Skip to main content
Log in

Differences in predatory behavior among three bird species when attacking chemically defended and undefended prey

  • Article
  • Published:
Journal of Ethology Aims and scope Submit manuscript

Abstract

Birds are important predators of insects and insects often incorporate chemical defenses that may make themselves distasteful or toxic to the predators. Predators can respond to chemically defended prey in multiple ways, the predator psychology approach to predation often treats predation as a general process despite the possibility for multiple responses among species. The effectiveness of a prey’s chemical defense at reducing predation might also vary depending on what predator is attacking the prey. Here, we compared the attack strategies of three different species of avian predators (Japanese bush warblers [Horornis diphone], narcissus flycatchers [Ficedula narcissina], and Japanese tits [Parus minor]) which are found in the temperate forests of Japan. We found overall, that undefended prey was preferred over the defended prey, but the different predator species had different preferences and handled prey differently from one another. This suggests that different predator species might exert different selection pressures on chemically defended prey and this adds to our growing appreciation that predator behavior can vary among predator species. Moreover, our findings emphasize the importance of understanding differences in behavior among free-living predator species in studies of aposematism and mimicry.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adamová-Ježová D, Hospodková E, Fuchsová L, Štys P, Exnerová A (2016) Through experience to boldness? Deactivation of neophobia towards novel and aposematic prey in three European species of tits (Paridae). Behav Proc 131:24–31

    Google Scholar 

  • Barnett CA, Bateson M, Rowe C (2007) State-dependent decision making: educated predators strategically trade-off the costs and benefits of consuming aposematic prey. Behav Ecol 18:645–651

    Google Scholar 

  • Barnett CA, Skelhorn J, Bateson M, Rowe C (2012) Educated predators make strategic decisions to eat defended prey according to their toxin content. Behav Ecol 23:418–424

    Google Scholar 

  • Barnett CA, Bateson M, Rowe C (2014) Better the devil you know: avian predators find variayion in prey toxicity aversive. Biol Lett 10:20140533

    PubMed  PubMed Central  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H (2018) lme4: linear mixed-effects models using ‘Eigen’ and S4. R package version 1.1-19. https://CRAN.R-project.org/web/packages/lme4/index.html. Accessed 28 Dec 2018

  • Benjamini Y, Hochberg T (1995) Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J R Stat Soc B 5:289–300

    Google Scholar 

  • Berenbaum MR, Feeny PP (2008) Chemical mediation of host-plant specialization: the Papilionid paradigm. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 3–19

    Google Scholar 

  • Boyden TC (1976) Butterfly palatability and mimicry: experiments with Ameiva lizards. Evolution 30:73–81

    PubMed  Google Scholar 

  • Buskirk WH, Powell GVN, Wittenberger JF, Buskirk RE, Powell TU (1972) Interspecific bird flocks in tropical highland Panama. Auk 89:612–624

    Google Scholar 

  • Carroll J, Sherratt TN (2013) A direct comparison of the effectiveness of two anti-predator strategies under field conditions. J Zool 291:279–285

    Google Scholar 

  • Chai P (1986) Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest. Biol J Linn Soc 29:161–189

    Google Scholar 

  • Chatelain M, Halpin CG, Rowe C (2013) Ambient temperature influences birds’ decisions to eat toxic prey. Anim Behav 86:733–740

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cuthill IC, Stevens M, Sheppard J, Maddocks T, Párraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434:72–74

    CAS  PubMed  Google Scholar 

  • Dell’aglio DD, Stevens M, Jiggins CD (2016) Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest. Ecol Entomol 41:627–631

    PubMed  PubMed Central  Google Scholar 

  • Exnerová A, Landová E, Štys P, Fuchs R, Prokopová M, Cehláriková P (2003) Reactions of passerine birds to aposematic firebugs (Pyrrhocoris apterus; Hemiptera). Biol J Linn Soc 78:517–525

    Google Scholar 

  • Exnerová A, Štys P, Fučíková E, Vesalá S, Svádová K, Prokopová M, Jarošík V, Fuchs R, Landová E (2007) Avoidance of aposematic prey in European tits (Paridae): learned or innate? Behav Ecol 18:148–156

    Google Scholar 

  • Gamberale-Stille G, Guilford T (2004) Automimicry destabilises aposematism: predator sample-and-reject behaviour may prove a solution. Proc R Soc B 271:2612–2625

    Google Scholar 

  • Halpin CG, Rowe C (2017) The effect of distastefulness and conspicuous coloration on the post-attack rejection behaviour of predators and survival of prey. Biol J Linn Soc 120:236–244

    Google Scholar 

  • Halpin CG, Skelhorn J, Rowe C (2008) Being conspicuous and defended: selective benefits for the individual. Behav Ecol 19:1012–1017

    Google Scholar 

  • Hämäläinen L, Mappes J, Thorogood R, Valkonen JK, Karttunen K, Salmi T, Rowland HM (2019) Predators’ consumption of unpalatable prey does not vary as a function of bitter taste perception. Behav Ecol. https://doi.org/10.1093/beheco/arz199

    Article  Google Scholar 

  • Holen ØH (2013) Disentangling taste and toxicity in aposematic prey. Proc R Soc B 280:20122588

    PubMed  Google Scholar 

  • Järvi T, Sillén-Tullberg B, Wiklund C (1981) The cost of being aposematic: an experimental study of predation on larvae of Papillion machon by the great tit, Parus major. Oikos 36:267–272

    Google Scholar 

  • Kang C, Cho H-J, Lee S-I, Jablonski PG (2016) Post-attack aposematic display in prey facilitates predator avoidance learning. Front Ecol Evol 4:35

    Google Scholar 

  • Karr JR (1977) Ecological correlates of rarity in a tropical forest bird community. Auk 94:240–247

    Google Scholar 

  • Lövei GL, Ferrante M (2017) A review of the sentinel prey method as a way of quantifying invertebrate predation under field conditions. Insect Sci 24:528–542

    PubMed  Google Scholar 

  • Marples NM, Brakefield PM, Cowie RJ (1989) Differences between the 7-spot and 2-spot ladybird beetles (Coccinellidae) in their toxic effects on a bird predator. Ecol Entomol 14:79–84

    Google Scholar 

  • Marples NM, Speed MJ, Thomas RJ (2018) An individual-based profitability spectrum for understanding interactions between predators and their prey. Biol J Linn Soc 125:1–13

    Google Scholar 

  • Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Ann Rev Entomol 47:57–92

    CAS  Google Scholar 

  • Nokelainen O, Valkonen J, Lindstedt C, Mappes J (2014) Changes in predator community structure shifts the efficacy of two warning signals in Arctiid moths. J Anim Ecol 83:598–605

    PubMed  Google Scholar 

  • Pagani-Nuñéz E, Barnett CA, Gu H, Goodale E (2016) The need for new categorizations of dietary specialism incorporating spatio-temporal variability of individual diet specialization. J Zool 300:1–7

    Google Scholar 

  • Päckert M, Martens J, Eck S, Nazarenko AA, Valchuk OP, Petri B, Veith M (2005) The great tit (Parus major)—a misclassified ring species. Biol J Linn Soc 86:153–174

    Google Scholar 

  • Pinheiro CEG, Campos VC (2019) The responses of wild jacamars (Galbula ruficauda, Galbulidae) to aposematic, aposematic and cryptic, and cryptic butterflies in central Brazil. Ecol Entomol 44:441–450

    Google Scholar 

  • Pinheiro CEG, de Campos VC (2013) Do rufous tailed jacamars (Galbula ruficauda) play with aposematic butterflies. Ornitolog Neotrop 24:365–367

    Google Scholar 

  • R Development Core Team [online] (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.Rproject.org. Accessed 23 Apr 2018

  • Rönkä K, Mappes J, Michalis C, Kiviö R, Salokannas J, Rojas B (2018) Can multiple model mimicry explain warning signal polymorphism in the wood tiger moth, Arctia plantaginis (Lepidoptera: Erebidae)? Biol J Linn Soc 124:237–260

    Google Scholar 

  • Roper TJ, Wistow R (1986) Aposematic colouration and avoidance learning in chicks. Quart J Exp Psychol B Comp Physiol Psychol 38:141–149

    Google Scholar 

  • Roslin T, Hardwick B, Novotny V, Petry WK, Andrew NR, Asmus A, Barrio IC, Basset Y, Boesing AL, Bonebrake TC, Cameron EK, Dáttilo W, Donoso DA, Drozd P, Gray DS, Hill SJ, Hopkins T, Huang S, Koane B, Laird-Hopkins B, Laukkanen L, Lewis OT, Milne S, Mwesige I, Nakamura A, Nell CS, Nichols E, Prokurat A, Sam K, Schmidt NM, Slade A, Slade V, Suchanková A, Tedar T, van Nouhuys S, Vandvik V, Weissflog A, Zhikovich V, Slade EM (2017) Higher predation risk for insect prey at low lattitudes and elevations. Science 356:742–744

    CAS  PubMed  Google Scholar 

  • Ruxton GD, Allen W, Sherratt TN, Speed MP (2018) Avoiding attack: the evolution of crypsis, warning signals, and mimicry. Oxford University Press, Oxford

    Google Scholar 

  • Seymoure BM, Raymondo A, McGraw KJ, McMillan WO, Rutowski RL (2018) Environment-dependent attack rates of cryptic and aposematic butterflies. Curr Zool 64:663–669

    PubMed  Google Scholar 

  • Skelhorn J, Rowe C (2006a) Avian predators taste-reject aposematic prey on the basis of their chemical defence. Biol Lett 2:348–350

    PubMed  PubMed Central  Google Scholar 

  • Skelhorn J, Rowe C (2006b) Predator avoidance learning of prey with secreted or stored defences and the evolution of insect defence. Anim Behav 72:827–834

    Google Scholar 

  • Skelhorn J, Rowe C (2007) Predators’ toxin burdens influence their strategic decisions to eat toxic prey. Curr Biol 17:1479–1483

    CAS  PubMed  Google Scholar 

  • Skelhorn J, Rowe C (2009) Distastefulness as an antipredator defence strategy. Anim Behav 78:761–766

    Google Scholar 

  • Skelhorn J, Halpin CG, Rowe C (2016) Learning about aposematism. Behav Ecol 27:955–964

    Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • Therneau TM (2018) A package for survival analysis in S. version 2.43-3. https://CRAN.R-project.org/package=survival. Accessed 9 Jan 2019

  • Tsujimoto D, Lin C-H, Kurihara N, Barnett CRA (2019) Citizen science in the class-room: the consistency of student collected data and its value in ecological hypothesis testing. Ornithol Sci 18:39–47

    Google Scholar 

  • Valkonnen JK, Nokelainen O, Niskanen M, Kilpimaa J, Björkland M, Mappes J (2011) Variation in predator species abundance can cause variable selection pressure on warning signalling prey. Ecol Evol 2:1971–1976

    Google Scholar 

  • Vesely P, Ernestová B, Nedvéd O, Fuchs R (2017) Do predator energy demands or previous exposure influence protection by aposematic coloration of prey? Curr Zool 63:259–267

    PubMed  Google Scholar 

  • Wiklund C, Järvi T (1982) Survival of distasteful insects after being attacked by naive birds: a reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution 36:998–1002

    PubMed  Google Scholar 

  • Yamazaki Y, Pagani-Núñez E, Sota T, Barnett CRA (2020) The truth is in the detail: predators attack aposematic prey with less aggression than other prey types. Biol J Linn Soc (in press)

Download references

Acknowledgements

CRAB thanks Tomoki Kurihara for valuable statistical advice and discussions. We thank two anonymous reviewers who made many valuable comments. We also thank Kyoto University and Kyoto City Council for permission to use the field sites. All research adhered to the ABS/ASAB regulations for the use of animals in research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Craig R. A. Barnett.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 74 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barnett, C.R.A., Ringhofer, M. & Suzuki, T.N. Differences in predatory behavior among three bird species when attacking chemically defended and undefended prey. J Ethol 39, 29–37 (2021). https://doi.org/10.1007/s10164-020-00668-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10164-020-00668-w

Keywords

Navigation