Herpetology Notes, volume 13: 301-303 (2020) (published online on 14 April 2020)

Tadpole predation in the chemically defended Oophaga pumilio (Anura: Dendrobatidae) by Oxybelis aeneus (Squamata: Colubridae)

Bruce Sellmeijer1 and Matthijs P. van den Burg2,3,*

Defensive chemicals are widely used throughout their invertebrate prey, which consists largely of mites the tree of life as an antipredator mechanism, and and ants (Donnelly, 1991). Differences in alkaloid their acquisition can be endogenous or exogenous. defences among populations of O. pumilio have been The secretion of exogenously derived alkaloids explained by age, size, sex, geographic location, time, as a seemingly passive defence mechanism has and arthropod composition (Bolton et al., 2017; Prates evolved independently in anuran amphibians of et al., 2019). Despite having defensive alkaloids, there various families on different continents, e.g. within is still evidence of predation on adult O. pumilio (e.g. Eleutherodactylus (Eleutherodactylidae), Mantella birds, snakes, spiders, fish and invertebrates; Santos (Mantellidae), Melanophryniscus (Bufonidae), and Cannatella, 2011; Alvarado et al., 2013; Lenger et Pseudophryne (Myobatrachidae), and members of the al., 2014), though potential predators have also been family Dendrobatidae (Daly, 1998; Smith et al., 2002; reported to reject O. pumilio (Santos and Cannatella, Daly et al., 2007; Rodriguez et al., 2010). Aspects of 2011; Hovey et al., 2014). On the other hand, records alkaloid secretion, the dietary sources of alkaloids, and on O. pumilio tadpole predation are rare (but see Maple their physiological effects on potential predators have [2002] and Stynoski et al. [2014a]). been mainly studied in Dendrobatidae (Daly et al., Oophaga pumilio is widely known for its maternal 1992, 1994a, b; Wang et al., 2007; Tarvin et al., 2016; attending behaviour, with females transporting tadpoles Wang and Wang, 2017). Despite numerous studies and to water stored inside bromeliads, where they develop continued scientific interest into this system, accounts of solely on a diet of maternally provided unfertilized eggs predation and/or predator interactions with aposematic, (Weygoldt, 1980). Interestingly, recent studies identified chemically defended amphibian species are rare. that these unfertilized eggs are provisioned with Among Dendrobatidae, Oophaga pumilio (Schmidt, invertebrate-derived alkaloids, which are presumed to 1857) is a well-known and studied species of poison frog deter tadpole predation (Stynoski et al., 2014b; Saporito that exhibits aposematism (Saporito et al., 2006, 2007a). et al., 2019). However, to what extent these provisioned Similar to other poison frogs (Daly et al., 2002; Saporito alkaloids prevent tadpole predation has only been studied et al., 2007b), O. pumilio uptake dietary alkaloids from for three potential predators, two spider (Cupiennius sp. and C. coccineus) and one snake species (Leptodeira septentrionalis), and seemingly only prevents spider predation (Maple, 2002; Stynoski et al., 2014a). It is noteworthy that all recorded observations of O. pumilio tadpole predation have been nocturnal (Maple, 2002; 1 Bocas Dive Center, Calle 2da, Isla Colón, Panama. Stynoski et al., 2014a). 2 Department of Biogeography and Global Change, Museo Oxybelis aeneus (Wagler, 1824) is an arboreal vine Nacional de Ciencias Naturales (MNCN), Consejo Superior snake that occurs from the southwestern United States de Investigaciones Científicas (CSIC), C/ José Gutiérrez along the Pacific coast of Central America southwards Abascal 2, 28006 Madrid, Spain. to southeast Brazil, though recent research highlights 3 Institute of Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, P.O. Box 94248, 1090GE the potential presence of four species within what is Amsterdam, The Netherlands. currently called Oxybelis aeneus (Jadin et al., 2019). * Corresponding author. E-mail: [email protected] This diurnally active, rear-fanged snake is mildly 302 Bruce Sellmeijer & Matthijs P. van den Burg venomous and mainly encountered at heights below 2 Acknowledgements. We thank R. Saporito for providing m (Franzen, 1996). Oxybelis aeneus is regarded as a comments and recommendations that improved an earlier version generalist predator and has been observed preying on of this manuscript. vertebrates from multiple major taxa groups, including References amphibians, birds, fish and small mammals, but it mostly feeds on lizards (Henderson, 1982; Franzen, Alvarado, J.B., Alvarez, A., Saporito, R.A. (2013): Oophaga 1996; Hetherington, 2006; López-de La Cruz et al., pumilio (Strawberry Poison Frog), Predation. Herpetological 2016). However, predation by O. aeneus on poison Review 44: 298. Bolton, S.K., Dickerson, K., Saporito, R.A. (2017): Variable frogs has, to our knowledge, not yet been reported in alkaloid defenses in the Dendrobatid poison frog Oophaga the literature, and we were unable to find records from pumilio are perceived as differences in palatability to arthropods. online sources (GBIF, iNaturalist, Observado, and social Journal of Chemical Ecology 43: 273–289. media platforms). Daly, J.W. (1998): Thirty years of discovering arthropod alkaloids On 1 August 2019, on Isla Colón in Panama (GPS N° in amphibian skin. Journal of Natural Products 61: 162–172. 9.395994, W° -82.271355; Bocas Del Toro province), Daly, J.W., Secunda, S.I., Garraffo, H.M., Spande, T.F., Wisnieski, A., Nishihira, C., Cover Jr, J.F. (1992): Variability in alkaloid at 16:00h, while photographing individuals of Oophaga profiles in neotropical poison frogs (Dendrobatidae): genetic pumilio, we observed an adult Oxybelis aeneus predating versus environmental determinants. Toxicon 30: 887–898. on a stage >38 O. pumilio tadpole. The observed tadpole Daly, J.W., Garraffo, H.M., Spande, T.F., Jaramillo, C., Rand, was identical to those attended by adult O. pumilio in A.S. (1994a): Dietary source for skin alkaloids of poison frogs nearby bromeliads. The O. aeneus (~80 cm total length) (Dendrobatidae)? Journal of Chemical Ecology 20: 943–955. had plunged its head into standing water stored inside Daly, J.W., Secunda, S.I., Garraffo, H.M., Spande, T.F., Wisnieski, a bromeliad located approximately 1.5 m above the A., Cover Jr, J.F. (1994b): An uptake system for dietary alkaloids in poison frogs (Dendrobatidae). Toxicon 32: 657–663. ground. Upon disturbance, the snake removed its head Daly, J.W., Kaneko, T., Wilham, J., Garraffo, H.M., Spande, T. from the bromeliad and the tail of the tadpole could be F., Espinosa, A., Donnelly, M.A. (2002): Bioactive alkaloids observed sticking out from the snake’s mouth. While of frog skin: combinatorial bioprospecting reveals that swallowing the tadpole whole, the O. aeneus fled before pumiliotoxins have an arthropod source. Proceedings of the we could take a photograph of this reported observation. National Academy of Sciences 99: 13996–14001. We used the size and development of the tail to estimate Daly, J.W., Wilham, J.M., Spande, T.F., Garraffo, H.M., Gil, R.R., Silva, G.L., Vaira, M. (2007): Alkaloids in bufonid toads the tadpole stage. (Melanophryniscus): temporal and geographic determinants Although we present a single observation, it suggests for two Argentinian species. Journal of Chemical Ecology 33: that Oxybelis aeneus is able to withstand alkaloid 871–887. quantities as found in late stage O. pumilio tadpoles. As Donnelly, M.A. (1991): Feeding patterns of the strawberry poison we were unable to follow the adult O. aeneus, we do not frog, Dendrobates pumilio (Anura: Dendronatidae). Copeia know whether the tadpole was eventually regurgitated, 1991: 723–730. Franzen, M. (1996): Ökologische und morphologische Aspekte or whether the snake experienced any ill effects from einer Costaricanischen Population von Oxybelis aeneus (Wagler, the defensive alkaloids. Future work could assess the 1824) (Serpentes: Colubridae). Herpetozoa 9: 121–131. frequency of O. pumilio tadpole predation by Oxybelis Henderson, R.W. (1982): Trophic relationships and foraging aeneus, and whether this predator also preys upon strategies of some New World tree snakes (Leptophis, Oxybelis, adult O. pumilio. Also, although the spider Cupiennius Uromacer). Amphibia-Reptilia 3: 71–80. coccineus appears to be able to distinguish late stage Hetherington, T.E. (2006): Oxybelis aeneus (Brown Vinesnake), (37-45) alkaloid-containing tadpoles (Stynoski et al., Diet. Herpetological Review 37: 93–94. Hovey, K.J., Viloria, M.O., Saporito, R.A. (2014): Oophaga 2014a, b), ideally this should be assessed for other pumilio (Strawberry Poison Frog), Predator-prey interactions. predator species. Another hypothesis to assess would Herpetologial Review 47: 113–114. be whether tadpole predators do prey on younger Jadin, R.C., Blair, C., Jowers, M.J., Carmona, A., Murphy, O. pumilio tadpole stages (<30) that lack maternally J.C. (2019: Hiding in the lianas of the tree of life: molecular provisioned alkaloids (Saporito et al., 2019), and if they phylogenetics and species delimitation reveal considerable can distinguish them from alkaloid-free species. Lastly, cryptic diversity of New World vine snakes. Molecular Phylogenetics and Evolution 134: 61–65. the low number of predation reports suggests little is Lenger, D.R., Berkey, J.K., Dugas, M.B. (2014): Predation on the still known about Oophaga pumilio tadpole predation toxic Oophaga pumilio (Anura: Dendrobatidae) by Rhadinaea and how effective maternally provisioned alkaloids are decorata (Squamata: Collubridae). Herpetology Notes 7: 83– as a defence mechanism. 84. Tadpole predation in the chemically defended Oophaga pumilio 303

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Accepted by Clarissa Canedo