets; and less nearby agriculture. We therefore propose a framework of three management strategies (protect, recover or transform) by considering: (1) if reefs were above or below a proposed threshold of >10% cover of the coral taxa important for structural complexity and carbonate production; and (2) reef exposure to severe thermal stress during the 2014-2017 global coral bleaching event. Our findings can guide urgent management efforts for coral reefs, by identifying key threats across multiple scales and strategic policy priorities that might sustain a network of functioning reefs in the Indo-Pacific to avoid ecosystem collapse.

Thermal resistances and acclimation potential during coral larval ontogeny in Acropora pulchra.

Rising temperature can adversely affect specific functions of corals. Coral gametes and planulae of Acropora pulchra were evaluated to determine their temperature resistances, and the potential of developmental thermal acclimation was examined on gametes. Results highlight that fertilization success displays a relatively high thermal resistance at ET50 (median effective temperature) 31.5 ±â€¯0.5 °C after 4 h and 30 min. Additionally, probability of larval survival is halved at LT50 (median lethal temperature) 28.4 ±â€¯0.42 °C after 14 days. The pre-exposure of oocytes to 30 °C and 32 °C for 1 h increases the cell development pace during fertilization at ambient temperature. Pre-exposure of gametes, separately at 32 °C for 1 h, increases fertilization success rate by 63% at 32°C, conversely, pre-exposure to 30 °C induces more variable results. These results evidenced the occurrence of developmental thermal acclimation as a result of thermal pre-exposure of oocytes.

Industrial Melanism in the Seasnake Emydocephalus annulatus.

Although classically associated with urban environments in invertebrates, melanism in terrestrial snakes is more often linked to occupancy of cool climates [1-3]. Thermal advantages to melanism do not apply in aquatic snakes [4], but although turtle-headed seasnakes (Emydocephalus annulatus) are banded or blotched across a wide geographic range [5], most individuals are melanic in polluted inshore bays of the Pacific island of New Caledonia [4]. Why has melanism evolved in these urban sites? Because trace elements bind to melanin, darker feathers enhance a bird's ability to shed pollutants [6]. Reptiles in polluted habitats also accumulate trace elements, which are expelled when the skin is sloughed [7-11]. Might melanism enable snakes to rid themselves of harmful pollutants? We measured trace elements in sloughed skins of seasnakes from urban-industrial versus other areas and in dark versus light skin. For the latter comparison, we used data from laticaudine seasnakes (sea kraits Laticauda spp.), in which each individual is dark and light banded, facilitating comparisons between dark and light skin. As predicted, concentrations of trace elements were higher in snakes from urban-industrial areas and higher in darker than paler skin (even within the same slough). The rate of excretion of trace elements is further enhanced by higher frequencies of sloughing in melanic than banded individuals, even within the same population, because of higher rates of algal settlement on darker skin. Thus, melanism of seasnakes in polluted sites may facilitate excretion of trace elements via sloughing. VIDEO ABSTRACT.

Major Sources of Organic Matter in a Complex Coral Reef Lagoon: Identification from Isotopic Signatures (δ13C and δ15N).

A wide investigation was conducted into the main organic matter (OM) sources supporting coral reef trophic networks in the lagoon of New Caledonia. Sampling included different reef locations (fringing, intermediate and barrier reef), different associated ecosystems (mangroves and seagrass beds) and rivers. In total, 30 taxa of macrophytes, plus pools of particulate and sedimentary OM (POM and SOM) were sampled. Isotopic signatures (C and N) of each OM sources was characterized and the composition of OM pools assessed. In addition, spatial and seasonal variations of reef OM sources were examined. Mangroves isotopic signatures were the most C-depleted (-30.17 ± 0.41 ‰) and seagrass signatures were the most C-enriched (-4.36 ± 0.72 ‰). Trichodesmium spp. had the most N-depleted signatures (-0.14 ± 0.03 ‰) whereas mangroves had the most N-enriched signatures (6.47 ± 0.41 ‰). The composition of POM and SOM varied along a coast-to-barrier reef gradient. River POM and marine POM contributed equally to coastal POM, whereas marine POM represented 90% of the POM on barrier reefs, compared to 10% river POM. The relative importance of river POM, marine POM and mangroves to the SOM pool decreased from fringing to barrier reefs. Conversely, the relative importance of seagrass, Trichodesmium spp. and macroalgae increased along this gradient. Overall, spatial fluctuations in POM and SOM were much greater than in primary producers. Seasonal fluctuations were low for all OM sources. Our results demonstrated that a large variety of OM sources sustain coral reefs, varying in their origin, composition and role and suggest that δ13C was a more useful fingerprint than δ15N in this endeavour. This study also suggested substantial OM exchanges and trophic connections between coral reefs and surrounding ecosystems. Finally, the importance of accounting for environmental characteristics at small temporal and spatial scales before drawing general patterns is highlighted.

An unusual occurrence of Nautilus macromphalus in a cenote in the Loyalty Islands (New Caledonia).

Exploration of a landlocked cenote on Lifou (Loyalty Islands) revealed 37 shells of the cephalopod Nautilus macromphalus Sowerby, 1849, in saltwater on the cenote floor, approximately 40 m below the water surface. The occurrence of these shells is unusual because N. macromphalus is restricted to the open marine waters surrounding the island. All of the shells are mature, and nearly all of them are unbroken, with faded red-brown color stripes. We analyzed seven shells to determine their age. Radiocarbon dating yielded ages of 6380±30 to 7095±30 y BP. The 238U-series radionuclides 210Pb (half-life  = 22.3 y) and 226Ra (half-life  = 1600 y) also were measured. Two of the samples showed radioactive equilibrium between the nuclides, consistent with the old radiocarbon dates, but the other five samples showed excess 210Pb. When corrected for radioactive decay, the 226Ra activities were much greater than those found in living Nautilus. We conclude that exposure to high activities of 222Rn and 226Ra in the salty groundwater of the cenote altered the activities originally incorporated into the shells. Human placement of the shells in the cavity is rejected based on their radiocarbon age and the geometry of the cenote. The most probable explanation is that the animals entered the flooded karstic system through a connection on the seaward side at approximately 7,000 y BP, during an interval of slowly rising sea level. Unable to find an exit and/or due to anoxic bottom waters, the animals were trapped and died inside. The open connection with the sea persisted for ∼700 y, but after ∼6400 y BP, the connection was lost, probably due to a roof collapse. This is a rare example of Nautilus in a karstic coastal basin and provides a minimum age for the appearance of N. macromphalus in the Loyalty Islands.

Adlardia novaecaledoniae n. g., n. sp. (Digenea: Cryptogonimidae) from the fork-tailed threadfin bream Nemipterus furcosus (Val.) (Perciformes: Nemipteridae) off New Caledonia.

Adlardia novaecaledoniae n. g., n. sp. (Digenea: Cryptogonimidae) is described from the fish Nemipterus furcosus (Val.) (Perciformes: Nemipteridae) from off New Caledonia (South Pacific). Adlardia n. g. is distinguished from all other cryptogonimid genera by the combination of an elongate body, the presence of oral spines, intestinal caeca that open via ani at the posterior end of the body, a highly lobed ovary, oblique testes that are located in the mid-hindbody, vitelline follicles that extend from midway between the testes and ovary to midway between the ovary and ventral sucker, and an excretory vesicle that bifurcates dorsal to the ovary and reunites immediately anterior to the pharynx. A. novaecaledoniae n. sp. is the only cryptogonimid that has been reported with an excretory vesicle that reunites anterior to the pharynx. Siphoderina elongata (Gu & Shen, 1979) Miller & Cribb, 2008 is transferred to Adlardia as A. elongata (Gu & Shen, 1979) n. comb. based on morphological and ecological (host group) agreement with A. novaecaledoniae. Bayesian inference analysis of LSU rDNA revealed that A. novaecaledoniae nested well within a clade containing cryptogonimid taxa known almost exclusively from haemulid and lutjanid fishes, suggesting that host-switching between teleosts of the Haemuloidea, Lutjanoidea and Sparoidea may have been common in the evolutionary history of this system.

Stable isotopes (delta13C and delta15N) of organic matrix from coral skeleton.

The evolutionary success of reef-building corals in nutrient-poor tropical waters is attributed to endosymbiotic dinoflagellates. The algae release photosynthetic products to the coral animal cells, augment nutrient flux, and enhance the rate of coral calcification. Natural abundance of stable isotopes (delta13C and delta18O) provides answers to modern and paleobiological questions about the effect of photosymbiosis on sources of carbon and oxygen in coral skeletal calcium carbonate. Here we compare 17 species of symbiotic and nonsymbiotic corals to determine whether evidence for photosymbiosis appears in stable isotopes (delta13C and delta15N) of an organic skeletal compartment, the coral skeletal organic matrix (OM). Mean OM delta13C in symbiotic and nonsymbiotic corals was similar (-26.08 per thousand vs. -24.31 per thousand), but mean OM delta15N was significantly depleted in 15N in the former (4.09 per thousand) relative to the latter (12.28 per thousand), indicating an effect of the algae on OM synthesis and revealing OM delta15N as a proxy for photosymbiosis. To answer an important paleobiological question about the origin of photosymbiosis in reef-building corals, we applied this proxy test to a fossil coral (Pachythecalis major) from the Triassic (240 million years ago) in which OM is preserved. Mean OM delta15N was 4.66 per thousand, suggesting that P. major was photosymbiotic. The results show that symbiotic algae augment coral calcification by contributing to the synthesis of skeletal OM and that they may have done so as early as the Triassic.