Usually, incited by fear, prey try to detect stimuli that announce the presence of predators, which, in turn, must develop strategies to remain imperceptible. Although this relationship traditionally involves the consumption of prey, predators can also affect their prey through predator-induced alterations in foraging, habitat use, or morphology. These alterations in prey traits, resulting from non-consumptive effects, were investigated through different stimuli induced by artificial snakes on the anti-predator behavior of birds when foraging upon Morus nigra trees. Experiments were developed for each type of snakes static position reflected different states of foraging behavior adopted by snakes (i.e., sit-and-wait, coiled, and active foraging) using three treatments: artificial snake, snake-shaped mimicry, and control (i.e., no stimulus). Regardless of the behavior adopted by snakes, the models caused drastic changes to the behaviors of birds. The other treatments did not trigger behavioral changes, except for the snake-shaped mimicry treatment, which simulated a coiled snake. This study demonstrates how birds perceive and respond to different predator-like stimuli, highlighting the cognitive and behavioral abilities of vertebrates.
Predators control prey populations through a combination of consumptive and non-consumptive effects. We investigated the effects of non-consumptive effects induced by different stimuli emitted by tree snakes on the anti-predatory behaviors of neotropical frugivorous birds when foraging upon M. nigra. Our results revealed that they react to predation risk by identifying conspicuous visual signals of their predators and therefore alter their foraging behavior, resulting in a decreased fruit-collecting rate. In addition, we presented a new perspective on the cognitive and learning capacities of neotropical frugivorous birds, investigating some attributes they use to locate and identify their predators.
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Abrams PA (1995) Implications of dynamically-variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134
Altmann SA (1956) Avian mobbing behavior and predator recognition. Condor 58:241–253
Barnea A, Yom-Tov Y, Friedman J (1992) Effect of frugivorous birds on seed dispersal and germination of multi-seeded fruits. Acta Oecol 13:209–219
Bernot R, Turner A (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146
Breviglieri CPB, Piccoli GC, Uieda W, Romero GQ (2013) Predation-risk effects of predator identity on the foraging behaviors of frugivorous bats. Oecologia 173:905–912
Brinkerhoff RJ, Haddad NM, Orrock J (2005) Corridors and olfactory predator cues affect small mammal corridors. J Mammal 86:662–66
Brown JS, Kotler BP, Bouskila A (2001) Ecology of fear: foraging games between predators and prey with pulsed resources. Zool Ann Fenn 38:71–87
Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399
Burger J, Gochfeld M, Murray BG Jr (1991) Role of a predator’s eye size in risk perception by basking black iguana, Ctenosaura similis. Anim Behav 42:471–476
Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago
Davidson GL, Butler S, Fernández-Juricic E, Thornton A, Clayton NS (2014) Gaze sensitivity: function and mechanisms from sensory and cognitive perspectives. Anim Behav 87:3–15
Dominey WJ (1983) Mobbing in colonially nesting fishes, especially the bluegill, Lepomis macrochirus. Copeia 1983:1086–1088
Durner GM, Gates JE (1989) Spatial ecology of black rat snakes of Remington Farms, Maryland. J Wildlife Manage 57:812–826
Fitzgerald M, Shine R, Lemckert F (2002) Spatial ecology of arboreal snakes (Hoplocephalus stephensii, Elapidae) in an eastern Australian forest. Aust Ecol 27:537–545
Fraga R, Lima AP, Prudente ALC, Magnusson WE (2013) Guide to the snakes of the Manaus region-Central Amazonia. INPA, Manaus
Hartmann PA, Marques OAV (2005) Diet and habitat use of two sympatric species of Philodryas (Colubridae), in south Brazil. Amphibia-Reptilia 26:25–31
Hernández L, Laundré JW (2005) Foraging in the ‘landscape of fear’ and its implications for habitat use and diet quality of elk (Cervus elaphus) and bison (Bison bison). Wildlife Biol 11:215–220
Hossie TJ, Sherratt TN (2013) Defensive posture and eyespots deter avian predators from attacking caterpillar models. Anim Behav 86:383–389
Hossie TJ, Sherratt TN (2014) Does defensive posture increase mimetic fidelity of caterpillars with eyespots to their putative snake models? Curr Zool 60:76–89
Hunter LTB, Skinner JD (1998) Vigilance behavior in African ungulates: the role of predation pressure. Behaviour 135:195–211
Janzen DH, Hallwachs W, Burns JM (2010) A tropical horde of counterfeit predator eyes. P Natl Acad Sci USA 107:11659–11665
Jones RB (1980) Reactions of male domestic chicks to two-dimensional eye-like shapes. Anim Behav 28:212–218
Jordano P, Garcia C, Godoy JA, Garcia-Castanõ JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. P Natl Acad Sci USA 104:3278–3282
Koenig SE, Wunderle JM, Enkerlin-Hoeflich ECJR (2007) Vines and canopy contact: a route for snake predation on parrot nests. Bird Conserv Int 17:79–91
Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7
Lima SL (1998) Non-lethal effects in the ecology of predator-prey interactions. Bioscience 48:25–34
Lima S, Bednekoff P (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
Lorenzi H, Bacher L, Lacerda M, Sartori S (2006) Frutas brasileiras e exóticas cultivadas: de consumo in natura. Instituto Plantarum de Estudos da Flora, São Paulo
Lorenzi H, Souza HM, Torres MAV, Bacher LB (2003) Árvores Exóticas no Brasil: madeiras, ornamentais e aromáticas. Platarum, Nova Odessa
Lučan RK, Šálek M (2013) Observation of successful mobbing of an insectivorous bat, Taphozous nudiventris (Emballonuridae), on an avian predator, Tyto alba (Tytonidae). Mammalia 77:235–236
Marques OAV, Eterovic A, Strüssmann C, Sazima I (2005) Serpentes do Pantanal (Guia Ilustrado). Holos Editora, São Paulo
Martins M (1993) Why do snakes sleep on the vegetation in central Amazonia? Herp Rev 24:83–84
Ostrow BD (2006) Bald eagle kills crow chasing a hawk. Wilson J Ornithol 118:569–570
Petranka JW, Kats LB, Sih A (1987) Predator-prey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish. Anim Behav 35:420–42
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.Rproject.org/
Ripple WJ, Beschta RL (2006) Linking wolves to willows via risk-sensitive foraging by ungulates in the northern Yellowstone ecosystem. Forest Ecol Manag 230:96–106
Robinson WD, Rompré G, Robinson TR (2005) Videography of Panama bird nests shows snakes are principal predators. Ornitol Neotrop 16:187–195
Rolim GS, Camargo MBP, Lania DG, Moraes JFL (2007) Classificação climática de Köppen e de Thornthwaite e sua aplicabilidade na determinação de zonas agroclimáticas para o Estado de São Paulo. Bragantia 66:711–720
Romero GQ, Koricheva J (2011) Contrasting cascade effects of carnivores on plant fitness: a meta-analysis. J Anim Ecol 80:696–704
Romero GQ, Antiqueira PAP, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behaviour. PLoS One 6:e20689
Sih A, McCarthy TM (2002) Prey responses to pulses of risk and safety: testing the risk allocation hypothesis. Anim Behav 63:437–443
Skutch AF (1985) Clutch size, nesting success, and predation on nests of neotropical birds, reviewed. Ornithol Monogr 36:575–594
Sordahl TA (1990) The risks of avian mobbing and distraction behavior: an anecdotal review. Wilson Bull 102:349–352
Stevens GC (1987) Lianas as structural parasites: the Bursera simaruba example. Ecology 68:77–81
Templeton CN, Greene E, Davis K (2005) Allometry of alarm calls: black-capped chickadees encode information about predator size. Science 308:1934–1937
Valeix M, Loveridge AJ, Chamaillé–Jammes S, Davidson Z, Murindagomo F, Fritz H, Macdonald ADW (2009) Behavioral adjustments of African herbivores to predation risk by lions: spatiotemporal variations influence habitat use. Ecology 90:23–30
Weatherhead PJ, Blouin-Demers G (2004) Understanding avian nest predation: why ornithologists should study snakes. J Avian Biol 35:185–190
The authors thank the Graduate Ecology Program of the State University of Campinas (UNICAMP). CPBB received a post-doctorate scholarship from the National Post-doctoral Program/Brazilian Federal Agency for the Support and Evaluation of Graduate Education (Programa Nacional de Pós-Doutorado/Coordination for the Improvement of Higher Education Personnel—PNPD/CAPES). GQR received a research scholarship from the Brazilian National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq). Thanks to the Betânia Inn for granting access to its property, where we developed part of the field experiments. We thank Paulo Sérgio Bernarde and Guilherme Amaral for giving in the pictures included in Fig. 1. The authors thank Nicky Clayton and two anonymous reviewers for their valuable comments on the manuscript.
We confirm that there are no competing interests for any of the authors. All research presented in the manuscript was conducted in accordance with all applicable laws and rules set forth by their governments and institutions. The access of researchers areas of study and the development of methodological procedures were authorized by the team responsible for Núcleo Picinguaba subordinate to the PESM, and the owner of the Inn Bethany. During our experiment, none of the vertebrate species involved was captured or even manipulated, because it is non-invasive methods. Therefore, specific licenses for capture, transport, or collection agencies are not required. It is also worth mentioning that the species of birds filmed throughout this study are not categorized in any degree of threat or are protected by law, according to state environmental agencies (SMA), national (MMA/IBAMA) or international (IUCN).
Communicated by N. Clayton
Electronic supplementary material
Below is the link to the electronic supplementary material.
Bird species that foraged upon Morus nigra during the experiment. (DOCX 555 kb)
Mobbing behavior in the presence of the snake models. (DOCX 344 kb)
Tangara seledon behavior (i.e., mobbing) in response to the snake model. (MPEG 29516 kb)
Tangara seledon behavior (i.e., mobbing) in response to the snake-shaped mimicry treatment using vines simulating “coiled” behavior. (MPEG 45488 kb)
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Breviglieri, C.P.B., Romero, G.Q. Snakes and forbidden fruits: non-consumptive effects of snakes on the behaviors of frugivorous birds. Behav Ecol Sociobiol 70, 777–783 (2016) doi:10.1007/s00265-016-2101-7
- Bird anti-predatory behavior
- Cognitive and behavioral abilities
- Predator cues
- Foraging behavior