A Leucistic Brilliant-Thighed Poison Frog Allobates Femoralis (� ��Obatoidea�

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Herpetology Notes, volume 13: 321-323 (2020) (published online on 14 April 2020)

A leucistic brilliant-thighed poison frog Allobates femoralis (� ��obatoidea�

Rodrigo Tavares-Pinheiro1, Carlos Eduardo Costa-Campos1,*, Igor Luis Kaefer2

Several chromatic anomalies have been reported the characteristic yellowish spots on the upper arm at in anurans, the most frequent of which are melanism, the point of insertion and on the upper and rear side of albinism, and leucism (Toledo et al., 2011). Leucism the thigh (Fig. 1). This condition differs from albinism, occurs when the animal body is partially or totally a hypopigmentary anomaly characterized by complete depigmented, while remaining margins of the body absence of pigmentation, including the eyes, which and eyes remain pigmented (Miller, 2005; Henle et al., become pink or reddish (Miller, 2005). 2017). The loss of pigmentation is hardly observed in The individual was found active at 10:00 h on the natural populations because (1) it is associated with leaf litter of a primary dense forest area located in the morphological and immunological abnormalities municipality of Pedra Branca do Amapari, Amapá (Sanabria et al., 2010), and (2) it negatively selects State, Brazil (GPS: 0.7918°N, 51.9783°W). This area is individuals because they become more visible to located within the Extractive Reserve Beija-Flor-Brilho- predators (Bechtel, 1995). Such selective pressures de-Fogo around the Igarapé Água Fria, a large tributary might be especially strong for anurans that are active of the Amapari River. The individual was photographed, during the day and therefore more vulnerable to collected and deposited in the Herpetological Collection visually-oriented predators. In spite of this, recent of the Universidade Federal do Amapá (Macapá, Brazil) publications have reported leucism in diurnal anurans, under the voucher CECC 3521. The only other species such as in the dendrobatoids Dendrobates truncatus of cryptically coloured frogs found in this region are (Cope, 1861) (Rivera-Prieto and Marín-C, 2017), and Anomaloglossus baeobatrachus (Boistel and Massary, Anomaloglossus stepheni (Martins, 1989) (Moraes and 1999) and Ameerega pulchripecta (Silverstone, 1976), Kaefer, 2015). which significantly differ from Allobates femoralis in Here we report leucism for the brilliant-thighed external morphology (Lötters et al., 2007). poison frog Allobates femoralis (Boulenger, 1884) Despite having pan-Amazonian distribution and (Dendrobatoidea: Aromobatidae), a forest-dependent being one of the most extensively studied anurans from species distributed throughout the Amazon basin (Frost, the biome (e.g., Lougheed et al., 1999; Amézquita 2020). On 10 December 2019, we found a juvenile et al., 2009; Kaefer et al., 2012; Simões et al., 2014; of Allobates femoralis (26.8 mm snout-vent length, Stückler et al., 2019), this is the first report of leucism unknown sex) with a marked reduction of dark pigment in Allobates femoralis. This taxon likely comprises a (melanin) in the whole-body skin, as compared to an number of similar, undescribed species behind its name individual with normal colouration. The individual (Montanarin et al., 2011; Grant et al., 2017), which retained dark pigmentation in the iris and pupil, on the engage in mimicry with species of Aromobatidae, dorsal portion of the head, as well as on the limbs, and Dendrobatidae, Leptodactylidae and Craugastoridae that also show bright yellow, orange or red femoral patches contrasting against a dark body (Amézquita et al., 2017). Considering that the femoral patches act as aposematic signals when contrasting to a dark 1 �� background (Amézquita et al., 2017), and the absence Biol�� of alkaloids in skin secretions of the group (Saporito and 419, Macap�� 2 Instituto de Ciências Biológicas, Universidade Federal do Grant, 2018), it is likely that leucistic individuals of A. Amazonas, 69067-005, Manaus, Amazonas, Brazil. femoralis might be more vulnerable to predation when * Corresponding author. E-mail: [email protected] compared to the normal co-specifics. 322 Rodrigo Tavares-Pinheiro et al.

Figure 1. Comparative dorsolateral view of normal (A) and leucistic (B) Allobates femoralis (Boulenger, 1884) from eastern Amazonia, Brazil. Details of head (C) and venter (D) of the leucistic individual (voucher CECC 3521).

Leucism is considered as a hypopigmentary congenital Acknowledgments. We are grateful to Secretaria Municipal disorder that reflects low genetic diversity levels and do Meio Ambiente (SEMAM) of Pedra Branca do Amapari for the expression of deleterious recessive alleles in the logistical support and the opportunity to carry out research on the Reserva Extrativista Beija-Flor-Brilho-de-Fogo; Instituto population, being commonly associated with increased Chico Mendes de Conservação da Biodiversidade (ICMBio/ inbreeding (Bensch et al., 2000; Frankham, 2003). Given SISBIO #48102-2) and SEMAM (process #011/2019) for capture that the recent reports of leucism in Amazonian anurans permits; Samuel Farias and Rilton Nascimento for their support come from dendrobatoids found in relatively pristine during field work; Lucas Ferrante and Renato Nali for comments habitats (Moraes and Kaefer, 2015; Rivera-Pietro and on an earlier version of this manuscript. This study is part of the Marín-C, 2017; this study), life history traits of the project “Natural history of anuran amphibians from the eastern Amazon”. group such as territoriality, low vagility and pronounced genetic structure (Kaefer et al., 2013; Simões et al., 2014) References could be associated with inbreeding and consequent expression of recessive alleles. However, further reports Amézquita, A., Lima, A.P., Jehle, R., Castellanos, L., Ramos, O., of chromatic anomalies in frogs are needed for a better Crawford, A.J., Gasser, H., Hödl, W. (2009): Calls, colours, comprehension of the causes and consequences of this shapes, and genes: A multi-trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. phenomenon in nature. Biological Journal of the Linnean Society 98: 826–838. Amézquita, A., Ramos, Ó., González, M.C., Rodríguez, C., Medina, I., Simões, P.I., Lima, A.P. (2017): Conspicuousness, color A leucistic brilliant-thighed poison frog Allobates femoralis 323

resemblance, and toxicity in geographically diverging mimicry: Martins, M. (1989): Nova espécie de Colostethus da Amazonia The pan-Amazonian frog Allobates femoralis. Evolution 71: central (Amphibia: Dendrobatidae). Revista Brasileira de 1039–1050. Biologia 49: 1009–1012. Bechtel, H.B. (1995): Reptile and amphibian variants: colors, Miller, J.D. (2005): All about albinism. Missouri Conservationist patterns and scales. Malabar, F.L., Krieger Publishing. 66: 5–7. Bensch, S., Hansson, B., Hasselquist, D., Nielsen, B. (2000): Partial Montanarin, A., Kaefer, I.L., Lima, A.P. (2011): Courtship and albinism in a semi-isolated population of Great Reed Warblers. mating behaviour of the brilliant-thighed frog Allobates femoralis Hereditas 133: 167–170. from Central Amazonia: implications for the study of a species Boistel, R., Massary, J.C. De. (1999): Les amphibiens vénéneux de complex. Ethology, Ecology and Evolution 23: 141–150. la famille des dendrobatidés. Le Courier de la Nature 176: 34– Moraes, L.J.C.L., Kaefer, I.L. (2015): Leucism in the Amazonian 39. diurnal frog Anomaloglossus stepheni (Martins, 1989) (Anura: Boulenger, G.A. (1884): On a collection of frogs from Yurimaguas, Aromobatidae). Herpetology Notes 8: 179–181. Huallaga River, Northern Peru. Proceedings of the Zoological Rivera-Prieto, D.A., Marín-C, D. (2017): Atypical coloration in the Society of London 1883: 635–638. yellow-striped poisonous frog, Dendrobates truncatus (Cope, Cope, E.D. (1861): Descriptions of reptiles from tropical America 1861), in the Colombian Magdalena river valley. Cuadernos de and Asia. Proceedings of the Academy of Natural Sciences of Herpetología 31: 33–35. Philadelphia 12: 368–374. Sanabria, E.A., Quiroga, L.B., Laspiur, A. (2010): First record of Frankham, R. (2003): Genetics and Conservation Biology. Comptes partial albinism and scoliosis in Odontophrynus occidentalis Rendus Biologies 326: S22–S29. tadpoles (Anura: Cycloramphidae). Brazilian Archives of Frost, D.R. (2020): Amphibian Species of the World: an Online Biology and Technology 53: 641–642. Reference. Version 6.0. American Museum of Natural History, Saporito, R.A., Grant, T. (2018): Comment on Amézquita et al. New York. Available at: http://research.amnh.org/herpetology/ (2018) “Conspicuousness, color resemblance, and toxicity in amphibia/index.html. Accessed on 16 March 2020. geographically diverging mimicry: The pan-Amazonian frog Grant, T., Rada, M., Anganoy-Criollo, M., Batista, A., Dias, P.H., Allobates femoralis”. Evolution 72-4: 1009–1014. Jeckel, A.M., Machado, D.J., Rueda-Almonacid, J.V. (2017): Silverstone, P.A. (1976): A revision of the poison-arrow frogs of Phylogenetic Systematics of Dart-Poison Frogs and Their the genus Phyllobates Bibron in Sagra (family Dendrobatidae). Relatives Revisited (Anura: Dendrobatoidea). South American Science Bulletin. Natural History Museum of Los Angeles Journal of Herpetology 12: S1–S90. County 27: 1–53. Henle, K., Dubois, A., Vershinin, V. (2017): Commented glossary, Simões, P.I., Stow, A., Hödl, W., Amézquita, A., Farias, I.P., Lima, terminology and synonymies of anomalies in natural populations A.P. (2014): The value of including intraspecific measures of of amphibians. Mertensiella 25: 9–48. biodiversity in environmental impact surveys is highlighted Kaefer, I.L., Montanarin, A., Costa, R.S., Lima, A.P. (2012): by the Amazonian brilliant-thighed frog (Allobates femoralis). Temporal Patterns of Reproductive Activity and Site Attachment Tropical Conservation Science 7: 811–828. of the Brilliant-Thighed Frog Allobates femoralis from Central Stückler, S., Ringler, M., Pašukonis, A., Weinlein, S., Hödl, Amazonia. Journal of Herpetology 46: 549–554. W., Ringler, E. (2019): Spatio-Temporal Characteristics of Kaefer, I.L., Tsuji-Nishikido, B.M., Mota, E.P., Farias, I.P., Lima, the Prolonged Courtship in Brilliant-Thighed Poison Frogs, A.P. (2013): The Early Stages of Speciation in Amazonian Allobates femoralis. Herpetologica 75: 268–279. Forest Frogs: Phenotypic Conservatism Despite Strong Genetic Toledo, L.F., Sazima, I., Haddad, C.F.B. (2011): Behavioural Structure. Evolutionary Biology 40: 228–245. defences of anurans: an overview. Ethology Ecology & Lötters, S., Jungfer, K.H., Henkel, H.W., Schmitz, W. (2007): Evolution 23: 1–25. Poison Frogs: Biology, Species & Captive Husbandry. Frankfurt/ Main, Chimaira. Lougheed, S.C., Gascon, C., Jones, D.A., Bogart, J.P., Boag, P.T. (1999): Ridges and rivers: a test of competing hypotheses of Amazonian diversification using a dart-poison frog (Epipedobates femoralis). Proceedings of the Royal Society B: Biological Sciences 266: 1829–1835.

Accepted by Renato Nali