Herpetology Notes, volume 12: 795-798 (2019) (published online on 25 July 2019)

Opportunistic predation by two aquatic-feeding predators on an explosive-breeding aggregation of arboreal gliding treefrogs (Agalychnis spurrelli Boulenger, 1913; Anura: Phyllomedusidae) on the Osa Peninsula of Costa Rica

Brandon A. Güell1,*, Katherine González2, and Fillipe Pedroso-Santos3

Predation of the eggs and larvae of many anuran taxa breeding counterparts (e.g., Agalychnis callidryas Cope, is tractable to study and consequently well documented. 1862) and offer dense gatherings of attainable prey Predators of these life stages are taxonomically diverse — are limited to two studies (Roberts, 1994; Ortega- and include numerous species of invertebrates, fish, Andrade, 2008). Here, we document a rare observation amphibians, reptiles, birds, and mammals (Savage, of simultaneous opportunistic predation on explosively- 2002; Wells, 2010; Güell and González, 2019). breeding phyllomedusid treefrogs by avian and reptilian However, most information on predation of adults of predators in a lowland tropical rainforest pond on Costa many anuran species is largely anecdotal (Wells, 2010), Rica’s Osa Peninsula. particularly for species with elusive natural histories (but Predation events were observed and documented during see Toledo, 2005 for a review). Adult phyllomedusid the rainy season on June 19, 2018 by B.A.G. and K.G. treefrogs (Anura: Phyllomedusidae) are entirely arboreal and canopy-dwelling, making natural history observations difficult (Duellman, 1968; Duellman, 1970; Savage, 2002). Thus, most observations of adult phyllomedusid behaviour and natural history occur during short breeding periods when adults descend from the canopy to reproduce, laying their eggs on vegetation overhanging forest pools (Duellman, 1968; Savage, 2001). Predation on adult phyllomedusids remains poorly documented, but observations include predation by snakes (Savage, 2002; Falkenberg, et al., 2013), theraphosid spiders (Menin, et al., 2005; Jiménez- Arcos, et al., 2014), and large anurans (Alvares, et al., 2013). Reports of predation during the explosive- breeding of adult phyllomedusids — which have even narrower breeding phenologies than their prolonged

1 Department of Biology, Boston University, 5 Cummington Mall, Boston, MA, 02215, United States of America. 2 Department of Biology, Purdue University, 915 W. State Figure 1. Location of Shampoo Pond on Costa Rica’s Osa Street, West Lafayette, IN, 47907, United States of America. Peninsula inset with an aerial photo of the site. The dashed 3 Universidade Federal do Amapá, Departamento de Ciências outline on the inset image indicates the northwest section of Biológicas e da Saúde, Laboratório de Herpetologia. Macapá, the pond where the aggregation of Agalychnis spurrelli took AP, Brazil, CEP: 68.903-419. place and predation of adult frogs was observed. Inset photo * Corresponding author. E-mail: [email protected] by Cesar Barrio-Amorós. 796 Brandon A. Güell et al.

Figure 2. (A) Breeding aggregation of Agalychnis spurrelli and their egg clutches on palm leaves at Shampoo Pond in Osa Peninsula, Costa Rica. (B) Predation of an adult male A. spurrelli by an actively hunting adult Tigrisoma mexicanum. (C) One of the two observed opportunistic ‘sit-and-wait’ Caiman crocodilus predators situated under vegetation where A. spurrelli aggregations were most dense. Photos by Brandon A. Güell.

at Shampoo Pond; a large permanent pond measuring were left. Males, apparent by their considerably smaller ca. 3000 m2, on the Osa Peninsula of Costa Rica (Fig. size (Duellman, 1970; Savage, 2002; Ortega-Andrade, 1). Upon arrival at the pond at 05:30 h, we observed a 2008) outnumbered females at least 9:1. Contrary to single large breeding aggregation of gliding treefrogs, reports of A. spurrelli reproductive activity by Scott Agalychnis spurrelli Boulenger, 1913, concentrated in and Starrett (1974) from a different site on the Osa ca. 20 m2 of the northwest corner (Fig. 1). Frogs were Peninsula, intraspecific competition was high; males covering palm fronds and leaves of Ardisia opegrapha scrambled and fought for females, and attempted to Oersted, which overhung the pond surface from 1–8 m dislodge amplectant males (Fig. 2A). We also observed in height and extended across it for several meters (Fig. no bladder-filling or courtship behaviour by females 2; see also Thompson, et al., 2016). The aggregation which has been reported in other Ecuadorian (Vargas, appeared close to its peak of reproductive activity et al., 2000) and Costa Rican (Gray, 1997) populations. since frogs were not observed to be leaving the group Egg clutches were primarily laid on the upper side of (Fig. 1A). At 08:30 h, we conservatively estimated the palm and A. opegrapha leaves and covered most visible aggregation had reduced to 60% of its former size, and leaves where the aggregation was most dense (Fig. 2A). using point count estimates of frog densities per meter At 8:30 h we also noticed the presence of an adult tiger of occupied pond edge, similar to methods used by heron (Tigrisoma mexicanum, Swainson, 1834) perched Scott and Starrett (1974), assessed that ca. 2000 frogs on vegetation overhanging the pond, and two spectacled Predation by two aquatic-feeding predators on Agalychnis spurrelli 797 caimans (Caiman crocodilus Linnaeus, 1758) situated C. crocodilus are generalist aquatic predators relying in the pond under the foliage where the frog aggregation heavily on a diet of fishes, molluscs and crustaceans, was most dense (Fig. 2B–C). and rarely feed on terrestrial prey (Thorbjarnarson, We observed a total of five predation attempts 1993; Da Silveira and Magnusson, 1999; Hancock and by the tiger heron, of which four were successful. Kushlan, 2010). Caimans are also typically nocturnal Multiple predation attempts were made by the two hunters. Thus, our observation of T. mexicanum and caimans, with one successful capture. All attempts and C. crocodilus diurnally feeding on arboreal frogs successful captures by the heron and caimans were of suggests that the large explosive-breeding aggregation male A. spurrelli. We observed the tiger heron actively of A. spurrelli offered an infrequent, yet rich feeding hunting prey in an ‘upright’ posture (sensu Hancock opportunity for both predators, and provides a record of and Kushlan, 2010) by ‘head and neck swaying’ while two novel predators of adult phyllomedusid treefrogs. standing and walking slowly on branches near the edges of the frog breeding aggregation, then using a ‘bill thrust’ Acknowledgements. This study was supported by the technique (sensu Hancock and Kushlan, 2010) to seize National Science Foundation (NSF Research Grant; IOS- each frog. We observed the four successful captures 1354072 to K.M.W.), Sigma Xi (Grant-in-Aid-of-Research; between 8:50 h and 9:48 h. The heron handled each G2018031596022314 to B.A.G.), and Boston University (Teaching Fellowship to B.A.G.). We thank Karen Warkentin for prey item for several minutes, and in most cases used comments on an earlier version of this manuscript, Marvin López the central rachis of palm fronds, upon which it stood, to for helping identify vegetation, and Cesar Barrio-Amorós for the stun or kill frogs by hitting and rubbing them against the aerial photograph of Shampoo Pond and a pre-peer review. rachis until they became limp, before swallowing them whole. We observed frogs attempting to evade capture References by clinging to nearby vegetation and jumping away. Alvares, J.A., Solana, E., Foster, S.R. (2013): Agalychnis callidryas In one instance, we observed a frog clinging to a leaf (red-eyed treefrog). Predation. Herpetological Review 44: 117– for ~15 seconds before the heron managed to remove 118. it from the palm frond and successfully eat it. Another Da Silveira, R., Magnusson, W.E. (1999): Diets of spectacled managed to escape when the heron made a positional and black caiman in the Anavilhanas Archipelago, Central adjustment to the frog within its beak ~3 minutes after Amazonia, Brazil. Journal of Herpetology: 181–192. being caught. However, almost immediately we saw the Duellman, W.E. (1968): The genera of phyllomedusine frogs heron successfully capture and consume a different frog. (Anura: Hylidae). University of Kansas, Head and neck swaying are characteristic movements Duellman, W.E. (1970): The hylid frogs of Middle America. Monographs of the Museum of Natural History, University of of herons hunting terrestrial prey, and are thought to be Kansas 1-2: 1–753. used to obtain parallax for hunting difficult to catch prey Falkenberg, L.M., Protázio, A.S., Albuquerque, R.L., Mesquita, (Hancock and Kushlan, 2010). We observed the tiger D.O. (2013): Predation of Phyllomedusa nordestina (Anura: heron, which typically feeds on aquatic prey, using this Hylidae) by Leptodeira annulata (Serpente: Dipsadidae) in a technique to aid in catching these atypical, arboreal frog temporary pond. Herpetology Notes 6: 97–98. prey (Hancock and Kushlan, 2010). Gray, A. (1997): Observations on the biology of Agalychnis Contrary to the active hunting strategy of the heron, spurrelli from the Caribbean lowlands of Costa Rica. Journal of the two caimans exhibited sit-and-wait strategies the International Herpetological Society 22: 61–70. Güell, B.A., González, K. (2019): Mating mayhem. Frontiers in to opportunistically snatch dislodged males, which Ecology and the Environment 17: 128–128. probably fell due to intraspecific interactions. Frogs that Hancock, J., Kushlan, J.A. (2010): The Herons Handbook. A&C fell into the pool immediately swam to the water’s edge Black, and returned up into the trees. However, in one instance Jiménez-Arcos, V.H., Centenero-Alcala, E., Vásquez Reyes, L.D., at 9:42 h, after the predation activity from the heron Blair, C., Santa Cruz-Padilla, S.A. (2014): Agalychnis danicolor above dislodged a frog into the pond, we saw one of the (Mexican leaf treefrog). Predation. Herpetological Review 45: caimans successfully catch and eat a male frog. 677. Existing observations of predation by snakes, birds, Menin, M., De Jesus Rodrigues, D., De Azevedo, C.S. (2005): Predation on amphibians by spiders (Arachnida, Araneae) in and white-faced capuchin monkeys on adults of arboreal the Neotropical region. Phyllomedusa: Journal of Herpetology explosive-breeding phyllomedusids have been reported 4: 39–47. from much smaller breeding aggregations and consist of Ortega-Andrade, H.M. (2008): Agalychnis spurrelli Boulenger many observations of single-predation events (Roberts, (Anura, Hylidae): Variación, distribución y sinonimia. Papeis 1994; Ortega-Andrade, 2008). Both T. mexicanum and Avulsos de Zoologia 48: 103–117. 798 Brandon A. Güell et al.

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Accepted by Jim Labisko