Evolutionary Ecology

, Volume 33, Issue 5, pp 625–636 | Cite as

Don’t waste your time: predators avoid prey with conspicuous colors that signal long handling time

  • Vivek Philip CyriacEmail author
  • Ullasa Kodandaramaiah
Original Paper


Most studies on warning signal theory have focused on aposematic prey, which signal unpalatability through conspicuous signals. Palatable prey that are difficult to capture or process may also use conspicuous signals to advertise unprofitability to predators. Theory predicts that predators should avoid prey with long handling time, especially when other prey with shorter handling times are abundant. However, it is unclear if prey can benefit by signaling longer handling time. In experiments with dough models as prey, we show that chickens can learn to associate colors with increased handling time and avoid such prey when alternative prey are abundant. Overall, our experiment demonstrates that advertising longer handling time to predators can be advantageous to prey when other more profitable prey are abundant.


Handling time Antipredatory strategies Conspicuous colorations 



We thank Jayasooryan CS, Nawaf AM, Rohit Anand and Harshad Mayekar for help with the experiment. We thank Shaji for permitting us to carry out the experiment in his property. We thank Almut Kelber, Balamurali GS and Hema Somanathan for discussions. John Endler provided insightful comments on the manuscript. This study was funded by an INSPIRE Faculty Award from the Department of Science and Technology (DST/INSPIRE/04/2013/000476) to UK.

Author’s contribution

VPC conceived the study, designed and carried out the experiment, and analyzed the data; UK provided materials; VPC and UK wrote the paper and gave final approval.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The experimental protocol was approved by the Institutional Animal Ethics Committee of Indian Institute of Science Education and Research Thiruvananthapuram.

Supplementary material

10682_2019_9998_MOESM1_ESM.docx (116 kb)
Supplementary file1 (DOCX 115 kb)


  1. Altwegg R, Eng M, Caspersen S, Anholt BR (2006) Functional response and prey defence level in an experimental predator–prey system. Evol Ecol Res 8:115–128Google Scholar
  2. Amo L, Galván I, Tomás G, Sanz JJ (2008) Predator odour recognition and avoidance in a songbird. Funct Ecol 22:289–293CrossRefGoogle Scholar
  3. 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 18:645–651CrossRefGoogle Scholar
  4. Barnett CA, Skelhorn J, Bateson M, Rowe C (2011) Educated predators make strategic decisions to eat defended prey according to their toxin content. Behav Ecol 23:418–424CrossRefGoogle Scholar
  5. Barnett CA, Bateson M, Rowe C (2014) Better the devil you know: avian predators find variation in prey toxicity aversive. Biol Lett 10:20140533CrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  7. Bence JR, Murdoch WW (1986) Prey size selection by the mosquitofish: relation to optimal diet theory. Ecology 67:324–336CrossRefGoogle Scholar
  8. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  9. Caro TM (1995) Pursuit-deterrence revisited. Trends Ecol Evol 10:500–503CrossRefGoogle Scholar
  10. Caro T, Ruxton G (2019) Aposematism: unpacking the defences. Trends Ecol Evol 34:595–604CrossRefGoogle Scholar
  11. Caro SP, Balthazart J, Bonadonna F (2015) The perfume of reproduction in birds: chemosignaling in avian social life. Horm Behav 68:25–42CrossRefGoogle Scholar
  12. Charnov EL (1976) Optimal foraging: attack strategy of a mantid. Am Nat 110:141–151CrossRefGoogle Scholar
  13. Cody ML (1971) Finch flocks in the Mojave Desert. Theor Popul Biol 2:141–158CrossRefGoogle Scholar
  14. Cooper WE Jr, Anderson RA (2006) Adjusting prey handling times and methods affects profitability in the broad-headed skink (Eumeces laticeps). Herpetologica 62:356–365CrossRefGoogle Scholar
  15. Cooper SM, Ginnett TF (1998) Spines protect plants against browsing by small climbing mammals. Oecologia 113:219–221CrossRefGoogle Scholar
  16. Cooper SM, Owen-Smith N (1986) Effects of plant spinescence on large mammalian herbivores. Oecologia 68:446–455CrossRefGoogle Scholar
  17. Cott HB (1940) Adaptive coloration in animals. Methuen, LondonGoogle Scholar
  18. Creswell PD, Mclay CL (1990) Handling times, prey size and species selection by Cancer novaezelandiae (Jacquinot, 1853) feeding on molluscan prey. J Exp Mar Biol Ecol 140:13–28CrossRefGoogle Scholar
  19. Croy MI, Hughes RN (1991) The role of learning and memory in the feeding behaviour of the fifteen-spined stickleback, Spinachia spinachia L. Anim Behav 41:149–159CrossRefGoogle Scholar
  20. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252Google Scholar
  21. Endler JA, Rojas B (2009) The spatial pattern of natural selection when selection depends on experience. Am Nat 173:E62–E78CrossRefGoogle Scholar
  22. Ganchrow JR, Steiner JE, Bartana A (1990) Behavioral reactions to gustatory stimuli in young chicks (Gallus gallus domesticus). Dev Psychobiol J Int Soc Dev Psychobiol 23:103–117CrossRefGoogle Scholar
  23. Gentle MJ (1971) Taste and its importance to the domestic chicken. Br Poult Sci 12:77–86CrossRefGoogle Scholar
  24. Halpin CG, Skelhorn J, Rowe C (2013) Predators’ decisions to eat defended prey depend on the size of undefended prey. Anim Behav 85:1315–1321CrossRefGoogle Scholar
  25. Halpin CG, Skelhorn J, Rowe C (2014) Increased predation of nutrient-enriched aposematic prey. Proc R Soc B Biol Sci 281:20133255CrossRefGoogle Scholar
  26. Hammill E, Petchey OL, Anholt BR (2010) Predator functional response changed by induced defenses in prey. Am Nat 176:723–731CrossRefGoogle Scholar
  27. Hancox AP, Allen JA (1991) A simulation of evasive mimicry in the wild. J Zool 223:9–13CrossRefGoogle Scholar
  28. Hasson O (1991) Pursuit-deterrent signals: communication between prey and predator. Trends Ecol Evol 6:325–329CrossRefGoogle Scholar
  29. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefGoogle Scholar
  30. Kamil AC (1983) Optimal foraging theory and the psychology of learning. Am Zool 23:291–302CrossRefGoogle Scholar
  31. Krebs JR (1980) Optimal foraging, predation risk and territory defence. Ardea 68:83–90Google Scholar
  32. Krebs J, Ryan J, Charnov E (1974) Hunting by expectation or optimal foraging: a study of patch use by chickadees. Anim Behav 22:953–964CrossRefGoogle Scholar
  33. Krebs JR, Erichsen JT, Webber MI, Charnov EL (1977) Optimal prey selection in the great tit (Parus major). Anim Behav 25:30–38CrossRefGoogle Scholar
  34. Leclaire S, Bourret V, Bonadonna F (2017a) Blue petrels recognize the odor of their egg. J Exp Biol 220:3022–3025CrossRefGoogle Scholar
  35. Leclaire S, Strandh M, Mardon J et al (2017b) Odour-based discrimination of similarity at the major histocompatibility complex in birds. Proc R Soc B Biol Sci 284:20162466CrossRefGoogle Scholar
  36. Lemon WC (1991) Fitness consequences of foraging behaviour in the zebra finch. Nature 352:153CrossRefGoogle Scholar
  37. Lev-Yadun S (2001) Aposematic (warning) coloration associated with thorns in higher plants. J Theor Biol 210:385–388CrossRefGoogle Scholar
  38. Lev-Yadun S (2009) Aposematic (warning) coloration in plants. In: Baluška F (ed) Plant–Environment interactions: from sensory plant biology to active plant behavior. Springer, Berlin, pp 167–202CrossRefGoogle Scholar
  39. Lev-Yadun S (2016) Defensive (anti-herbivory) coloration in land plants. Springer International Publishing, ChamCrossRefGoogle Scholar
  40. Liu H-X, Rajapaksha P, Wang Z et al (2018) An update on the sense of taste in chickens: a better developed system than previously appreciated. J Nutr Food Sci 8:686Google Scholar
  41. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609CrossRefGoogle Scholar
  42. Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603CrossRefGoogle Scholar
  43. Niknafs S, Roura E (2018) Nutrient sensing, taste and feed intake in avian species. Nutr Res Rev 31:256–266CrossRefGoogle Scholar
  44. Okuyama T (2015) Optimal foraging behavior with an explicit consideration of within-individual behavioral variation: an example of predation. Evol Ecol 29:599–607CrossRefGoogle Scholar
  45. O’Neill HM (2008) Influence of storage and temperature treatment on nutritional value of wheat for poultry. PhD thesis, University of NottinghamGoogle Scholar
  46. Pinheiro CE (1996) Palatablility and escaping ability in Neotropical butterflies: tests with wild kingbirds (Tyrannus melancholicus, Tyrannidae). Biol J Linn Soc 59:351–365CrossRefGoogle Scholar
  47. Pinheiro CEG, Freitas AVL, Campos VC et al (2016) Both palatable and unpalatable butterflies use bright colors to signal difficulty of capture to predators. Neotrop Entomol 45:107–113CrossRefGoogle Scholar
  48. Poulton EB (1890) The colours of animals: their meaning and use, especially considered in the case of insects. K. Paul, Trench, Trübner & Company, LondonCrossRefGoogle Scholar
  49. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  50. Rajendran MV (1985) Studies in uropeltid snakes. Madurai Kamaraj University, MaduraiGoogle Scholar
  51. Rojas B, Burdfield-Steel E, Pakkanen H et al (2017) How to fight multiple enemies: target-specific chemical defences in an aposematic moth. Proc R Soc B Biol Sci 284:20171424CrossRefGoogle Scholar
  52. Rojas B, Mappes J, Burdfield-Steel E (2019) Multiple modalities in insect warning displays have additive effects against wild avian predators. Behav Ecol Sociobiol 73:37CrossRefGoogle Scholar
  53. Rowe C, Skelhorn J, Halpin CG (2017) Avian cognition and the evolution of warning signals. In: Cate CT, Healy SD (eds) Avian cognition. Cambridge University Press, CambridgeGoogle Scholar
  54. Rowland HM, Parker MR, Jiang P et al (2015) Comparative taste biology with special focus on birds and reptiles. In: Doty RL (ed) Handbook of olfaction and gustation. Wiley, New York, pp 957–982CrossRefGoogle Scholar
  55. Ruxton GD, Sherratt TN, Speed MP (2004a) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, OxfordCrossRefGoogle Scholar
  56. Ruxton GD, Speed M, Sherratt TN (2004b) Evasive mimicry: when (if ever) could mimicry based on difficulty of capture evolve? Proc R Soc Lond B Biol Sci 271:2135–2142CrossRefGoogle Scholar
  57. Schoener TW (1969) Models of optimal size for solitary predators. Am Nat 103:277–313CrossRefGoogle Scholar
  58. Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404CrossRefGoogle Scholar
  59. Skelhorn J, Rowe C (2007) Predators’ toxin burdens influence their strategic decisions to eat toxic prey. Curr Biol 17:1479–1483CrossRefGoogle Scholar
  60. Skelhorn J, Rowe C (2009) Distastefulness as an antipredator defence strategy. Anim Behav 78:761–766CrossRefGoogle Scholar
  61. Skelhorn J, Rowe C (2010) Birds learn to use distastefulness as a signal of toxicity. Proc R Soc Lond B Biol Sci 277:1729–1734CrossRefGoogle Scholar
  62. Skelhorn J, Halpin CG, Rowe C (2016) Learning about aposematic prey. Behav Ecol 27:955–964CrossRefGoogle Scholar
  63. Speed MP (2000) Warning signals, receiver psychology and predator memory. Anim Behav 60:269–278CrossRefGoogle Scholar
  64. Speed MP (2001) Can receiver psychology explain the evolution of aposematism? Anim Behav 61:205–216CrossRefGoogle Scholar
  65. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  66. Stevens M, Ruxton GD (2012) Linking the evolution and form of warning coloration in nature. Proc R Soc B 279:417–426CrossRefGoogle Scholar
  67. Stevison B, Kensinger B, Luttbeg B (2016) Different morphological traits influence predator defense and space use in Physa acuta. Am Malacol Bull 34:79–84CrossRefGoogle Scholar
  68. Sullivan KA (1988) Ontogeny of time budgets in yellow-eyed juncos: adaptation to ecological constaints. Ecology 69:118–124CrossRefGoogle Scholar
  69. Therneau TM (2018) coxme: mixed effects Cox models. R package version 2.2-10. Accessed June 2019
  70. Veselý P, Ernestová B, Nedvěd O, Fuchs R (2017) Do predator energy demands or previous exposure influence protection by aposematic coloration of prey? Curr Zool 63:259–267Google Scholar
  71. Wang L-Y, Huang W-S, Tang H-C et al (2018) Too hard to swallow: a secret secondary defence of an aposematic insect. J Exp Biol 221:jeb172486CrossRefGoogle Scholar
  72. Webb JK, Brown GP, Child T et al (2008) A native dasyurid predator (Common Planigale, Planigale maculata) rapidly learns to avoid a toxic invader. Austral Ecol 33:821–829CrossRefGoogle Scholar
  73. Weimerskirch H, Ancel A, Caloin M et al (2003) Foraging efficiency and adjustment of energy expenditure in a pelagic seabird provisioning its chick. J Anim Ecol 72:500–508CrossRefGoogle Scholar
  74. Werner EE, Hall DJ (1974) Optimal foraging and the size selection of prey by the bluegill sunfish (Lepomis macrochirus). Ecology 55:1042–1052CrossRefGoogle Scholar
  75. Whitman DW, Vincent S (2008) Large size as an antipredator defense in an insect. J Orthoptera Res 17:353–371CrossRefGoogle Scholar
  76. Wilson SL, Kerley GIH (2003) The effect of plant spinescence on the foraging efficiency of bushbuck and boergoats: browsers of similar body size. J Arid Environ 55:150–158CrossRefGoogle Scholar
  77. Winters AE, Wilson NG, van den Berg CP et al (2018) Toxicity and taste: unequal chemical defences in a mimicry ring. Proc R Soc B Biol Sci 285:20180457Google Scholar
  78. Zahavi A, Zahavi A (1997) The handicap principle: a missing piece of Darwin’s puzzle. Oxford University Press, New YorkGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.IISER-TVM Centre for Research and Education in Ecology and Evolution (ICREEE), School of BiologyIndian Institute of Science Education and Research ThiruvananthapuramThiruvananthapuramIndia

Personalised recommendations