Turtle-headed seasnakes are melanic (black) in polluted sites, but not in other areas

Although classically associated with urban environments in invertebrates, melanism in terrestrial snakes is more often linked to occupancy of cool climates []. Thermal advantages to melanism do not apply in aquatic snakes [], but although turtle-headed seasnakes (Emydocephalus annulatus) are banded or blotched across a wide geographic range [], most individuals are melanic in polluted inshore bays of the Pacific island of New Caledonia []. Why has melanism evolved in these urban sites? Because trace elements bind to melanin, darker feathers enhance a bird’s ability to shed pollutants []. Reptiles in polluted habitats also accumulate trace elements, which are expelled when the skin is sloughed []. 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.

Heavy metal concentrations in northern water snakes (Nerodia sipedon) from East Fork Poplar Creek and the Little River, East Tennessee, USA.

Excretion of three heavy metals in the shed skin of exposed corn snakes (Elaphe guttata).

Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): the effect of sex, body size, and colour pattern.

Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): the effect of sex, body size, and colour pattern.

The Evolution of Melanism: The Study of a Recurring Necessity; With Special Reference to Industrial Melanism in the Lepidoptera.

Our mark-recapture data from a color-polymorphic population in New Caledonia [] show that the proportions of snakes that exhibited heavy algal fouling and sloughing at the time of capture were higher in melanic snakes than in banded snakes (logistic regression, algae χ= 20.86, degrees of freedom [df] = 1, p < 0.0001; sloughing χ= 9.12, df = 1, p < 0.003), but with similar seasonal patterns of sloughing in both color morphs.

Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): the effect of sex, body size, and colour pattern.

Mean concentrations of the 13 trace elements in sloughed skins analyzed ranged from 0.14 μg.gfor Cd to 1,385 μg.gfor Fe, with a maximum concentration of 6,195 μg.gof Fe ( Figures 2 and S1 Tables S2 and S3 ). There was no significant difference in trace-element concentrations between E. annulatus versus the laticaudine species (MANOVA, F(1,13) = 4.74, p = 0.35; Figure 3 ). For all 13 trace elements, mean concentrations were significantly higher in urban-industrial sites than in non-industrial sites ( Figures 2 and S1 Table S2 ; for statistical results, see Table S3 ). Concentrations of five trace elements (Co, Mn, Ni, Pb, Zn) were significantly higher in darker bands than in lighter bands (for statistical results see Table S3 ).

Some sites were close to urban-industrial areas, some were non-industrial, and one site was near the mouth of a major river that carried significant volumes of sediment. The panels show data (mean ± SE) for levels of trace elements in light- and dark-colored rings of sloughs from sea kraits from each type of site.

Concentrations of Trace Elements (ln μg.g -1 Dry Weight) in Sloughed Skins of Sea Kraits (Laticauda spp.) from the Great Lagoon of New Caledonia

Figure 2 Concentrations of Trace Elements (ln μg.g -1 Dry Weight) in Sloughed Skins of Sea Kraits (Laticauda spp.) from the Great Lagoon of New Caledonia

We surveyed color morphs of turtle-headed seasnakes across their geographic range, using a combination of field observations and examination of museum specimens ( Table S1 ). Melanism was common in E. annulatus from urban-industrial sites within New Caledonia and in a remote Barrier Reef atoll used as a bombing range in Australia (association between % melanism with the categories of urban-industrial, non-industrial, and river-mouth: F(2,20) = 27.61, p < 0.001; post hoc Tukey tests show that urban-industrial > non-industrial or river-mouth), whereas most snakes from less heavily polluted sites were banded or blotched ( Figure 1 and Table S1 ).

(C) Frequencies of melanism in snakes from urban-industrial sites versus other areas.

Discussion

In the seasnake Emydocephalus annulatus, melanism is more frequent in urban-industrial sites than in less polluted locations. Melanic snakes slough more often than banded conspecifics, and sloughing eliminates more trace elements from darker skin than from lighter skin. In combination, these results suggest that industrial melanism enhances a seasnake’s ability to dispose of trace elements.

12 Eisler R. Vertebrates, Volume 2, Compendium of Trace Metals and Marine Biota. 13 Grillitsch B.

Schiesari L. The ecotoxicology of metals in reptiles. 14 Heydari Sereshk Z.

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Bustamante P. Anguilliform fish reveal large scale contamination by mine trace elements in the coral reefs of New Caledonia. 17 Puls R. Mineral Levels in Animal Health. Diagnostic Data. 16 Bonnet X.

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Bustamante P. Anguilliform fish reveal large scale contamination by mine trace elements in the coral reefs of New Caledonia. 18 Migon C.

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Nicolas E. Geochemical and hydrodynamic constraints on the distribution of trace-element concentrations in the lagoon of Nouméa, New Caledonia. 16 Bonnet X.

Briand M.J.

Brischoux F.

Letourneur Y.

Fauvel T.

Bustamante P. Anguilliform fish reveal large scale contamination by mine trace elements in the coral reefs of New Caledonia. 15 Rezaie-Atagholipour M.

Riyahi-Bakhtiari A.

Sajjadi M.

Yap C.K.

Ghaffari S.

Ebrahimi-Sirizi Z.

Ghezellou P. Metal concentrations in selected tissues and main prey species of the annulated sea snake (Hydrophis cyanocinctus) in the Hara Protected Area, northeastern coast of the Persian Gulf, Iran. 19 Mann R.M.

Sánchez-Hernández J.C.

Serra E.A.

Soares A.M. Bioaccumulation of Cd by a European lacertid lizard after chronic exposure to Cd-contaminated food. 20 Weir S.M.

Suski J.G.

Salice C.J. Ecological risk of anthropogenic pollutants to reptiles: Evaluating assumptions of sensitivity and exposure. 21 Heatwole H. Sea Snakes. 22 Heatwole H.

Seymour R. Pulmonary and cutaneous oxygen uptake in sea snakes and a file snake. 23 Fisher N.S.

Reinfelder J.R. The trophic transfer of metals in marine systems. 24 Mathews T.

Fisher N.S. Dominance of dietary intake of metals in marine elasmobranch and teleost fish. 25 Furness R.W.

Camphuysen K.C.J. Seabirds as monitors of the marine environment. 26 Aguilar A.

Borrel A.

Pastor T. Biological factors affecting variability of persistent pollutant levels in cetaceans. Concentrations of trace elements in these sloughs were higher than most previous records for marine reptiles [], including seasnakes [] and fishes (including the eels consumed by sea kraits []), and higher than can cause health problems in mammals and birds []. Seasnakes in the Noumea Lagoon are exposed to pollutants via run-off from terrestrial systems []. New Caledonia’s rich mineral deposits create high levels of trace-element contamination, further increased by mining activities []. High trace-element concentrations in sloughs of sea kraits from close to a river-mouth (but far from urban-industrial activity) suggest that melanism may benefit seasnakes in many areas. The primary uptake of trace elements presumably comes via ingestion of prey, with predatory snakes accumulating trace elements through time (i.e., bioaccumulation []). These snakes also might take up trace elements directly from the water [], given their high ratio of surface area to volume, and significant rates of gas exchange across the skin []. However, radiotracer studies on other aquatic species suggest that feeding is the primary pathway for uptake of trace elements in invertebrates [], fish [], seabirds [], and cetaceans [].

27 Shine R.

Brischoux F.

Pile A.J. A seasnake’s colour affects its susceptibility to algal fouling. Importantly, concentrations of trace elements were higher in darker than in lighter bands within the same slough ( Table S3 ). As in birds, then, melanin-rich areas of a snake’s outer surface accumulate trace elements, and, hence, sloughing reduces the trace-element load faster in melanic snakes than in paler conspecifics. That effect is amplified by the higher sloughing frequency of melanic Emydocephalus ( Figure 1 A), presumably because algal spores settle onto dark substrates, enhancing rates of algal fouling [].

28 Cook L.M.

Saccheri I.J. The peppered moth and industrial melanism: evolution of a natural selection case study. 29 Lukoschek V.

Beger M.

Ceccarelli D.

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Pratchett M. Enigmatic declines of Australia’s sea snakes from a biodiversity hotspot. The melanic morph appears to be a derived trait in E. annulatus, but the number of independent evolutionary increases in the frequency of melanism is unclear. A single origin may have been involved, as in peppered moths [], but occasional melanism is geographically widespread in E. annulatus ( Table S1 ). The only sites where melanism in E. annulatus was common, but which were not urban-industrial sites, were Saumarez Reef, an isolated reef that is used as a bombing range, and Ashmore Reef ( Table S1 ), a site where seasnake populations have plummeted in recent years, possibly due to pollution from fishing boats []. Future work should measure concentrations of trace elements at these reefs, to quantify the correlation between melanism and pollutant levels more robustly, and compare trace-element concentrations to snake coloration in populations of E. annulatus where the banded morph occurs at a high frequency.

2 Majerus M.E.N. Melanism: Evolution in Action. 6 Chatelain M.

Gasparini J.

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Frantz A. The adaptive function of melanin-based plumage coloration to trace metals. 30 Hansson L.A. Plasticity in pigmentation induced by conflicting threats from predation and UV radiation. 31 Shine R. All at sea: aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae). What alternative hypotheses could explain the high frequency of melanism in seasnakes from urban-industrial habitats? Melanin plays diverse and important physiological roles. For example, enhanced immune function in melanin-rich individuals might be advantageous in polluted sites where the animals are subject to chemical stresses [], or melanism might protect snakes from high UV levels in clear shallow water []. Ecological advantages to melanism (such as local color matching to the habitat, to avoid visual predation) or reproductive advantages (mate choice) seem less likely: there are no clear differences in habitat use between banded and melanic snakes in our study populations, and a snake’s color appears to play little role in mate recognition [].

In summary, melanism has evolved under diverse selective advantages. Intriguingly, the seasnakes we studied in the Indo-Pacific exhibit the same correlation as seen in insects and pigeons in European cities: melanism is more common in urban-industrial environments. However, the selective advantages underlying that common pattern may involve antipredator camouflage and physiological benefits in insects versus trace-element excretion in pigeons and seasnakes.