Herpetology Notes, volume 12: 1011-1014 (2019) (published online on 17 October 2019)

Mixed-species bird flocks mob an Amazon treeboa (Corallus hortulanus) (Linnaeus, 1758) (Serpentes: Boidae) in the Southwest Brazilian Amazon

Odair Diogo da Silva1, Thatiane Martins da Costa2, Eder Correa Fermiano1, Almério Câmara Gusmão3, Dionei José da Silva1, and Paulo Sérgio Bernarde4,*

Snakes in Brazilian Amazon communities prey on Ecuador, Peru, Bolivia and Brazil, in the Amazon, several groups of animals (amphibians, lizards, rodents, Cerrado, Caatinga and Atlantic Rainforest biomes, birds, other snakes, fish, mollusks, earthworms, with its southern limit located in the state of São Paulo centipedes, among others), and birds may represent the (Hernderson, 1997; Bérnils et al., 2007). This species fourth most consumed item in some areas (Martins and exhibits nocturnal and arboreal habits, preying on small Oliveira, 1998; Bernarde and Abe, 2006). Colubridae mammals (rodents, marsupials and bats), birds, lizards, (such as Oxybelis fulgidus, Phrynonax polylepis and anuran amphibians and monkeys (Martins and Oliveira, Spilotes pullatus) and Boidae (such as Boa constrictor, 1998; Crasto-Astor et al., 1998; Pizzatto et al., 2009; Corallus hortulanus and Epicrates cenchria) are among Bernarde and Abe, 2010; Gonzalez et al., 2016; Ribeiro- the main families that include birds in their diets (Martins Júnior et al., 2016). During hunting, it use the hunting and Oliveira, 1998; Pizzatto et al., 2009; Scartozzoni et tactics of waiting or actively seeking prey on vegetation al., 2009; Bernarde and Abe, 2010). up to 25 m in height (Martins and Oliveira, 1998; Costa- The Amazon tree boa or garden tree boa, Corallus Silva and Henderson, 2012, 2013, 2014; Costa-Silva et hortulanus (Linnaeus, 1758), is the most widespread al., 2012). Several bird genera and species have been Boidae species, with one of the most extensive variations recorded as prey (e.g., Icteridae, Pipridae, Thraupidae, (geographic and ecological) among Neotropical snakes Turdidae, Tyrannidae, Alcedinidae, Caprimulgidae, (Henderson et al., 1995, 2013), occurring in Colombia Psittacidae, Rallidae) (Castro-Astor et al., 1998; Martins (eastern Andes), Venezuela, Guyana, Suriname, and Oliveira, 1998; Pizzatto et al., 2009; Costa-Silva et al., 2012, Henderson and Pauers, 2012; Costa-Silva and Henderson, 2013; Gonzalez et al., 2016), and records indicate that this snake actively seeks and captures these birds at night while they sleep perched on vegetation 1 Programa de Pós-Graduação em Ambiente e Sistemas de (Costa-Silva et al., 2012; Costa-Silva and Henderson, Produção Agrícola, Universidade do Estado de Mato Grosso. 2013). Rod. MT 358 Km 07, Caixa Postal 287, Jardim Aeroporto, The formation of mixed flocks by birds is recognized Tangará da Serra, MT, 78300000, Brazil. as a positive trait, leading to increased foraging 2 Programa de Pós-Graduação em Ciências Ambientais, efficiency and decreased predation risks (Harrison and Universidade do Estado de Mato Grosso, Centro de Pesquisa de Limnologia, Biodiversidade, Etnobiologia do Pantanal, Whitehouse, 2011; Goodale et al., 2015). Some birds Av. Santos Dumont, s/nº – Cidade Universitária (Bloco II), may display mobbing behavior in the presence of Cáceres, MT, 78200000, Brazil. potential threats, such as the presence of snakes, hawks 3 Programa de Pós-Graduação em Biotecnologia e and owls, attempting to distract, confuse or physically Biodiversidade, Rede Bionorte, Universidade do Estado de attack predators by performing strong vocalizations Mato Grosso. Av. Santos Dumont, s/nº – Cidade Universitária and conspicuous visual displays (Altmann, 1956; Caro, (Bloco II), Cáceres, MT, 78200000, Brazil. 2005; Cunha and Fontenelle, 2014). In Brazil, anti- 4 Laboratório de Herpetologia, Centro Multidisciplinar, Campus Floresta, Universidade Federal do Acre, Cruzeiro do Sul, predatory bird behavior against snakes has been reported Acre State, 69980000, Brazil for Boa constrictor (Boidae) (Cunha and Fontenelle, * Corresponding author. E-mail: [email protected] 2014), Bothrops jararaca (Viperidae) (Sazima, 2015a) 1012 Odair Diogo da Silva et al. and Philodryas olfersii (Dipsadidae) (Sazima, 2015b). On August 7, 2016 at 9:00 AM in the forest area of the In this context, the present study reports an attack of a Água Doce Reserve (11°26’10.7”S; 61°42’30.0”W), mixed flock composed of a bird species group against located in the southwest Brazilian Amazon in the state an adult Corallus hortulanus individual. of Rondônia (Brazil), a mixed bird flock, including

Figure 1. A1) Silver-beaked tanager (Ramphocelus carbo) female; A2) Thick-billed Euphonia (Euphonia laniirostris) male; A3) Barred antshrike Male (Thamnophilus doliatus) female; B) Amazon treeboa (Corallus hortulanus) in a tree; C) Amazon treeboa (C. hortulanus) on the ground with the wounds on the body. Photos by Odair Diogo da Silva. Mixed-species bird flocks mob an Amazon treeboa, Southwest Brazilian Amazon 1013

23 individuals belonging to: thick-billed Euphonia Acknowledgments. The authors would like to thank Mr. Jorge (Euphonia laniirostris, d’Orbigny & Lafresnaye 1837), Antônio Cavallet, owner of the study area, for logistical support. flycatcher (Myiarchus sp.), great kiskadee (Pitangus We would like to thank the doctorate (Author ACG) and masters (Authors ODS and TMC) scholarships provided by National sulphuratus, Linnaeus 1766), silver-beaked tanager Council for the Improvement of Higher Education (CAPES). (Ramphocelus carbo, Pallas 1764), white-lined tanager (Tachyphonus rufus, Boddaert 1783), tanager (Tangara References sp.), barred antshrike (Thamnophilus doliatus, Linnaeus 1764) and buff-throated saltator (Saltator maximus, Altmann, S.A. (1956): Avian mobbing behavior and predator Muller, 1776) (Fig. 1) was observed mobbing an adult recognition. Condor 58: 241–253. Bernarde, P.S., ABE, A.S. (2006): A snake community at Espigão individual of Corallus hortulanus (approximate size = do Oeste, Rondônia, Southwestern Amazon, Brazil. South 1.10 meter in length), located about 5.5 m high on a tree American Journal of Herpetology 1: 102–113. branch (Fig. 1B). The birds dived towards the snake Bernarde, P.S., ABE, A.S. (2010): Hábitos alimentares de serpentes and carried out both indirect (without physical contact) em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10: and direct attacks with their beaks against the snake for 167–173. approximately 12 minutes. During this event the birds Bérnils, R.S., Giraudo, A.R., Carreira, S., Cechin, S.Z. (2007): maintained constant vocalizations, while the snake Répteis das porções subtropical e temperada da região Neotropical. Ciência & Ambiente 35: 101–136. attempted to defend itself by delivering attacks, until it Caro, T. (2005): Antipredator defenses in birds and mammals. loosened its branch perch and fell to the ground. At this Chicago, USA, The University of Chicago Press. point the flock climb down (up to 20 - 100 cm from Castro-Astor, I.N., Correia, J.M.S., Alves, M.A.S. (1998): Corallus the ground) and persisted in the attacks for additional hortulanus (Deer Snake). Predation. Herpetological Review 29: 8 minutes, resulting in injuries to the snake’s head and 44. body (Fig. 1C). Costa-Silva, P., Henderson, R.W. (2012): Observations on foraging Records of snake-directed mobbing behaviour behavior in the Amazon treeboa (Corallus hortulanus). Herpetology Notes 5: 531–532. are sporadically documented with respect to attack Costa-Silva, P., Henderson, R.W. (2013): Predation on a purple towards birds of prey (Cunha and Fontenelle, 2014) gallinule (Porphyrio martinica) by an Amazon treeboa (Corallus and generally involve bird-preying species, such as B. hortulanus) on Ilha Grande, Piauí, Brazil. Herpetology Notes 6: constrictor, C. hortulanus, Leptophis ahaetulla and P. 233–234. olfersii (Matheus et al., 1996; Cunha and Fontenelle, Costa-Silva, P., Henderson, R.W. (2014): Natural history 2014; Sazima, 2015b), even if only on occasion (i.e. observations of Amazon treeboas (Corallus hortulanus) on three B. jararaca) (Sazima, 2015a). This behaviour is most Islands in the Parnaíba Delta, Brazil. IRCF Journal Reptiles & Amphibians: Conservation and Natural History 21: 86–92. probably a protection strategy, both for adult birds and Costa-Silva, P., Henderson, R.W., Tavares, A.A., Araújo, S.C.M., their nests, since C. hortulanus is a snake known to Guzzi, A. (2012): Observations on foraging and new prey actively predate on birds, and therefore representing a records for the Amazon treeboa (Corallus hortulanus, Squamata, potential risk to this group (Martins and Oliveira, 1998). Boidae). IRCF Journal Reptiles & Amphibians: Conservation As the event was observed during the morning and since and Natural History 19: 187–190. C. hortulanus mainly has a nocturnal activity (Martins Cunha, F.C.R., Fontenelle, J.C.R. (2014): Registros de tumulto and Oliveira, 1998), it is possible that the individual was em aves no Brasil: uma revisão usando a plataforma WikiAves. Atualidades Ornitológicas 177: 46–53. resting and that its presence was detected by the birds, Gonzalez, R.C., Silva-Soares, T., Crozariol, M.A., Citeli, N.K., which then initiated the attacks. In spite of previous Brito, G.R.R. (2016): Corallus hortulanus (Linnaeus, 1758) records of snakes scared away by physical attacks of (Squamata: Serpentes: Boidae) diet: Predation events on two birds, sometimes also resulting in precluding predatory Passeriformes at the Atlantic Rainforest, southeastern Brazil. success (Sazima, 2015a, 2015b; this study), there are Herpetology Notes 9: 87–89. also evidence for the mobbing failing to prevent the Goodale, E., Ding, P., Liu, X., Martínez, A., Si, X., Walters, M., predation (e.g. the predation of a young Golden-hooded Robinson, S.K. (2015): The structure of mixed-species bird flocks, and their response to anthropogenic disturbance, with tanager - Tangara larvata - by a Leptophis ahaetulla special reference to East Asia. Avian Research 6: 1–11. snake; Matheus et al., 1996). The mobbing report Harrison, N.M., Whitehouse, M.J. (2011): Mixed-species flocks: discussed in this study was effective in scaring away an example of niche construction? Animal Behaviour 81: 675– the snake, but further observations are needed to better 682. understand the success rate of this defence strategy. Henderson, R.W. (1997): A taxonomic review of the Corallus hortulanus complex of Neotropical tree boas. Caribbean Journal of Science 33: 198–221. 1014 Odair Diogo da Silva et al.

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Accepted by Angelica Crottini