Herpetology Notes, volume 14: 151-155 (2021) (published online on 22 January 2021)

Multiple observations of atypical colouration in Central American Agalychnis treefrogs (Anura: Phyllomedusidae)

Brandon A. Güell1,*, Manuel Sánchez Mendoza2,3, Steven Gallo Gutiérrez, David Garro Acuña, Dionisio Paniagua4, and César Barrio Amorós5

Atypical colouration has been widely documented individuals within this group (though albino, leucistic, across amphibian and reptile taxa (Bechtel, 1995) and other morphs are common in the pet trade). Here we and has been particularly well characterised in North report multiple observations of atypical colouration in American species (Hensley, 1959; Dyrkacz, 1981). It wild gliding treefrogs (Agalychnis spurrelli Boulenger, varies from complete albinism—the absence of any 1913) and red-eyed treefrogs (A. callidryas Cope, 1862) skin pigments including in the eyes—to leucism—the (Anura: Phyllomedusidae). absence of almost all skin pigments except for in the From 2017 to 2020, we opportunistically observed eyes—and different types of partial albinism that are five atypically coloured A. spurrelli at Shampoo Pond determined by the presence and activity of several in Piro (8.2455°N, 83.2045°W) and a rural pond 10 km kinds of chromatophores (Dyrkacz, 1981; Prüst, 1984; outside of Sierpe on Costa Rica’s Osa Peninsula (Table Bechtel, 1991). 1). In contrast to typical individuals that are green In anurans, atypical colouration has been documented with orange coloured flanks and feet (Fig. 1A), these in several species at both tadpole (Maneyro and Achaval, atypically coloured A. spurrelli were completely yellow 2004; Rodrigues and Oliveira-Filho, 2004; Mitchell and in colour but retained red irises and the white dorsal Mcgranaghan, 2005; Sanabria et al., 2010; Elgue et spots that are usually outlined by black (Duellman, al., 2013; Smith, 2014) and adult life stages (Hensley, 1970; Savage, 2002) (Fig. 1B). Interestingly, the 1959; Boschwitz, 1962; Petrovic, 1973; Sazima, 1974; individual we observed on July 22, 2017 retained black Dyrkacz, 1981; Toledo et al., 2011; Moraes and Kaefer, colouration on its dorsum which typically outlines 2015; Rios and Vinicius De Mira-Mendes, 2016; Rivera white spots, but the pattern was sporadic and irregular Prieto and Marín, 2017; Turner, 2017; Tavares-Pinheiro (Fig. 1E). All individuals were adult males, as apparent et al., 2020). However, almost every report is restricted by their size (Duellman, 1970; Savage, 2002), and to single, rare observations within one species. were each seen during unique explosive breeding Treefrogs of the genus Agalychnis Cope, 1864 include aggregations that are characteristic of this species (Scott some of the most colourful and well-studied frogs in and Starrett, 1974; Thompson et al., 2016; Güell and all of Central America, with A. callidryas as one of the González, 2019; Güell et al., 2019). In two cases, we most conspicuous and photographed species due to its observed the same individuals, evident by their number abundance, wide distribution, and charismatic appearance and location of dorsal white spots, within the same (Duellman, 1970; Savage, 2002). Despite this, we are breeding season. We saw the first individual on June 7th unaware of any reports of atypical colouration in wild and again on July 22nd of 2017 and the other on June 6th and again on June 16th of 2018, both at Shampoo Pond (Table 1). Agalychnis spurrelli males engage in intense scramble competition during explosive reproductive events and non-amplexed males commonly attempt 1 Department of Biology, Boston University, 5 Cummington Mall, Boston, Massachusetts 02215, USA. to dislodge amplexed males (Güell, et al., 2019). We 2 Tortugas Preciosas de Osa, Puerto Jiménez 60702, Costa Rica. did not observe atypically coloured frogs in amplexus, 3 Namá Conservation, Heredia 40101, Costa Rica. but in every case they performed normal scrambling 4 Surcos Tours, Puerto Jiménez 60702, Costa Rica. behaviours, including physical combat with competitors 5 Doc Frog Expeditions/CRWild, Uvita 60504 Costa Rica. and calling behaviour. Although we did not collect or * Corresponding author. E-mail: [email protected] measure these individuals, they were comparable in © 2020 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. size to other typically coloured males (Fig. 1C and D), 152 Brandon A. Güell�et al.

Figure 1. Comparative views of typical (A) and atypically coloured (B–E) adult Agalychnis spurrelli during explosive reproductive events on Costa Rica’s Osa Peninsula. Photos by Brandon A. Güell (A, C, D), Steven Gallo Gutiérrez (B), and Dionisio Paniagua (E). and they showed no visible signs of other physiological on individuals attacked and killed by avian predators (B. or behavioural abnormalities. However, one individual Güell pers. obs.). had scars on its dorsum (Fig. 1D), similar to those found Multiple observations of atypical colouration in Agalychnis treefrogs 153

Figure 2. Comparative views of typical (A and C) and atypically coloured (B and D) Agalychnis callidryas adults and tadpoles from Gamboa, Panamá. Photos by Brandon A. Güell (A and B) and Karen M. Warkentin (C and D). 154 Brandon A. Güell ����l.

Table 1. DateTable and location 1. Date and of atypicallylocation of colouredatypically Agalychniscoloured Agalychnis observations. observations. Ind = Individual.Ind = Individual. CRI CRI= Costa = Costa Rica, Rica, PAN = Panama. PAN = Panama.

Species Date Time Site Ind Sex Observer A. spurrelli 2017-05-20 10:30 Shampoo Pond, Osa Peninsula (CRI) 1 Male M. Sánchez 2017-06-07 8:00 Shampoo Pond, Osa Peninsula (CRI) 1 Male M. Sánchez

2017-07-22 7:04 Shampoo Pond, Osa Peninsula (CRI) 2 Male D. Paniagua

2018-06-06 7:15 Shampoo Pond, Osa Peninsula (CRI) 3 Male B. Güell

2018-06-16 9:20 Shampoo Pond, Osa Peninsula (CRI) 3 Male B. Güell

2019-07-15 9:30 Shampoo Pond, Osa Peninsula (CRI) 4 Male B. Güell

2020-07-21 5:43 Sierpe, Osa Peninsula (CRI) 5 Male S. Gallo and D. Garro A. callidryas 2009-07-02 NA Gamboa (PAN) 1 – K. Warkentin 2015-06-21 9:40 Experimental Pond, Gamboa (PAN) 2 Male B. Güell

On June 21, 2015 at 09:40 h we observed a single instance, complete heterochromia has been observed in atypically coloured male A. callidryas at Experimental typically coloured A. callidryas individuals in Quepos, Pond in Gamboa, Panamá (9.7150°N, 79.4214°W) (Fig. Costa Rica (Oscar Herrera pers. obs.). Many studies 2B). Similar to our observations of atypically coloured also suggest that albino individuals experience high A. spurrelli, this A. callidryas individual was completely mortality rates since the loss of pigmentation is often yellow but retained red irises. In 2009, an atypically associated with other congenital defects (Browder, coloured tadpole, that had hatched from an A. callidryas 1972; Bechtel, 1991; Sanabria et al., 2010) and may egg clutch collected from a pond in Gamboa, Panamá, increase susceptibility to predation (Bechtel, 1995). was found in a large mesocosm experiment (Fig. 2D; However, less is known about the consequences of K. Warkentin pers. obs.). The tadpole had significantly atypical colouration on adult reproductive ecology and reduced pigments on its head, body, and tail and also behaviour. For instance, whether leucism or albinism seemed to lack pigments in its eyes. affects how individuals find or attain mates is unknown. To our knowledge, this is the first record of any This may be particularly important for species, such as type of atypical colouration in the wild for the genus A. callidryas, that rely on visual cues for communication Agalychnis. The presence of typical colouration in the and reproduction (Jacobs et al., 2017) and warrants eyes and yellow pigments in the skin suggests that further study. most of the adult individuals we observed were xanthic individuals (Dyrkacz, 1981; Prüst, 1984; Bechtel, 1991). Acknowledgements. We thank Karen M. Warkentin for providing However, the A. spurrelli individual that retained black photographs of A. callidryas tadpoles and Randall R. Jiménez for pre-peer reviewing this article. pigment on its dorsum must also have had functional melanophores. Interestingly, all atypically coloured A. References spurrelli individuals we observed also had white dorsal spots. Bechtel, H.B. (1991): Inherited color defects: Comparison between Albinism and other colour abnormalities are humans and snakes. International Journal of Dermatology 30: considered to be extremely rare, with estimates of 243–246. Bechtel, H.B. (1995): Reptile and amphibian variants: colors, incidence ranging from 1 in 10,000–30,000 (Bechtel, patterns, and scales. 1995). Breeding populations of A. spurrelli on the Boschwitz, D. (1962): An albino specimen of Hyla arborea Osa Peninsula are large, with reported observations savignyi Audouin. Zoologischer Anzeiger 168: 213–216. of ~10,000 frogs during single reproductive events Browder, L.W. (1972): Genetic and embryological studies of 1 albinism in Rana pipiens. Journal of Experimental Zoology (Scott and Starrett, 1974; Güell and González, 2019). Thus, our repeated observations of atypically coloured 180: 149–155. A. spurrelli within and between breeding seasons may Duellman, W.E. (1970): The Hylid Frogs of Middle America. Monographs of the Museum of Natural History, University of simply reflect the large population densities at these Kansas 1–2: 1–753. sites. However, it could also suggest that rare mutations Dyrkacz, S. (1981): Recent instances of albinism in North American affecting colouration of the skin and eyes in Agalychnis amphibians and reptiles. Society for the Study of Amphibians species is more common than previously thought. For and Reptiles, Herpetological Circular, 11: 1–31. Multiple observations of atypical colouration in Agalychnis treefrogs 155

Elgue, E., Cruces, S., Pereira, G., Achaval-Coppes, F., Maneyro, R. Rodrigues, A., Oliveira-Filho, J. (2004): Natural history notes. (2013): Natural history notes. Leptodactylus gracilis (Duméril’s Leptodactylus ocellatus (Rã-manteiga). Tadpole albinism. Striped Frog). Albino tadpole. Herpetological Review 44: 123– Herpetological Review 35: 373. 124. Sanabria, E.A., Quiroga, L.B., Laspiur, A. (2010): First record of Güell, B.A., González, K. (2019): Mating mayhem. Frontiers in partial albinism and scoliosis in Odontophrynus occidentalis Ecology and the Environment 17: 128–128. tadpoles (Anura: Cycloramphidae). Brazilian Archives of Güell, B.A., González, K., Pedroso-Santos, F. (2019): Opportunistic Biology and Technology 53: 641–642. predation by two aquatic-feeding predators on an explosive- Savage, J.M. (2002): The Amphibians and Reptiles of Costa Rica: breeding aggregation of arboreal gliding treefrogs (Agalychnis A Herpetofauna between Two Continents, between Two Seas. spurrelli Boulenger, 1913; Anura: Phyllomedusidae) on the Osa Chigago, Illinois, USA, University of Chicago Press. Peninsula of Costa Rica. Herpetology Notes 12: 795–798. Sazima, I. (1974): An albino hylid frog, Phrynohyas mesophaea Hensley, M. (1959): Albinism in North American Amphibians (Hensel). Journal of Herpetology 8: 264–265. and Reptiles. East Lansing, Michigan, USA, Michigan State Scott, N.J., Starrett, A. (1974): An unusual breeding aggregation University. of frogs, with notes on the ecology of Agalychnis spurrelli Jacobs, L.E., Vega, A., Dudgeon, S., Kaiser, K., Robertson, J.M. (Anura: Hylidae). Bulletin of the Southern California Academy (2017): Local not vocal: assortative female choice in divergent of Sciences 73: 86–94. populations of red-eyed treefrogs, Agalychnis callidryas Smith, G.R. (2014): Leucistic wood frog tadpole (Lithobates (Hylidae: Phyllomedusinae). Biological Journal of the Linnean sylvaticus) from central Ohio. Bulletin of the Maryland Society 120: 171–178. Herpetological Society 50: 74–74. Maneyro, R., Achaval, F. (2004): Natural history notes. Tavares-Pinheiro, R., Costa-Campos, C.E., Kaefer, I.L. (2020): Melanophryniscus montevidensis (Darwins Toad). Albino A leucistic brilliant-thighed poison frog Allobates femoralis larvae. Herpetological Review 35: 261. (Dendrobatoidea). Herpetology Notes 13: 321–323. Mitchell, J., Mcgranaghan, L. (2005): Albinism in american Thompson, M.E., Donnelly, M.A., Mendoza, M.S. (2016): bullfrog (Rana catesbeiana) tadpoles from Virginia. Banisteria Natural history notes. Agalychnis spurrelli (Gliding Leaf Frog). 25: 51. Explosive breeding aggregation. Herpetological Review 46: Moraes, L.J.C.D.L., Kaefer, I.L. (2015): Leucism in the Amazonian 434–435. diurnal frog Anomaloglossus stepheni (Martins, 1989) (Anura: Toledo, L.F., Da Silva, N.R., Araújo, O.G.D.S. (2011): Albinism in Aromobatidae). Herpetology Notes 8: 179–181. two Amazonian frogs: Elachistocleis carvalhoi (Microhylidae) Petrovic, C.A. (1973): An “albino” frog, Eleutherodactylus and Lithobates palmipes (Ranidae). Herpetology Notes 4: 145– planirostris Cope. Journal of Herpetology 7: 49–51. 146. Prüst, E. (1984): Albinism in snakes. Litteratura Serpentium 4: Turner, G.S. (2017): A hypomelanistic Roth’s tree frog Litoria 6–15. rothii from North Queensland. Queensland Naturalist 55: 22. Rios, C.H.V., Vinicius De Mira-Mendes, C. (2016): Natural history notes. Hypsiboas semilineatus. Leucism. Herpetological Review 47: 277. Rivera Prieto, D.A., Marín, D. (2017): Atypical colororation in the yellow-striped poisonous frog, Dendrobates truncatus (Cope, 1861), in the Colombian Magdalena river valley. Cuadernos de Herpetologia 31: 33–35.

Accepted by Fabrício Oda