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Two records of xanthism in Corallus hortulana (Serpentes: Boidae) in Bolivia with comments on the yellow, patternless morphotype

ABSTRACT

Snakes display a wide range of skin colors and patterns, acting in ecological, behavioral, and physiological roles. Xanthism has been reported in numerous snake species, including many neotropical taxa. Corallus hortulana is a polychromatic species widely distributed throughout South America. Yellow, patternless individuals, while rare, have been recognized as within the species’ polychromatic range. We report the first yellow, patternless specimens of Corallus hortulana collected in Bolivia and discuss whether these individuals fit the criteria of xanthism.

KEYWORDS:
snakes; polychromatism; chromatic aberrancies; Amazon

RESUMEN

Las serpientes muestran una amplia gama de colores y patrones de piel, actuando en roles ecológicos, de comportamiento y fisiológicos. Además, se ha informado xantismo en numerosas especies de serpientes, incluidos muchos taxones neotropicales. Corallus hortulana es una especie policromática ampliamente distribuida en América del Sur. Los individuos amarillos sin patrón, aunque raros, se han reconocido dentro del rango policromático de la especie. Reportamos los primeros especímenes amarillos sin patrón de Corallus hortulana recolectados en Bolivia y discutimos si estos individuos cumplen con los criterios de xantismo.

PALABRAS CLAVE:
serpientes; policromátismo; aberraciones cromáticas; Amazonía

Snakes display an extremely wide range of skin colors and patterns, which serve ecological, behavioral, and physiological roles (e.g. camouflage, warning, thermoregulation, mimicry) (Bechtel 1978Bechtel, H.B. 1978. Color and pattern in snakes. Journal of Herpetology 12: 521-532.; Cooper and Greenberg 1992Cooper, W.E. Jr. ; Greenberg, N. 1992. Reptilian coloration and behavior. In: Gans, C.; Crews, D. (Ed.). Biology of the Reptilia. University of Chicago Press, Chicago, p.298-422. ; Allen et al. 2013Allen, W.L.; Baddeley, R.; Scott-Samuel, N.E.; Cuthill, I.C. 2013. The evolution and function of pattern diversity in snakes. Behavioral Ecology, 24: 1237-1250.). Chromatic aberrancies have been reported in numerous snake species, including many neotropical taxa (Bechtel 1978; Dyrkacz 1981Dyrkacz, S. 1981. Recent Instances of Albinism in North American Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles, Herpetological Circular 11: 1-31.; Krecsák 2008Krecsák, L. 2008. Albinism and leucism among European Viperinae: a review. Russian Journal of Herpetology , 15: 97-102. ; 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.). Chromatic aberrancies or atypical coloration has been argued to reduced fitness and survival in snakes (Krecsák 2008; Cyriac and Kodandaramaiah 2019Cyriac, V.P.; Kodandaramaiah, U. 2019. Conspicuous colours reduce predation rates in fossorial uropeltid snakes. PeerJ, 7: e7508.). However, Stephenson et al. (2022Stephenson, B.P.; Velani, Z.; Ihász, N. 2022. The effect of albinism on avian predator attack rates in eastern garter snakes. Zoology, 150: 125987.) presented evidence that albinism does not increase predation risk in the eastern garter snake, Thamnophis sirtalis (Linnaeus, 1758). Overall, however, empirical evidence regarding chromatic aberrancies in wild snake populations and their effects on fitness and survivability remain scarce.

Common aberrant color patterns of hyperpigmentation and/or hypopigmentation in snake species include albinism, characterized by total (red eyes and completely pigmentless body) to partial absence of pigmentation; leucism, defined by normally pigmented eyes and partially or totally pigmentless body; xanthism and erythrism characterized by the overabundance of yellow or red pigment, respectively; and melanism, an overexpression of the black pigment melanin (Harris 1970Harris, H.S. 1970. Abnormal pigmentation in Maryland amphibians and reptiles. Bulletin of the Maryland Herpetological Society, 6: 21-27.; Bechtel 1978Bechtel, H.B. 1978. Color and pattern in snakes. Journal of Herpetology 12: 521-532., 1995Bechtel, H.B. 1995. Reptile and amphibian variants. Colors, patterns, and scales. Krieger Publishing Co., USA, 224p.; Dyrkacz 1981Dyrkacz, S. 1981. Recent Instances of Albinism in North American Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles, Herpetological Circular 11: 1-31.). Due to ambiguity in the literature, 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 redefined and clarified the criteria and terminology used to describe aberrant color patterns in wild snakes.

The tree boa Corallus hortulana (Linnaeus, 1758) is a medium-sized booid with a maximum snout to vent length of 1787 mm (Henderson 2002Henderson, R.W. 2002. Neotropical Treeboas: Natural History of the Corallus hortulanus Complex. Krieger Publishing, Malabar, 228p.). It is a primarily nocturnal and arboreal snake species that is widely distributed throughout South America (Henderson et al. 1995; Stafford and Henderson 1996Stafford, P.J.; Henderson, R.W. 1996. Kaleidoscopic Tree Boas: The Genus Corallus of Tropical America. Krieger Publishing, Malabar , 86p.; Henderson 1993, 1997, 2002; Duarte et al. 2015Duarte, M.; Freitas, T.; Prudente, A.L. 2015. Polycromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica, 45: 373-382.). The species inhabits mostly lowland areas, including: primary and secondary forest, seasonally flooded savannas, flooded forests, dry forests, and gallery forests associated with rivers, streams, and lagoons (Silva 1993Silva, N.J. Jr. 1993. The snakes from Samuel Hydroelectric Power Plant and vicinity, Rondônia, Brazil. Herpetological Natural History, 1: 37-86.; Stafford and Henderson 1996; Henderson 1993, 1997, 2002; Martins and Oliveira 1998Martins, M.; Oliveira, M.E. 1998. Natural history of snakes in forests of the Manaus region, Central Amazonia, Brazil. Herpetological Natural History, 6: 78-150.; Duellman 2005Duellman, W.E. 2005. Cusco Amazónico: The Lives of Amphibians and Reptiles in an Amazonian Rainforest. Comstock Publishing Associates, Cornell University Press, Ithaka, 456p.; Rivas et al. 2022Rivas, L.R.; Mendoza-Miranda, P.; Miranda, O. 2022. Guía Ilustrada de Anfibios y Reptiles de la Ciudad de Trinidad, Bolivia. Universidad Autónoma del Beni José Ballivián, Wildlife Conservation Society, Grupo de Trabajo para los Llanos de Moxos, Trinidad, 255p.).

Amazonian populations of C. hortulana are highly polychromatic, displaying a range of colors and patterns (Stafford and Henderson 1996Stafford, P.J.; Henderson, R.W. 1996. Kaleidoscopic Tree Boas: The Genus Corallus of Tropical America. Krieger Publishing, Malabar , 86p.; Henderson 1993, 1997, 2002; Duarte et al. 2015Duarte, M.; Freitas, T.; Prudente, A.L. 2015. Polycromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica, 45: 373-382.). Polychromatism in snakes has been suggested to be associated with several environmental, geographical, behavioral, and genetic variables (Henderson 1997; Farallo and Forstner 2012Farallo, V.R.; Forstner, M.R.J. 2012. Predation and the maintenance of color polymorphism in a habitat specialist Squamate. PLoS ONE, 7: e30316.; Pizzatto and Dubey 2012Pizzatto, L.; Dubey, S. 2012. Colour-polymorphic snake species are older. Biological Journal of the Linnean Society, 107: 210-218. ; Duarte et al. 2015). In C. hortulana, the polychromatism has been described and categorized into character states or morphotypes [see Henderson (1997) and Duarte et al. (2015) for more details]. Interestingly, there is only one record of an aberrant color pattern (leucism) in C. hortulana, documented from a specimen in French Guiana (Fernandes et al. 2022Fernandes, 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.), which does not fit within the designated morphotypes of Henderson (1997) or Duarte et al. (2015). To the best of our knowledge, there are no other published reports on chromatic aberrancies in C. hortulana.

Here, we report and describe two cases of yellow, patternless (xanthic) specimens of Corallus hortulana collected in the Department of Beni, Bolivia. The individuals were identified following Henderson (1993Henderson, R.W. 1993. Corallus enydris (Linnaeus). Catalogue of American Amphibians and Reptiles, 576: 1-6., 1997Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of Neotropical tree boa. Caribbean Journal of Science, 33: 198-221., 2002Henderson, R.W. 2002. Neotropical Treeboas: Natural History of the Corallus hortulanus Complex. Krieger Publishing, Malabar, 228p.) and Peters and Orejas-Miranda (1970Peters, J.A.; Orejas-Miranda, B. 1970. Catalogue of the Neotropical Squamata: Part I Snakes. Bulletin of the United States National Museum, 297: 1-347.) based on the following diagnostic characters: strongly laterally compressed body with smooth dorsal scales (midbody dorsal scale count 37-63); scales of the head: subocular scales present and in contact with supralabial scales; loreal scale fragmented and numerous infraloreal scales present; and nasal scales in contact and separating internasals from rostral.

The first specimen was collected in Yacuma Province, 100 m west of the bank of the Mamoré River, by a trail to the community of Exaltación (13°18’10.69”S, 65°14’45.96”W), on June 15, 2015, at 00:32 h, by R.L. Powell, C.B. Eversole, and D. Lizarro, during a herpetofaunal survey. The snake was found 2.5 m high in a tree in primary forest. The specimen is a female measuring 102 cm snout to vent length, 21.7 cm tail length, with a live weight of 180 g. (Figure 1). The specimen was deposited in the Colección de Historia Natural de Herpetología, Centro de Investigación de Recursos Acuáticos, Universidad Autónoma del Beni José Ballivián (voucher CIRA-208).

Figure 1
Adult Corallus hortulana (CIRAH-208) collected in Yacuma Province, Department of Beni, Bolivia. A - overall view; B - detail of the head. Credit: R.L. Powell, C.B. Eversole, D. Lizarro. This figure is in color in the electronic version.

The second individual was also found during a herpetofaunal survey in Yacuma Province, by the east bank of the Niquisi River (13°56’22.36”S, 65°13’4.06”W), adjacent to an oxbow lake of the Mamoré River, in the vicinity of the Toboso community (Canichana Community Land of Origin) on September 26, 2017, at 22:31 h; L.R. Rivas, and R. Chungara. The snake was found 2.3 m high in tree. The individual was not collected and its sex was not determined. It was examined, measured (total length = 150 cm), photographed [vouchered photo record: CIRA(VP)-851] (Figure 2) and released on the site of capture.

Figure 2
Adult Corallus hortulana (CIRA(VP)-851) recorded in Yacuma Province, Department of Beni, Bolivia. A - overall view; B - detail of the head. Credit: L.R. Rivas. This figure is in color in the electronic version.

Both individuals in life were yellow and patternless with a white ventral region, and had a few flecks of light tan scales and numerous scattered small areas (2-5 scales) without pigmentation on the dorsum. The eye pigmentation of both specimens was yellow. The records were within 70 km of each other (Figure 3).

Figure 3
Location records of two xanthic individuals of Corallus hortulana in Bolivia (yellow circles) (CIRA-208, CIRA(VP)-851). Corallus hortulana distribution range in Bolivia based on Henderson (1997Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of Neotropical tree boa. Caribbean Journal of Science, 33: 198-221.), Embert (2008Embert, D. 2008. Distribution, diversity and conservation status of Bolivian Reptiles. Doctoral thesis, Rheinische Friedrich-Wilhelms-Universität Bonn, Germany, 429p. (https://bonndoc.ulb.uni-bonn.de/xmlui/handle/20.500.11811/3619).
https://bonndoc.ulb.uni-bonn.de/xmlui/ha...
), and Nogueira et al. (2019Nogueira, C.C.; Argôlo, A.J.S.; Arzamendia, V.; Azevedo, J.A.; Barbo, F.E.; Bérnils, R.S.; et al. 2019. Atlas of Brazilian snakes: verified point-locality maps to mitigate the Wallacean Shortfall in a megadiverse snake fauna. South American Journal of Herpetology , 14 (suppl. 1): 1-274. ). This figure is in color in the electronic version.

Yellow, patternless individuals of C. hortulana have been recognized as within the species polychromatic range (referred to as character states or morphotypes) (Henderson et al. 1995Henderson, R.W.; Waller, T.; Micucci, P.; Puorto, G.; Bourgeois, R.W. 1995. Ecological correlates and patterns in the distribution of Neotropical boines (Serpentes: Boidae): a preliminary assessment. Herpetological Natural History, 3: 15-27.; Stafford and Henderson 1996Stafford, P.J.; Henderson, R.W. 1996. Kaleidoscopic Tree Boas: The Genus Corallus of Tropical America. Krieger Publishing, Malabar , 86p.; Henderson 1993, 1997, 2002; Duarte et al. 2015Duarte, M.; Freitas, T.; Prudente, A.L. 2015. Polycromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica, 45: 373-382.). Among 112 preserved specimens from the Amazon basin examined by Duarte et al. (2015), only two were light-colored, patternless individuals. Henderson (1997, 2002) examined more than 600 specimens from throughout the species’ range, including over 170 specimens from mainland South America; less than 5.9% were flecked or patternless yellow individuals, none of them from Bolivia.

While Henderson (1997Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of Neotropical tree boa. Caribbean Journal of Science, 33: 198-221.) and Duarte et al. (2015Duarte, M.; Freitas, T.; Prudente, A.L. 2015. Polycromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica, 45: 373-382.) made important contributions via their detailed analyses of morphotypes and color patterns of C. hortulana, we argue that the light-colored, designless Morphotype 6 of Duarte et al. (2015), as well as the yellow, flecked Character State 6 and yellow, patternless Character State 7 of Henderson (1997) all meet the criteria of xanthism (i.e., overexpression of yellow pigmentation associated with the lack of red, brown, or black pigmentation) (Harris 1970Harris, H.S. 1970. Abnormal pigmentation in Maryland amphibians and reptiles. Bulletin of the Maryland Herpetological Society, 6: 21-27.; Bechtel 1978Bechtel, H.B. 1978. Color and pattern in snakes. Journal of Herpetology 12: 521-532., 1995; Dyrkacz 1981Dyrkacz, S. 1981. Recent Instances of Albinism in North American Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles, Herpetological Circular 11: 1-31.; 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.).

Interestingly, 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.) reported that xanthism in neotropical snakes was rarely observed and was only documented in nocturnal species (which would include C. hortulana). Our records are the first report of xanthism in C. hortulana in Bolivia, and contribute to the understanding of the occurrence and distribution of chromatic aberrancies in wild populations of this species.

ACKNOWLEDGMENTS

The General Directorate of Biodiversity and Protected Areas for collection permits (Bolivia) and the Centro de Investigación de Recursos Acuáticos (CIRA), Universidad Autónoma del Beni “José Ballivian” for logistical support. We wish to thank the people of the Canichana Community Lands of Origin. Special thanks to Dr. Diego Baldo, Laboratorio de Genética Evolutiva, Instituto de Biología Subtropical (CONICET-UNaM), Facultad de Ciencias Exactas Químicas y Naturales, Universidad Nacional de Misiones, Misiones, Argentina for consulting on xanthism.

REFERENCES

  • Allen, W.L.; Baddeley, R.; Scott-Samuel, N.E.; Cuthill, I.C. 2013. The evolution and function of pattern diversity in snakes. Behavioral Ecology, 24: 1237-1250.
  • Bechtel, H.B. 1978. Color and pattern in snakes. Journal of Herpetology 12: 521-532.
  • Bechtel, H.B. 1995. Reptile and amphibian variants. Colors, patterns, and scales Krieger Publishing Co., USA, 224p.
  • 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.
  • Cooper, W.E. Jr. ; Greenberg, N. 1992. Reptilian coloration and behavior. In: Gans, C.; Crews, D. (Ed.). Biology of the Reptilia University of Chicago Press, Chicago, p.298-422.
  • Cyriac, V.P.; Kodandaramaiah, U. 2019. Conspicuous colours reduce predation rates in fossorial uropeltid snakes. PeerJ, 7: e7508.
  • Duarte, M.; Freitas, T.; Prudente, A.L. 2015. Polycromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin, Brazil. Acta Amazonica, 45: 373-382.
  • Duellman, W.E. 2005. Cusco Amazónico: The Lives of Amphibians and Reptiles in an Amazonian Rainforest Comstock Publishing Associates, Cornell University Press, Ithaka, 456p.
  • Dyrkacz, S. 1981. Recent Instances of Albinism in North American Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles, Herpetological Circular 11: 1-31.
  • Embert, D. 2008. Distribution, diversity and conservation status of Bolivian Reptiles Doctoral thesis, Rheinische Friedrich-Wilhelms-Universität Bonn, Germany, 429p. (https://bonndoc.ulb.uni-bonn.de/xmlui/handle/20.500.11811/3619).
    » https://bonndoc.ulb.uni-bonn.de/xmlui/handle/20.500.11811/3619
  • Farallo, V.R.; Forstner, M.R.J. 2012. Predation and the maintenance of color polymorphism in a habitat specialist Squamate. PLoS ONE, 7: e30316.
  • 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.
  • Krecsák, L. 2008. Albinism and leucism among European Viperinae: a review. Russian Journal of Herpetology , 15: 97-102.
  • Harris, H.S. 1970. Abnormal pigmentation in Maryland amphibians and reptiles. Bulletin of the Maryland Herpetological Society, 6: 21-27.
  • Henderson, R.W. 1993. Corallus enydris (Linnaeus). Catalogue of American Amphibians and Reptiles, 576: 1-6.
  • Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of Neotropical tree boa. Caribbean Journal of Science, 33: 198-221.
  • Henderson, R.W. 2002. Neotropical Treeboas: Natural History of the Corallus hortulanus Complex Krieger Publishing, Malabar, 228p.
  • Henderson, R.W.; Waller, T.; Micucci, P.; Puorto, G.; Bourgeois, R.W. 1995. Ecological correlates and patterns in the distribution of Neotropical boines (Serpentes: Boidae): a preliminary assessment. Herpetological Natural History, 3: 15-27.
  • Martins, M.; Oliveira, M.E. 1998. Natural history of snakes in forests of the Manaus region, Central Amazonia, Brazil. Herpetological Natural History, 6: 78-150.
  • Nogueira, C.C.; Argôlo, A.J.S.; Arzamendia, V.; Azevedo, J.A.; Barbo, F.E.; Bérnils, R.S.; et al 2019. Atlas of Brazilian snakes: verified point-locality maps to mitigate the Wallacean Shortfall in a megadiverse snake fauna. South American Journal of Herpetology , 14 (suppl. 1): 1-274.
  • Peters, J.A.; Orejas-Miranda, B. 1970. Catalogue of the Neotropical Squamata: Part I Snakes. Bulletin of the United States National Museum, 297: 1-347.
  • Pizzatto, L.; Dubey, S. 2012. Colour-polymorphic snake species are older. Biological Journal of the Linnean Society, 107: 210-218.
  • Rivas, L.R.; Mendoza-Miranda, P.; Miranda, O. 2022. Guía Ilustrada de Anfibios y Reptiles de la Ciudad de Trinidad, Bolivia Universidad Autónoma del Beni José Ballivián, Wildlife Conservation Society, Grupo de Trabajo para los Llanos de Moxos, Trinidad, 255p.
  • Silva, N.J. Jr. 1993. The snakes from Samuel Hydroelectric Power Plant and vicinity, Rondônia, Brazil. Herpetological Natural History, 1: 37-86.
  • Stafford, P.J.; Henderson, R.W. 1996. Kaleidoscopic Tree Boas: The Genus Corallus of Tropical America Krieger Publishing, Malabar , 86p.
  • Stephenson, B.P.; Velani, Z.; Ihász, N. 2022. The effect of albinism on avian predator attack rates in eastern garter snakes. Zoology, 150: 125987.
  • CITE AS:

    Rivas, L.R.; Eversole, C.B.; Crocker, A.V.; Powell, R.L. 2022. Two records of xanthism in Corallus hortulana (Serpentes: Boidae) in Bolivia with comments on the yellow, patternless morphotype. Acta Amazonica 53: 61-64.

Edited by

ASSOCIATE EDITOR:

Claudia Keller

Publication Dates

  • Publication in this collection
    23 Jan 2023
  • Date of issue
    Jan-Mar 2023

History

  • Received
    11 July 2022
  • Accepted
    24 Oct 2022
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