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First record of leucism in the polychromatic Amazon tree boa, Corallus hortulana (Serpentes, Boidae) of South America

ABSTRACT

Snakes have a wide variety of color patterns that can be related to specific ecological and physiological functions. However, genetic mutations can lead to the appearance of anomalous color patterns, which can directly interfere with the fitness of individuals. Leucism is a chromatic anomaly characterized by the almost total absence of epidermal and dermal chromatophores that produce the color. Corallus hortulana is an arboreal snake with nocturnal habits, widely distributed throughout South America, with a wide range of color patterns, known as polychromatism. Here we report the first case of leucism in Corallus hortulana and discuss the potential ecological implications of this anomaly in this species.

KEYWORDS:
Amazonia; Squamata; coloration; color pattern; snakes; French Guiana

RESUMO

As cobras possuem uma grande variedade de padrões de coloração que podem estar relacionadas a funções ecológicas e fisiológicas específicas. No entanto, mutações genéticas podem levar ao aparecimento de padrões de coloração anômalos que podem interferir diretamente na fitness do indivíduo. O leucismo é uma anomalia cromática caracterizada pela ausência quase total de cromatóforos epidérmicos e dérmicos que produzem a cor. Corallus hortulana é uma serpente arborícola de hábitos noturnos, amplamente distribuída pela América do Sul, com grande variação de padrões de cor, conhecida como policromatismo. Aqui nós relatamos o primeiro caso de leucismo em Corallus hortulana e discutimos as potenciais implicações ecológicas desta anomalia para a espécie.

PALAVRAS-CHAVE:
Amazônia; Squamata; coloração; padrão de cor; cobras; Guiana Francesa

Color in animals is characterized as the range of electromagnetic wavelengths reflected by pigments present in the chromatophores of the dermis and epidermis (Cuthill et al. 2017Cuthill, I.C.; Allen, W.L.; Arbuckle, K.; Caspers, B.; Chaplin, G.; Hauber, M.E.; et al. 2017. The biology of color. Science, 357: eaan0221. ). Snakes have a wide variety of color patterns ranging from cryptic to aposematic colors, which may have different ecological and physiological functions, (Davis Rabosky et al. 2016Davis Rabosky, A.R.; Cox, C.L.; Rabosky, D.L.; Title, P.O.; Holmes, I.A.; Feldman, A.; et al. 2016. Coral snakes predict the evolution of mimicry across New World snakes. Nature Communications, 7: 1-9. doi.org/10.1038/ncomms11484
https://doi.org/10.1038/ncomms11484...
, Deitloff et al. 2019Deitloff, J.; Myers, E.; Spear, S.; Stevenson, D.; Guyer, C. 2019. Multiple Paternity and Heritability of Color in Drymarchon couperi (Eastern Indigo Snakes). Herpetologica, 75: 224-232., Farooq and Uetz 2020Farooq, H.; Uetz, P. 2020. Identifying Australian snakes by color patterns. Vertebrate Zoology, 70: 473-482.). Color patterns reflect aspects of natural selection and predator-prey relationships (Davis Rabosky et al. 2016, Gustavo et al. 2016Gustavo, F.; Fran, R.; Federal, U. 2016. Predation in different phenotypes of venomous snakes in Atlantic Forest of Paraíba, Northeast Brazil. Revista Nordestina de Biologia, 24: 19-28., Cyriac and Kodandaramaiah 2019Cyriac, V.P.; Kodandaramaiah, U. 2019. Conspicuous colours reduce predation rates in fossorial uropeltid snakes. PeerJ, 7: e7508. ; Dallagnol Vargas et al. 2020Dallagnol Vargas, N.; Guimarães, M.; Caorsi, V.; Wolff Bordignon, D.; Borges-Martins, M. 2020. An experimental assessment of the antipredatory function of green dorsal coloration in poisonous Neotropical red-bellied toads. Journal of Zoology, 310: 171-179.).

Genetic mutations can lead to the emergence of aberrant or anomalous color patterns that can directly interfere with the fitness of individuals, as these anomalies often tend to reduce their chances of survival (Cyriac and Kodandaramaiah 2019Cyriac, V.P.; Kodandaramaiah, U. 2019. Conspicuous colours reduce predation rates in fossorial uropeltid snakes. PeerJ, 7: e7508. ). Albinism and melanism are the most common chromatic anomalies recorded in snakes (Prust 1984Prust, E. 1984. Albinism in snakes. Litteratura Serpentium, 4: 6-15., Borteiro et al. 2021Borteiro, C.; Abegg, A.D.; Oda, F.H.; Cardozo, D.; Kolenc, F.; Etchandy, I.; et al. 2021. Aberrant colourations in wild snakes: Case study in neotropical taxa and a review of terminology. Salamandra, 57: 124-138.). Recently, a new classification for chromatic anomalies found in snakes was proposed, to correcting some cases of individuals that had been classified as albinos but were actually of leucism (Borteiro et al. 2021). Leucism is an anomalous color pattern caused by the almost total absence of epidermal and dermal chromatophores, which may present some remnants of dispersed iridophores (Bechtel and Bechtel 1985Bechtel, H.B.; Bechtel, E. 1985. Genetics of color mutations in the snake, Elaphe obsoleta. Journal of Heredity, 76: 7-11., Borteiro et al. 2021).

Corallus hortulana (Linnaeus, 1758) is a polychromatic arboreal snake with nocturnal habits that is widely distributed throughout South America. Henderson (1997Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of neotropical tree boas. Caribbean Journal of Science, 33: 198-221.) classified the color patterns of this species into different categories based on the presence of spots on the dorsolateral and cephalic dorsal regions of the body for three background color morphs (taupe, yellow and brown). Although some color patterns in this species tend to be more frequent in certain regions of the Amazon, and the selection of color morphs by environmental variations has been suggested without explicit hypothesis testing, the predictor variables for the occurrence of color morphs are still unknown (Duarte et al. 2015Duarte, M. O.; Freitas, T.M.S.; Prudente, A.L.C. 2015. Polychromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica, 45: 373-382.).

Here we report the record of a leucistic individual of C. hortulana. The leucistic snake was sighted on July 14, 2021, at 08:45 pm, during a nocturnal survey on a trail by the margins of the road from Kourou to Cayenne, French Guiana (5°01’22.8”N; 52°29’02.7”W), in a region of savannas and secondary forests. The individual was photographed in situ and not collected, and the morphometric measurements were taken with a measuring tape in the field. The meristic characters were identified through the photographs taken. The individual (snout-vent length = 127 cm, tail length = 35.5 cm, unidentified sex) was moving along a branch approximately 1 m above the ground (Figure 1). The specimen was identified as Corallus hortulana due to the set of the following characters: 12 scales between the supra oculars, four subloreal scales, 14 circumorbital scales and contact between medial nasal scales, besides, the location falls within the expected geographic range of C. hortulana, following Henderson (1997Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of neotropical tree boas. Caribbean Journal of Science, 33: 198-221.). The individual was not collected. After handling, it was released at the point of capture.

Figure 1
Leucistic individual of Corallus hortulana recorded in French Guiana. This figure is in color in the electronic version.

The color of the individual was characterized by the predominance of white color throughout the body, with small spots of a light grayish color scattered through the body. The eyes had a black center and a peripheral region in shades of grayish blue. The tongue and internal part of the nasal orifices were dark purple color, with to pink labial pits (Figure 1). This coloration characterizes frame the individual as leucistic according to the classification of Borteiro et al. (2021Borteiro, C.; Abegg, A.D.; Oda, F.H.; Cardozo, D.; Kolenc, F.; Etchandy, I.; et al. 2021. Aberrant colourations in wild snakes: Case study in neotropical taxa and a review of terminology. Salamandra, 57: 124-138.), this being the first record in the wild of this chromatic anomaly for C. hortulana.

Leucism in wild snakes is extremely rarely reported. We found only one registered case for South American boids (Boa constrictor, Linnaeus 1758) in the state of Rio de Janeiro, Brazil (USA 2015USA. 2015. United States repatriates seven Boa constrictor to Brazil. US Department of Justice, Justice News 15: 17th, June. ( (https://www.justice.gov/opa/pr/united-states-repatriates-seven-boa-constrictors-brazil ). Accessed on 02 Sep 2021.
https://www.justice.gov/opa/pr/united-st...
). Furthermore, only one case of chromatic anomaly was recorded for the genus Corallus (erythrism in Corallus annulatus, Cope 1875) (Borteiro 2021Borteiro, C.; Abegg, A.D.; Oda, F.H.; Cardozo, D.; Kolenc, F.; Etchandy, I.; et al. 2021. Aberrant colourations in wild snakes: Case study in neotropical taxa and a review of terminology. Salamandra, 57: 124-138.), which is probably an underestimation due to the high diversity of color morphs in this group, especially within the Corallus hortulana (Henderson 1997Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of neotropical tree boas. Caribbean Journal of Science, 33: 198-221.).

From an ecological point of view, leucistic individuals become highly contrasting with the environment, especially in arboreal species. The fact that the specimen has reached adulthood may suggest that the nocturnal habit may be favorable to the survival of leucistic individuals, however, studies investigating this issue still need to be carried out.

ACKNOWLEDGMENTS

To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil), Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM, Brazil). J.A.R.A. and A.T.M. for reviewing the manuscript and philosophical contributions.

REFERENCES

  • Bechtel, H.B.; Bechtel, E. 1985. Genetics of color mutations in the snake, Elaphe obsoleta Journal of Heredity, 76: 7-11.
  • Borteiro, C.; Abegg, A.D.; Oda, F.H.; Cardozo, D.; Kolenc, F.; Etchandy, I.; et al. 2021. Aberrant colourations in wild snakes: Case study in neotropical taxa and a review of terminology. Salamandra, 57: 124-138.
  • Cuthill, I.C.; Allen, W.L.; Arbuckle, K.; Caspers, B.; Chaplin, G.; Hauber, M.E.; et al 2017. The biology of color. Science, 357: eaan0221.
  • Cyriac, V.P.; Kodandaramaiah, U. 2019. Conspicuous colours reduce predation rates in fossorial uropeltid snakes. PeerJ, 7: e7508.
  • Dallagnol Vargas, N.; Guimarães, M.; Caorsi, V.; Wolff Bordignon, D.; Borges-Martins, M. 2020. An experimental assessment of the antipredatory function of green dorsal coloration in poisonous Neotropical red-bellied toads. Journal of Zoology, 310: 171-179.
  • Davis Rabosky, A.R.; Cox, C.L.; Rabosky, D.L.; Title, P.O.; Holmes, I.A.; Feldman, A.; et al 2016. Coral snakes predict the evolution of mimicry across New World snakes. Nature Communications, 7: 1-9. doi.org/10.1038/ncomms11484
    » https://doi.org/10.1038/ncomms11484
  • Deitloff, J.; Myers, E.; Spear, S.; Stevenson, D.; Guyer, C. 2019. Multiple Paternity and Heritability of Color in Drymarchon couperi (Eastern Indigo Snakes). Herpetologica, 75: 224-232.
  • Duarte, M. O.; Freitas, T.M.S.; Prudente, A.L.C. 2015. Polychromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica, 45: 373-382.
  • Farooq, H.; Uetz, P. 2020. Identifying Australian snakes by color patterns. Vertebrate Zoology, 70: 473-482.
  • Gustavo, F.; Fran, R.; Federal, U. 2016. Predation in different phenotypes of venomous snakes in Atlantic Forest of Paraíba, Northeast Brazil. Revista Nordestina de Biologia, 24: 19-28.
  • Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of neotropical tree boas. Caribbean Journal of Science, 33: 198-221.
  • Prust, E. 1984. Albinism in snakes. Litteratura Serpentium, 4: 6-15.
  • USA. 2015. United States repatriates seven Boa constrictor to Brazil. US Department of Justice, Justice News 15: 17th, June. ( (https://www.justice.gov/opa/pr/united-states-repatriates-seven-boa-constrictors-brazil ). Accessed on 02 Sep 2021.
    » https://www.justice.gov/opa/pr/united-states-repatriates-seven-boa-constrictors-brazil
  • CITE AS:

    Fernandes, I.Y.; Dahan, A.; Fiot, B. 2022. First record of leucism in the polychromatic Amazon tree boa, Corallus hortulana (Serpentes, Boidae) of South America. Acta Amazonica 52: 42-44.

Edited by

ASSOCIATE EDITOR:

Claudia Keller

Publication Dates

  • Publication in this collection
    16 Mar 2022
  • Date of issue
    Jan-Mar 2022

History

  • Received
    23 July 2021
  • Accepted
    20 Dec 2021
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