Environmental correlates of internal coloration in frogs vary throughout space and lineages

Abstract

Internal organs of ectotherms have melanin‐containing cells that confer different degrees of coloration to them. Previous experimental studies analyzed their developmental origin, role in immunity, and hormonal regulation. For example, melanin increases with ultraviolet radiation (UV) and temperature in frogs and fish. However, little is known about how environmental variables influence the amount of coloration on organs among amphibian species over a large spatial extent. Here, we tested how climatic variables (temperature, UV, and photoperiod) influence the coloration of internal organs of anurans. We recorded the level of melanin pigmentation using four categories on 12 internal organs and structures of 388 specimens from 43 species belonging to six anuran families. Then, we tested which climatic variables had the highest covariation with the pigmentation on each organ after controlling for spatial autocorrelation in climatic variables and phylogenetic signal in organ coloration using the extended version of the RLQ ordination. Coloration in all organs was correlated with the phylogeny. However, the coloration of different organs was affected by different variables. Specifically, the coloration of the heart, kidneys, and rectum of hylids, Rhinella schneideri, some Leptodactylus, and Proceratophrys strongly covaried with temperature and photoperiod, whereas that of the testicle, lumbar parietal peritoneum, lungs, and mesenterium of Leiuperinae, Hylodidae, Adenomera, and most Leptodactylus had highest covariation with UV‐B and temperature. Our results support the notion that melanin pigmentation on the surface of organs of amphibians has an adaptive function conferred by the protective functions of the pigment. But most importantly, internal melanin seems to respond differently to climatic variables depending on the lineage and locality in which species occur.

Idiosyncratic liver pigment alterations of five frog species in response to contrasting land use patterns in the Brazilian Cerrado

“…Although our statistical model explained much variation in the three substances, other climatic factors that have been changing because of human activities, such as temperature and UV radiation can also change the amount of melanin in internal tissues of frogs ( Franco-Belussi, Provete & De Oliveira, 2017 ). Changes in these environmental variables may promote changes in hepatic metabolism, such as increasing glycogen and lipid levels ( Mizell, 1965 ; Barni & Bernocchi, 1991 ; Fenoglio, Bernocchi & Barni, 1992 ; Barni et al, 2002 ).…”

“…The idiosyncratic responses of species may be related to differences in life history traits. Internal melanin varies among species and organs in anurans, possibly due to its adaptive function conferred by the protective functions of the pigment (Provete et al, 2012;Franco-Belussi, Provete & De Oliveira, 2017). For example, Physalaemus and Leptodactylus are terrestrial and can have more contact with xenobiotics; while Boana, Scinax, and Dendropsophus are arboreal and putatively less exposed to aquatic xenobiotics (Silva et al, 2013).…”

Short-term effects of α-melanocyte-stimulating hormone in three distinct melanin-pigmented cell types of Anura

“…Environmental factors (i.e., UV radiation, photoperiod, temperature, xenobiotics and inflammatory agents) can modulate the pigment occurrence and intensity in several anuran. This demonstrates the adaptive and protective functions of the internal melanin under stress conditions (Franco-Belussi et al 2017). Such conditions can increase the plasmatic level of (*) shows differences between control and treated groups.…”

Peer Review #1 of "Idiosyncratic liver pigment alterations of five frog species in response to contrasting land use patterns in the Brazilian Cerrado (v0.1)"

“…This is an indirect effect of land use change that can affect the amount of internal melanin in frogs. Although our statistical model explained much variation in the three substances, other climatic factors that have been changing because of human activities, such as temperature and Ultra-violet radiation can also change the amount of melanin in internal tissues of frogs (Franco-Belussi et al 2017). Changes in these environmental variables may promote changes in hepatic metabolism, such as increasing glycogen and lipid levels (Mizell, 1965;Barni and Bernocchi, 1991;Fenoglio et al 1992, Barni et al 2002.…”