Advertisement

Snakes and forbidden fruits: non-consumptive effects of snakes on the behaviors of frugivorous birds

Abstract

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.

Significance statement

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.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2

References

  1. 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

  2. Altmann SA (1956) Avian mobbing behavior and predator recognition. Condor 58:241–253

  3. 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

  4. Bernot R, Turner A (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146

  5. 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

  6. Brinkerhoff RJ, Haddad NM, Orrock J (2005) Corridors and olfactory predator cues affect small mammal corridors. J Mammal 86:662–66

  7. 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

  8. Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399

  9. 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

  10. Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

  11. 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

  12. Dominey WJ (1983) Mobbing in colonially nesting fishes, especially the bluegill, Lepomis macrochirus. Copeia 1983:1086–1088

  13. Durner GM, Gates JE (1989) Spatial ecology of black rat snakes of Remington Farms, Maryland. J Wildlife Manage 57:812–826

  14. 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

  15. Fraga R, Lima AP, Prudente ALC, Magnusson WE (2013) Guide to the snakes of the Manaus region-Central Amazonia. INPA, Manaus

  16. Hartmann PA, Marques OAV (2005) Diet and habitat use of two sympatric species of Philodryas (Colubridae), in south Brazil. Amphibia-Reptilia 26:25–31

  17. 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

  18. Hossie TJ, Sherratt TN (2013) Defensive posture and eyespots deter avian predators from attacking caterpillar models. Anim Behav 86:383–389

  19. 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

  20. Hunter LTB, Skinner JD (1998) Vigilance behavior in African ungulates: the role of predation pressure. Behaviour 135:195–211

  21. Janzen DH, Hallwachs W, Burns JM (2010) A tropical horde of counterfeit predator eyes. P Natl Acad Sci USA 107:11659–11665

  22. Jones RB (1980) Reactions of male domestic chicks to two-dimensional eye-like shapes. Anim Behav 28:212–218

  23. 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

  24. 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

  25. Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7

  26. Lima SL (1998) Non-lethal effects in the ecology of predator-prey interactions. Bioscience 48:25–34

  27. Lima S, Bednekoff P (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

  28. 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

  29. Lorenzi H, Souza HM, Torres MAV, Bacher LB (2003) Árvores Exóticas no Brasil: madeiras, ornamentais e aromáticas. Platarum, Nova Odessa

  30. 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

  31. Marques OAV, Eterovic A, Strüssmann C, Sazima I (2005) Serpentes do Pantanal (Guia Ilustrado). Holos Editora, São Paulo

  32. Martins M (1993) Why do snakes sleep on the vegetation in central Amazonia? Herp Rev 24:83–84

  33. Ostrow BD (2006) Bald eagle kills crow chasing a hawk. Wilson J Ornithol 118:569–570

  34. 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

  35. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.Rproject.org/

  36. 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

  37. Robinson WD, Rompré G, Robinson TR (2005) Videography of Panama bird nests shows snakes are principal predators. Ornitol Neotrop 16:187–195

  38. 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

  39. Romero GQ, Koricheva J (2011) Contrasting cascade effects of carnivores on plant fitness: a meta-analysis. J Anim Ecol 80:696–704

  40. Romero GQ, Antiqueira PAP, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behaviour. PLoS One 6:e20689

  41. Sih A, McCarthy TM (2002) Prey responses to pulses of risk and safety: testing the risk allocation hypothesis. Anim Behav 63:437–443

  42. Skutch AF (1985) Clutch size, nesting success, and predation on nests of neotropical birds, reviewed. Ornithol Monogr 36:575–594

  43. Sordahl TA (1990) The risks of avian mobbing and distraction behavior: an anecdotal review. Wilson Bull 102:349–352

  44. Stevens GC (1987) Lianas as structural parasites: the Bursera simaruba example. Ecology 68:77–81

  45. Templeton CN, Greene E, Davis K (2005) Allometry of alarm calls: black-capped chickadees encode information about predator size. Science 308:1934–1937

  46. 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

  47. Weatherhead PJ, Blouin-Demers G (2004) Understanding avian nest predation: why ornithologists should study snakes. J Avian Biol 35:185–190

Download references

Acknowledgments

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.

Author information

Correspondence to Crasso Paulo B. Breviglieri.

Ethics declarations

Ethical approval

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).

Additional information

Communicated by N. Clayton

Electronic supplementary material

Below is the link to the electronic supplementary material.

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)

ESM 1

Bird species that foraged upon Morus nigra during the experiment. (DOCX 555 kb)

ESM 2

Mobbing behavior in the presence of the snake models. (DOCX 344 kb)

ESM 3

Tangara seledon behavior (i.e., mobbing) in response to the snake model. (MPEG 29516 kb)

ESM 4

Tangara seledon behavior (i.e., mobbing) in response to the snake-shaped mimicry treatment using vines simulating “coiled” behavior. (MPEG 45488 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Bird anti-predatory behavior
  • Cognitive and behavioral abilities
  • Predator cues
  • Foraging behavior
  • Vertebrates