ABSTRACT

Several bat species use caves as roosts and some of these caves can harbor high concentrations of individuals. Such caves may represent opportunities for certain predators, benefiting from the concentration of potential prey. Here, we report the predation of a Pteronotus bat by a Corallus hortulanus in the Brazilian Amazon. On three occasions over a year, individuals of C. hortulanus were observed around a cave that harbors populations containing tens of thousands of bats. On one occasion, an individual of this snake species was observed preying on a Pteronotus sp. as it left the cave. Our record extends the known diet for C. hortulanus, documenting the predation of a mormoopid bat by this snake species for the first time. This record reinforces the need for longitudinal studies at sites with exceptional bat populations to gain a deeper understanding of the ecological predator-prey relationships involving this diverse group of mammals.

KEYWORDS:
ambush predator; cave-dwelling bat; Chiroptera; Carajás National Forest; predator-prey interaction

RESUMO

Várias espécies de morcego usam cavernas como abrigo e algumas dessas cavernas podem abrigar altas concentrações de indivíduos. Tais cavernas podem representar oportunidades para determinados predadores, beneficiados pela concentração de presas potenciais. Aqui, relatamos a predação de um morcego Pteronotus por uma serpente Corallus hortulanus na Amazônia brasileira. Em três ocasiões ao longo de um ano, indivíduos de C. hortulanus foram observados na entrada e entorno de uma caverna que abriga populações contendo dezenas de milhares de morcegos. Em uma ocasião, um indivíduo dessa espécie de serpente foi observado predando um Pteronotus sp. ao emergir da caverna. Nosso registro amplia a dieta conhecida para C. hortulanus, documentando pela primeira vez a predação de um mormoopídeo por esta espécie de serpente. Este registro reforça a necessidade de estudos longitudinais em locais com populações excepcionais de morcegos para obtermos uma compreensão mais profunda das relações ecológicas predador-presa envolvendo esse diversificado grupo de mamíferos.

PALAVRAS-CHAVE:
predador de emboscada; morcego cavernícola; Chiroptera; Floresta Nacional de Carajás; interação predador-presa

Predator-prey coevolution is characterized as an inherently reciprocal process where the defensive adaptation of the prey results in a stronger selection of the predator to exploit such defenses (e.g., Brodie and Wilkinson 2010Brodie, E.D.; Wilkinson, A. 2010. Co-evolution of predators and prey. In: Breed, M.D.; Moore, J. (Ed.). Encyclopedia of Animal Behavior. Elsevier, Amsterdam, p.287-295.). Bats are known as predators of several species, and although non-phytophagous bats exploit a wide range of prey (i.e., insects, arachnids, small vertebrates), including groups displaying diverse adaptations to a more specialized diet (e.g., piscivorous, sanguivorous), there are very few natural predators specialized/adapted to hunt bats. Examples are the bat hawk, Macheiramphus alcinus Westermann, 1851, which feeds primarily on bats (Fenton et al. 1977Fenton, M.B.; Cumming, D.H.M.; Oxley, D.J. 1977. Prey of Bat Hawks and availability of bats. The Condor 9: 495-497.; Black et al. 1979Black, H.L.; Howard, G.; Stjernstedt, R. 1979. Observations on the feeding behavior of the Bat Hawk (Macheiramphus alcinus). Biotropica 11: 18-21.), the bat falcon, Falco rufigularis Daudin, 1800, whose dietary mammal component can be composed of up to 97% of bats (Beebe 1950Beebe, W. 1950. Home life of the Bat Falcon, Falco albigularis albigularis Daudin. Zoologica 35: 69-86.), and the Puerto Rican boa, Chilabothrus inornatus (Reinhardt, 1843), which is often reported ambushing at the entrance of bat roosts such as caves (e.g., Rodríguez-Durán 1996Rodríguez-Durán, A. 1996. Foraging ecology of the Puerto Rican Boa (Epicrates inornatus): bat predation, carrion feeding, and piracy. Journal of Herpetology 30: 533-536.). Bats are also opportunistically preyed upon by a large number of non-specialized predators, especially birds of prey, owls, and snakes, although records of natural predation (i.e., without any type of interference and/or human facilitation) are scarce in the literature (see Costa et al. 2016Costa, L.M.; Tabosa, L.O.; Luz, J.L.; Carvalho, W.D. 2016. Predadores naturais de morcegos no Brasil. Boletim da Sociedade Brasileira de Mastozoologia 77: 131-142.).

Mormoopid bats (Chiroptera) have a wide geographic distribution, occurring from the southwestern USA, throughout Central America to northeastern Brazil and northeastern Bolivia (Pavan 2019Pavan, A.C. 2019. Family Mormoopidae (ghost-faced, naked-backed and mustached bats). In: Wilson, D.E; Mittermeier, R.A. (Ed.). Handbook of the Mammals of the World: Bats . V.9. Lynx Edicions, Barcelona, p.424-443.). Pteronotus is the most specious genus of the Mormoopidae, with 16 currently recognized species (Pavan 2019). This genus is known to be obligate cave-dwelling where it forms large aggregations containing thousands of individuals (Rodríguez-Durán and Lewis 1987Rodríguez-Durán, A.; Lewis, R. 1987. Patterns of population size, diet and activity time for a multispecies assemblage of bats at a cave in Puerto Rico. Caribbean Journal of Science 23: 352-360.; Pavan 2019; Pimentel et al. 2022Pimentel, N.T.; Rocha, P.A.; Pedroso, M.A.; Bernard, E. 2022. Estimates of insect consumption and guano input in bat caves in Brazil. Mammal Research 67: 355-366.).

Boidae snakes mainly have ambush behavior (sit-and-wait predators), and the strategy of ambushing in places with greater flow/visitation of potential prey has been reported for some species (e.g., Rodríguez-Durán 1996Rodríguez-Durán, A. 1996. Foraging ecology of the Puerto Rican Boa (Epicrates inornatus): bat predation, carrion feeding, and piracy. Journal of Herpetology 30: 533-536.; Esbérard and Vrcibradic 2007Esbérard, C.E.L.; Vrcibradic, D. 2007. Snakes preying on bats: new records from Brazil and a review of recorded cases in the Neotropical Region. Revista Brasileira de Zoologia 24: 848-853.; Rocha-Santos et al. 2014Rocha-Santos, G.; Barbier, E.; Bordignon, M.O. 2014. Sweet trap: Boa constrictor (Serpentes: Boidae) preying on passerines on Cecropia pachystachya (Urticales: Cecropiaceae) in fruiting period. Biota Neotropica 14: e20140003.). The Amazon tree boa, Corallus hortulanus (Linnaeus, 1758), an arboreal boid snake that exhibits both active and ambush foraging, is the most widespread species of Corallus in South America and feeds mainly on birds and mammals (including bats) (Henderson 1997Henderson, R.W. 1997. A taxonomic review of the Corallus hortulanus complex of Neotropical Tree Boas. Caribbean Journal of Science 33: 198-221.; Scartozzoni and Molina 2004Scartozzoni, R.R.; Molina, F.D.B. 2004. Comportamento alimentar de Boa constrictor, Epicrates cenchria e Corallus hortulanus (Serpentes: Boidae) em Cativeiro. Revista de Etologia 6: 25-31.; Pizzatto et al. 2009Pizzatto, L.; Marques, O.A.V.; Facure, K. 2009. Food habits of Brazilian boid snakes: overview and new data, with special reference to Corallus hortulanus. Amphibia-Reptilia 30: 533-544.; Handerson and Pauers 2012Henderson, R.W.; Pauers, M.J. 2012. On the diets of Neotropical Treeboas (Squamata: Boidae: Corallus). South American Journal of Herpetology 7: 172-180.). In Brazil, as far as bats are concerned, this snake was previously recorded preying on Artibeus obscurus (Schinz, 1821), Artibeus sp., Carollia perspicillata (Linnaeus, 1758), Myotis sp., and Platyrrhinus lineatus (É. Geoffroy, 1810) (Barnett et al. 2007Barnett, A.; Schiel, V.; Deveny, A. 2007. Corallus hortulanus (Amazon tree boa): bat predation in Jaú National Park, Brazil. Herpetological Bulletin 100: 35-37.; Esbérard and Vrcibradic 2007; Pizzatto et al. 2009; Carvalho et al. 2019Carvalho, W.D.; Silvestre, S.M.; Mustin, K.; Hilário, R.R.; Toledo, J.J. 2019. Predation of an American fruit-eating bat (Artibeus sp.) by an Amazon tree boa (Corallus hortulanus) in the northern Brazilian Amazon. Acta Amazonica 49: 24-27.).

On April 1, 2022, during fieldwork for biomonitoring of caves in the Carajás National Forest, municipality of Parauapebas, Pará State, Brazil, the predation of a mustached bat (Pteronotus sp.) by a C. hortulanus was observed (in the cave N5SM2-0099; 06°08’09.2”S, 50°07’47.8”W; 480 m a.s.l.; Figure 1). Four species of Pteronotus shelter in sympatry in that cave: P. alitonus Pavan, Bobrowiec & Percequillo, 2018 (Amazonian common mustached bat), P. gymnonotus (Wagner, 1843) (big naked-backed bat), P. personatus (Wagner, 1843) (Wagner’s lesser mustached bat), and P. rubiginosus (Wagner, 1843) (Wagner’s common mustached bat). At least five other bat species use this cave: Carollia perspicillata, Glossophaga soricina (Pallas, 1766), Lampronycteris brachyotis (Dobson, 1879), Phyllostomus hastatus (Pallas, 1767), and Trachops cirrhosus (Spix, 1823).

Figure 1
Location of the cave where the predation of a mustached bat, Pteronotus sp. (Mormoopidae), by an Amazon tree boa (Corallus hortulanus) was recorded. This figure is in color in the electronic version.

On the same day of the predation event, we used a motion detection algorithm to automatically track and count the bats (Rodrigues et al. 2016Rodrigues, E.; Teixeira, J.M.; Teichrieb, V.; Bernard, E. 2016. Multi-objective tracking applied to bat populations. In: XVIII Symposium on Virtual and Augmented Reality, SVR 2016. IEEE Computer Society, Gramado, p.155-159. (https://ieeexplore.ieee.org/document/7517269)
https://ieeexplore.ieee.org/document/751... ; Otálora-Ardila et al. 2019Otálora-Ardila, A.; Torres, J.M.; Barbier, E.; Pimentel, N.T.; Leal, E.S.B.; Bernard, E. 2019. Thermally-assisted monitoring of bat abundance in an exceptional cave in Brazil’s Caatinga drylands. Acta Chiropterologica 21: 411-423.). The emergence of bats began at 18:00 h and lasted for 90 min (= 5,400 s), and our population census showed 88,464 bats sheltering in the cave, mostly Pteronotus spp. Therefore, during the emergence period, there were an average of 16 bats per second leaving the cave (88,464/5,400). The Amazon tree boa was initially observed around 17:00 h, resting next to the vegetation just above one of the cave entrances, where there is a large bat outflow (Figure 2a,b). With the beginning of the emergence of bats, the snake left its resting position and assumed a hunting posture, heading closer to the bat flow (Figure 2c). At around 19:00 h, that snake captured a Pteronotus sp. (an individual of P. alitonus or P. rubiginosus) by the head and constricted it (Figure 2d). From the time of our observation to the complete ingestion of the bat, about 40 min passed (Figure 2e,f).

Figure 2
Details of the predation event of a mustached bat, Pteronotus sp. (Mormoopidae), by an Amazon tree boa (Corallus hortulanus) in the Brazilian Amazon. A - Cave entrances, with emphasis on the place where C. hortulanus was observed (white circle); B - C. hortulanus resting before the beginning of the bat emergence; C - Emergence of Pteronotus bats and movement of the snake towards the outflow to ambush (white arrow); D - Capture and constriction of a Pteronotus sp. by C. hortulanus; E - Beginning of the bat’s ingestion; F - Finishing the bat’s ingestion; G - Example of another C. hortulanus observed around the cave, exhibiting a sit-and-wait behavior. This figure is in color in the electronic version.

We excluded the possibility that the preyed bat was a P. gymnonotus because this species has the membrane of the wings joined in the middle of the back, giving it the appearance of having a naked back (and this characteristic was not present in the preyed individual). We also excluded P. personatus because this is the smallest species occurring in the cave (body mass = 6.5-10 g; forearm length = 43-48 mm) (Pavan 2019Pavan, A.C. 2019. Family Mormoopidae (ghost-faced, naked-backed and mustached bats). In: Wilson, D.E; Mittermeier, R.A. (Ed.). Handbook of the Mammals of the World: Bats . V.9. Lynx Edicions, Barcelona, p.424-443.). Pteronotus alitonus has a mass of 18-26 g and a forearm of 59-64 mm, while P. rubiginosus has 20-27 g and 61-67 mm, respectively (Pavan 2019). This size discrepancy can be easily distinguished in situ. On the other hand, due to the similarity of the external morphological characteristics, we were not able to differentiate the preyed individual between P. alitonus and P. rubiginosus.

On the same night of predation, other smaller individuals (probably younger) of C. hortulanus were observed on the vegetation around the cave entrance. During our field expeditions in July 2021 and June and July 2022, we also observed C. hortulanus individuals around the same cave and hanging in lianas close to the main flight path used by bats during their emergence, but predation was not observed (Figure 2g). This aggregation of individuals of C. hortulanus in the same area, and in a time interval of 1 year, suggest this bat caves may be serving as a known and preferred ambush site of successful predation for this snake.

Roosting in large aggregations provides advantages, but also disadvantages such as attracting potential predators (Kunz and Fenton 2003Kunz, T.H.; Fenton, M.B. 2003. Bat Ecology. The University of Chicago Press, Chicago, 798p.). Bat caves that house thousands of bats have a higher temperature and strong odor (Ladle et al. 2012Ladle, R.J.; Firmino, J.V.; Malhado, A.C.; Rodríguez-Durán, A. 2012. Unexplored diversity and conservation potential of Neotropical hot caves. Conservation Biology 26: 978-982.), characteristics that can attract snakes. Indeed, the detection of potential prey by boid snakes seems to be an association of thermal, chemical, and visual stimuli (e.g., Cock Buning 1983Cock Buning, T. 1983. Thermal sensitivity as a specialization for prey capture and feeding in snakes. American Zoologist 23: 363-375.; Scartozzoni and Molina 2004Scartozzoni, R.R.; Molina, F.D.B. 2004. Comportamento alimentar de Boa constrictor, Epicrates cenchria e Corallus hortulanus (Serpentes: Boidae) em Cativeiro. Revista de Etologia 6: 25-31.). All these factors likely favor the location of bat caves by these snakes. The clustering behavior at cave entrances with high densities of bats has also been reported for C. inornatus (e.g., Rodríguez and Reagan 1984Rodríguez, G.A.; Reagan, D.P. 1984. Bat predation by the Puerto Rican Boa, Epicrates inornatus. Copeia 1984: 219-220.; Rodríguez-Durán 1996Rodríguez-Durán, A. 1996. Foraging ecology of the Puerto Rican Boa (Epicrates inornatus): bat predation, carrion feeding, and piracy. Journal of Herpetology 30: 533-536.). Studies using snake tagging, for example, may generate information on whether this behavior is restricted to a few individuals or if it is common to the species and shared.

Although bats emerge from the cave with considerable flight speed, the high number of individuals leaving at the same time should favor capture by snakes. Corallus hortulanus has the fastest lunge speed among four boid species, ranging between 90.91 and 151.52 cm sec^-1 (Charles 2007Charles, H.A. 2007. Comportamento predatório de serpentes (Boidae) de diferentes hábitos e biometria de crescimento e ecdises de Eunectes murinus Linnaeus, 1758 em laboratório. Master’s Dissertation, Universidade Federal do Rio de Janeiro (UFRJ), Brazil, 65p. (https://tede.ufrrj.br/jspui/handle/tede/188)
https://tede.ufrrj.br/jspui/handle/tede/... ). This attribute may favor the capture of moving prey, such as bats emerging from their diurnal roosts, in addition to thermal, chemical, and visual cues, as previously mentioned.

To the best of our knowledge, the only previous published records of predation by mormoopids in Brazil were by a spider (Lasiodora sp.) and anurans (Leptodactylus vastus Lutz, 1930 and Rhinella jimi (Stevaux, 2002)) (Gouveia et al. 2009Gouveia, S.F.; Rocha, P.A.; Mikalauskas, J.S.; Silveira, V.V-B. 2009. Rhinella jimi (Cururu Toad) and Leptodactylus vastus (Northeastern Pepper Frog): predation on bats. Herpetological Review 40: 210.; Dias et al. 2015Dias, S.C.; Rocha, P.A.; Bomfim, L.S.; Ferrari, S.F. 2015. Predação do morcego Pteronotus personatus (Mormoopidae) pela tarântula Lasiodora sp. (Theraphosidae, Araneae) em caverna no nordeste do Brasil. Biotemas 28: 173‑175.). In all these previous cases, the preyed bat was P. personatus. Therefore, this is the first documented trophic interaction event for C. hortulanus and Pteronotus and the third record of predators preying on a mormoopid in Brazil. While bats play a fundamental ecological role by preying on different taxonomic groups, they can also participate in the food web as important prey for other animals such as snakes.

A review of bat predation in Brazil showed that snakes, along with birds, are the main predators of this mammalian group, and those predations occurred mainly in the bat’s roost or its surroundings (Costa et al. 2016Costa, L.M.; Tabosa, L.O.; Luz, J.L.; Carvalho, W.D. 2016. Predadores naturais de morcegos no Brasil. Boletim da Sociedade Brasileira de Mastozoologia 77: 131-142.). So, roosts containing large aggregations of bats can be interesting sites for long-term trophic ecology studies involving the predation of these mammals. Among other matters of interest, this may indicate whether bats are predominant/preferred food items or they merely supplement the diet of their potential predators.

ACKNOWLEDGMENTS

We are grateful for the logistical support of the entire team at NGI-ICMBio-Carajás, FUNTEC-DF, and Vale S.A. We thank Pedro M.S. Nunes (Department of Zoology, UFPE) for the snake identification. This study was financed in part by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Brasil (Finance Code 001). E. Barbier was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) through a postdoctoral fellowship (grant #152672/2022-2), and is currently a postdoctoral fellow at the São Paulo Research Foundation (FAPESP; grant #2023/09610-8). N.T. Pimentel had a research grant from Instituto Brasileiro de Desenvolvimento e Sustentabilidade - IABS (76657/2022-2); and E. Bernard has a research productivity grant from CNPq.

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