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ORNITOLOGIA NEOTROPICAL 22: 459–464, 2011 © The Neotropical Ornithological Society

NEST PREDATION BY ARBOREAL SNAKES ON CAVITY- NESTING BIRDS IN DRY CHACO WOODLANDS

Igor Berkunsky1, Federico P. Kacoliris2, Sarah I. K. Faegre3, Román A. Ruggera4, Joaquín Carrera2, & Rosana M. Aramburú2

1Grupo de Ecología Matemática, Instituto Multidisciplinario de Ecosistemas y Desarrollo Sustentable, Universidad Nacional del Centro de la Provincia de Buenos Aires, Paraje Arroyo Seco s/n (B7000GHG) Tandil, Argentina. E-mail: [email protected] 2División Zoología Vertebrados, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata. Paseo del Bosque s/n (1900) La Plata, Argentina. 3Rota Avian Behavioral Ecology Program, PO Box 1298, Rota, MP 96951, USA. 4Instituto de Ecología Regional, Universidad Nacional de Tucumán. C.C. 34 (4107) Yerba Buena, Tucumán, Argentina.

Depredación por serpientes arborícolas en aves nidificantes de cavidades en los bosques del Chaco Seco.

Key words: Blue-fronted Parrot, Amazona aestiva, Blue crowned Parakeet, Aratinga acuticaudata, Nar- row-billed Woodcreeper, Lepidocolaptes angustifrons, Crested Hornero, Furnarius cristatus, arboreal snakes, cavity nesting, nest predation.

INTRODUCTION on factors affecting nest success and to understand the dynamics of predator-prey Ornithologists have extensively studied nest relationships (Benson et al. 2010). predation because predators are responsible When predators have been documented, for most nest failures (Ricklefs 1969, Martin snakes were identified as the most important 1995, Newton 1998). Factors correlated with group, accounting for up to 90% of all nest variation in the occurrence of predation on predation (Weatherhead & Blouin-Demers Neotropical birds have been intensively stud- 2004, Robinson et al. 2005, Weatherhead et al. ied and documented, but identity of predators 2010). Cavity nesting birds exhibit some char- has largely remained unknown (Larivière acteristics that could make them susceptible 1999, Lahti 2009). Knowledge of the identity to predation by arboreal snakes (Martin 1993, of predators is often necessary to accurately Christman & Dhondt 1997, Brightsmith focus conservation efforts for threatened spe- 2005). Accumulation of nestling feces inside cies as well as to interpret results of research the cavity produces a strong odor which

459 BERKUNSKY ET AL. could contribute to nest detection because long dry season (April–October, Gonzalez & snakes have a well-developed vomeronasal Flores 2010). (Jacobson’s) organ for detecting odor mole- Observations were collected from early cules (Conover 2007). October to late February in five consecutive Neotropical arboreal snakes have been breeding seasons (2002–2007) as part of a reported as common nest predators on open- parrot reproductive ecology monitoring pro- cup nests (Matheus et al. 1996, Robinson et al. gram. In each breeding season, we regularly 2005). Predation is also the main cause of nest monitored tree cavities that were used by failure for Neotropical cavity nesters (Auer et Blue-fronted Parrot (Amazona aestiva) and al. 2007). However, predators identities have Blue-crowned Parakeet (Aratinga acuticaudata). rarely been reported (Auer et al. 2007, We reached the entrance hole using climbing Berkunsky & Reboreda 2009, Renton & equipment. Active nests and empty cavities Brightsmith 2009, Berkunsky 2010) and, until were monitored regularly (on average every 3 this work, only a few studies have confirmed days and every 15 days respectively). cases of nest predation on Neotropical cavity We identified cavity nester species and we nesters by snakes (Koenig et al. 2007). recorded nest entrance height above ground The Dry Chaco region is one of the larg- (m), nest age (days), and snake presence (with est extensive forests of native dry forest in digital photographs and/or digital video). We South America (Gasparri & Grau 2009), identified snakes based on photographic ref- where more than 36 species of cavity-nesting erences (Cei 1993) and used age-specific birds occur (Cornelius et al. 2008). Arboreal markings and size to determine if individuals snakes are common in these woodlands, with were adults or juveniles. at least four reported species (Kacoliris et al. 2006, Berkunsky & Kacoliris 2008). While RESULTS several bird studies in the Chaco woodlands have reported the occurrence of nest preda- We observed nine predation events per- tion, none of these studies revealed the iden- formed by three snake species: Argentine tity of the nest predators (Erikson et al. 2001). Green Snake (Phylodrias baroni, Colubridae; 5 Here we report field observations cases, Fig. 1), Constrictor Boa (Boa constrictor recorded between 2002 and 2007 in Chaco occidentalis, Boidae; 2 cases), and Argentine Province, Argentina, on nest predation events Rainbow Boa (Epichrates cenchria alvarezii, performed by three snake species. Boidae; 2 cases). Snakes performing preda- tions were adults in all cases although we METHODS found a 0.65 m long juvenile Argentine Rain- bow Boa dead inside of an active Blue fronted Field observations were gathered at Loro Parrot (Amazona aestiva) nest on one occasion. Hablador Provincial Park and neighboring The snake had injuries and we think it was areas (25º48’00”S, 61º70’00”W, 170 m a.s.l.), attacked by one of the adult parrots. in the Chaco province, Argentina. The area is In most cases (eight of nine), we found a continuous dry forest dominated by White the snake inside of the cavity. In the ninth Quebracho Aspidosperma quebracho-blanco and case, because the nestling was equipped with Red Quebracho Schinopsis lorentzii. The cli- a radio-collar, we were able to find it in the mate is dry subtropical, with a marked sea- stomach of a 1.7 m Constrictor Boa in an sonality (75% of the 590 mm average annual underground burrow 50 m from the nest (IB rainfall occurs from November–March) and a and SIKF pers. observ.). In four of nine

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FIG. 1. Blue-crowned Parakeet nest, with nestlings killed by an Argentine Green Snake (Phylodrias baroni) on 8 January 2005, Loro Hablador Provincial Park, Chaco, Argentine (photograph: J. Carrera). opportunities, we observed the snakes attack- Additional remarks. As a part of a parrot moni- ing and/or swallowing nestlings. toring program, we visited empty tree cavities Cavity nesting bird species affected by every two weeks and often found individuals these predators were Blue-fronted Parrot of Argentine Rainbow Boa, Constrictor Boa, (four cases), Blue-crowned Parakeet (Aratinga and Flame snake (Oxyrhopus rhombifer inaequi- acuticaudata, three cases), and Narrow-billed fasciatus) inside those cavities. Woodcreeper (Lepidocolaptes angustifrons, one We also found Constrictor boas prowling case). Additionally, we documented another near active Blue-fronted Parrot nests on four predation event in an enclosed-nester, the occasions, all of which were at the nestling Crested Hornero (Furnarius cristatus, one case). stage. Snakes remained on the ground, near All predation events occurred in White Que- the main trunk (three cases) or on the nearest bracho (Aspidosperma quebracho-blanco), and tree (one case). nest entrances were on average 5.9 ± 0.24 m above ground. Successful attacks occurred DISCUSSION mainly during December (2 cases) and Janu- ary (5 cases) and all them were performed All successful predation events occurred dur- during the nestling stage (Fig. 2). ing nestling stage. This could be due to at least

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FIG. 2. Scores for the timing of successful (black dots) and unsuccessful (white dot) predation events. The duration of incubation (grey bars) and nestling (white bars) periods were obtained from previous works (Fraga 1980, Mezquida 2001, Berkunsky 2010). BFP: Blue-fronted Parrot, BCP: Blue-crowned Parakeet, NBW: Narrow-billed Woodcreeper, and CH: Crested Hornero. three factors. First, the nest could be easier to parents, usually the female, spends most of find during the nestling stage than the incuba- the time inside the nest. The only unsuccess- tion stage because of the strong odor pro- ful recorded predation attempt was during duced by accumulating nestling feces inside incubation resulting in a dead snake. the cavity. It is known that olfaction and Three arboreal snakes species (i.e., Argen- vomerolfaction are among the most impor- tine Green Snake, Constrictor Boa, and tant senses used by snakes to detect prey (Zug Argentine Rainbow Boa) were identified as et al. 2001). Also, parents enter and exit the predators of three cavity nesters (i.e., Blue- nest more frequently during nestling stage for fronted Parrot, Blue-crowned Parakeet, and nestling food provisioning. Second, nestlings Narrow-billed Woodcreeper) and of one tree in a late growing phase provide more energy enclosed-nester (i.e., Crested Hornero). Pre- than eggs and hatchlings. Third, in depredat- dation is responsible of 50% of nest losses in ing nests at the nestling stage, snakes would Blue fronted parrots (Berkunsky 2010). avoid encounters with adults. During nestling Besides the snakes reported here, only one period, parents spend less time inside the cav- bird, the Spot-winged Falconet (Spiziapteryx ity than during incubation, when one of the circumcinctus), was positively identified as

462 SHORT COMMUNICATIONS predator of Blue-fronted parrot nestlings Plata, Argentina. (Berkunsky 2010). Berkunsky, I., & F. P. Kacoliris. 2008. Oxyrhopus Random observations, such as those rhombifer inaequifasciatus (Flame snake): habits reported in this paper, provide clues about the and reproduction. Herpetol. Bull. 104: 41–42. predatory species but, however, do not allow a Berkunsky, I., & J. C. Reboreda. 2009. Nest-site fidelity and cavity reoccupation by Blue-fronted more detailed analysis since in most cases of parrots Amazona aestiva in the dry Chaco of predation the identity of the predator was not Argentina. Ibis 151: 145–150. determined. To achieve a better understand- Brightsmith, D. J. 2005. Competition, predation ing of the community of predators that affects and nest niche shifts among tropical cavity the cavity nesters of Chaco, studies involving nesters: ecological evidence. J. Avian Biol. 36: continuous nest monitoring would be needed. 74-83. Cei, J. M. 1993. Reptiles del noroeste, nordeste y ACKNOWLEDGMENTS este de Argentina. Herpetofauna de las Selvas Subtropicales, Puna y Pampas. Mus. Reg. Sci. We thank R. Rojas, J. Sardell, K. Jones, and J. Nat. Boll. (Torino) 14: 1–949. Melton for partnership and collaboration dur- Conover, M. R. 2007. Predator-prey dynamics: the ing fieldwork. We also thank the Dirección de role of olfaction. CRC Press, Boca Raton, Florida, USA. Fauna, Parques y Ecología of Chaco Province Cornelius, C., K. Cockle, N. Politi, I. Berkunsky, L. for granting permission for research. Susan Sandoval, V. Ojeda, L. Rivera, L. Hunter Jr., & Koenig, André Weller, and one anonymous K. Martin. 2008. Cavity-nesting birds in Neo- reviewer made valuable comments that tropical forests: cavities as a potentially limiting improved a previous version of this manu- resource. Ornitol. Neotrop. 19: 253–268. script. This study would not have been possi- Christman, B. J., & A. A. Dhondt. 1997. Nest pre- ble without the financial support of The dation in Black-capped chickadees: how safe Amazona Society (U.S. and U.K. divisions), are cavity nests? Auk 114: 769–773. Parrots International, The World Parrot Erikson, L. M., L. Edenius, V. Areskoug, & D. A. Trust, and numerous private donors. IB was Meritt. 2001. Nest-predation at the edge: an supported by fellowships from Consejo experimental study contrasting two types of edges in the dry Chaco, Paraguay. Ecography Nacional de Investigaciones Científicas y Téc- 24: 742–750. nicas de Argentina (CONICET) and the Fraga, R. 1980. The breeding of Rufous Hornero. Comisión de Investigaciones Científicas (Furnarius rufus). Condor 82: 58–68. (CIC). Gasparri, N. I., & R. H. Grau. 2009. Deforestation and fragmentation of Chaco dry forest in NW REFERENCES Argentina 1972–2007. Forest Ecol. Manag. 258: 913–921. Auer, S. K., R. D. Bassar, J. J. Fontaine, & T. E. Gonzalez, M. H., & O. K. Flores. 2010. Rainfall Martin. 2007. Breeding biology of passerines in analysis in chaco plains and its relationship with a subtropical montane forest in northwestern atmospheric circulation behavior and sea sur- Argentina. Condor 109: 321–333. face temperatures. Meteorológica 35: 53–66. Benson, T. J., J. D. Brown, & J. C. Bednarz. 2010. Kacoliris, F. P., I. Berkunsky, & J. Williams. 2006. Identifying predators clarifies predictors of nest Herpetofauna of the Argentinean impenetra- success in a temperate passerine. J. Anim. Ecol. ble Great Chaco. Phyllomedusa 5: 149–157. 79: 225–234. Koenig, S. E., J. Wunderle, & E. C. Enkerlin-Hoef- Berkunsky, I. 2010. Ecología reproductiva del Loro lich. 2007. Vines and canopy contact: a route hablador (Amazona aestiva) en el Chaco Argen- for snake predation on parrot nests. Bird Con- tino. Tesis Doc., Univ. Nacional de La Plata, La serv. Int. 17: 79–91.

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