Relationships between soil pollution by heavy metals and melanin‐dependent coloration of a fossorial amphisbaenian reptile

• Published in: Integrative zoology 2022-07, Vol.17 (4), p.596-607
• Main Authors: MARTÍN, José, RECIO, Pablo, RODRÍGUEZ‐RUIZ, Gonzalo, BARJA, Isabel, GUTIÉRREZ, Eduardo, GARCÍA, Luis V.
• Format: Article
• Language: English
• Subjects: amphisbaenians; Camouflage; Coloration; Colour; Communication; Contaminants; Endocrine disruptors; fossorial reptiles; Habitats; Heavy metals; Hypotheses; Industrial pollution; Melanin; Melanism; Melanization; Metal concentrations; Metals; Physiological functions; Physiology; Pollution; Reptiles; Seabirds; Skin; Skin tests; Soil; Soil contamination; Soil pollution; Thermoregulation
• ISSN: 1749-4877; 1749-4869; 1749-4877
• DOI: 10.1111/1749-4877.12562

Melanin is the basis of coloration in many animals, and although it is often used in communication, thermoregulation, or camouflage, melanin has many other physiological functions. For example, in polluted habitats, melanin can have a detoxifying function. Melanic coloration would help to sequester in the skin the heavy metal contaminants from inside the body, which will be expelled to the exterior when the skin is sloughed. Moreover, animals should have evolved more melanic colorations in more polluted habitats (“industrial melanism” hypothesis). We examined whether the fossorial amphisbaenian reptile, Trogonophis wiegmanni, is able to eliminate heavy metals, derived from soil pollution by seagull depositions, through sloughing its skin. Our results suggest a covariation between levels of soil pollution by heavy metals and the concentration of heavy metals in the sloughed skins of amphisbaenians. This suggests that amphisbaenians may expel heavy metals from their bodies when they slough the skins. We also tested whether amphisbaenians inhabiting soils with higher levels of heavy metal pollution had darker (melanin‐dependent) body colorations. However, contrary to predictions from the “industrial melanization” hypothesis, we found a negative relationship between soil pollution and proportions of melanic coloration. This contradictory result could, however, be explained because heavy metals have endocrine disruption effects that increase physiological stress, and higher stress levels could result in decreased melanogenesis. We suggest that although amphisbaenians might have some detoxifying mechanism linked to melanin in the skin, this process might be negatively affected by stress and result ineffective under conditions of high soil pollution. Melanin in the skin sequesters heavy metals, allowing detoxification when the skin is sloughed, and, thus, animals should be darker in polluted habitats to enhance detoxification (“industrial melanism hypothesis”). However, we found that although in the most polluted soils amphisbaenians expulse more heavy metals in sloughed skins, they have lighter colorations. This could result from pollution‐induced increased stress that impairs melanogenesis, limiting detoxification efficacy.