Role of chemical and visual cues of mammalian predators in nest defense in birds

  • Luisa Amo
  • Gustavo Tomás
  • Alejandro López-García
Original Article


We explore for the first time the relative importance of chemical and visual cues of predators in nest defense and antipredator behavior in a hole-nesting songbird, the blue tit Cyanistes caeruleus. Birds breeding in nest boxes were exposed to chemical or visual cues of a predatory and a non-predatory mammal during the nestling stage, and their behavior both outside and inside nest boxes was recorded with video films. Our results show that birds respond equally to chemical and to visual cues of predators in a context of nest defense. Adult birds minimized predation risk by decreasing the time spent inside the nest box while feeding nestlings when they were exposed to either visual or chemical cues of a mammalian predator. They decreased the time spent in non-essential activities for nestlings’ survival, such as nest sanitation activities, but they maintained provisioning rates so that the nestlings’ growth was not compromised. In this way, birds minimized the risk of predation while provisioning nestlings when a predator was detected in the vicinity of their nest.

Significant statement

We explored the role of predator chemical and visual cues for risk assessment in blue tits. Our results showed for the first time that birds respond equally to chemical and to visual cues of mammalian predators. Birds decreased time exposed to predation risk when entering the nest box to feed the nestlings. They reduced time spent in non-essential activities for nestling survival, such as nest sanitation. However, they maintained provisioning rates so that nestling growth was not impaired.


Avian olfaction Predation risk assessment Chemical cues Visual cues Provisioning behavior Nest defense Predator cues 



We especially thank Paz Manzano for English corrections. We thank anonymous referees that help us to improve the manuscript with their comments.

Compliance with ethical standards


LA was supported by the Ramón y Cajal program and the CGL2014-58890-P project. GT was partly supported by the Ramón y Cajal program.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

No nest was deserted during the course of the experiment. Results of a previous study showed that exposure to predator chemical cues did not affect body condition of blue tit nestlings, even when cues were located inside nest boxes (Amo et al. 2008). The experiment was conducted under license issued by the Instituto Aragonés de Gestión Ambiental (INAGA/500201/24/2013/11743).


  1. Amo L, López P, Martín J (2004) Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Anim Behav 67:647–653CrossRefGoogle Scholar
  2. Amo L, López P, Martín J (2005) Chemical assessment of predation risk in the wall lizard, Podarcis muralis, is influenced by time exposed to chemical cues of ambush snakes. Herpetol J 15:21–25Google Scholar
  3. Amo L, Galván I, Tomás G, Sanz JJ (2008) Predator odour recognition and avoidance in a songbird. Funct Ecol 22:289–293CrossRefGoogle Scholar
  4. Amo L, Visser ME, van Oers K (2011a) Smelling out predators is innate in birds. Ardea 99:188–184CrossRefGoogle Scholar
  5. Amo L, Caro SP, Visser ME (2011b) Sleeping birds do not respond to predator odour. PLoS One 6:e27576CrossRefPubMedPubMedCentralGoogle Scholar
  6. Amo L, López-Rull I, Pagán I, Macías-Garcia C (2015) Evidence that the house finch (Carpodacus mexicanus) uses scent to avoid omnivore mammals. Rev Chil Hist Nat 88:5CrossRefGoogle Scholar
  7. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosc Biobehav Rev 29:1123–1144CrossRefGoogle Scholar
  8. Brown GE, Magnavacca G (2003) Predator inspection behaviour in a characin fish: an interaction between chemical and visual information? Ethology 109:739–750CrossRefGoogle Scholar
  9. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator/prey systems: a review and prospectus. Ecoscience 5:338–352CrossRefGoogle Scholar
  10. Chivers DP, Mirza RS, Bryer PS, Kiesecker JM (2001) Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. Can J Zool 79:867–873CrossRefGoogle Scholar
  11. Cramp S, Perrins CM (1993) Handbook of the birds of Europe, the Middle East and North Africa. The birds of the Western Palearctic. Vol. VII. Flycatchers to shrikes. Oxford Univ Press, OxfordGoogle Scholar
  12. Eichholz MW, Dassow JA, Stafford JD, Weatherhead PJ (2012) Experimental evidence that nesting ducks use mammalian urine to assess predator abundance. Auk 129:638–644CrossRefGoogle Scholar
  13. Garamszegi LZ, Eens M, Török J (2009) Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim Behav 77:803–812CrossRefGoogle Scholar
  14. García-Navas V, Sanz JJ (2010) Flexibility in the foraging behavior of blue tits in response to short-term manipulations of brood size. Ethology 116:744–754Google Scholar
  15. Godard RD, Bowers BB, Wilson CM (2007) Eastern bluebirds Sialia sialis do not avoid nest boxes with chemical cues from two common nest predators. J Avian Biol 38:128–131CrossRefGoogle Scholar
  16. Gonzálvez FG, Rodríguez-Gironés MA (2013) Seeing is believing: information content and behavioural response to visual and chemical cues. Proc R Soc B 280:20130886CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hartman EJ, Abrahams MV (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proc R Soc Lond B 267:571–575CrossRefGoogle Scholar
  18. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58CrossRefGoogle Scholar
  19. Hemmi JM (2005) Predator avoidance in fiddler crabs: 2. The visual cues. Anim Behav 69:615–625CrossRefGoogle Scholar
  20. Hettena A, Blumstein DT, Munoz N (2014) Prey responses to predator’s sounds: a review and empirical study. Ethology 120:427–452CrossRefGoogle Scholar
  21. Hettyey A, Rölli F, Thürlimann N, Zürcher A, Van Buskirk J (2012) Visual cues contribute to predator detection in anuran larvae. Biol J Linn Soc 106:820–827CrossRefGoogle Scholar
  22. Hund AK, Aberle MA, Safran RJ (2015) Do parents alter provisioning rates across the nestling period in response to ectoparasites: an experimental test in the North American barn swallow Hirundo rustica erythrogaster. Anim Behav 110:187–196CrossRefGoogle Scholar
  23. Hurtrez-Boussès S, Renaud F, Blondel J, Perret P, Galán MJ (2000) Effects of ectoparasites of young on parents’ behaviour in a Mediterranean population of blue tits. J Avian Biol 31:266–269CrossRefGoogle Scholar
  24. Ibáñez-Álamo JD, Sanllorente O, Arco L, Soler M (2013) Is nest predation an important selective pressure determining fecal sac removal? Ann Zool Fenn 50:71–78CrossRefGoogle Scholar
  25. Johnson LS, Murphy SM, Parrish GW (2011) Lack of predator-odor detection and avoidance by a songbird, the house wren. J Field Ornithol 82:150–157CrossRefGoogle Scholar
  26. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394CrossRefGoogle Scholar
  27. Kiesecker JM, Chivers DP, Anderson M, Blaustein AR (2002) Effect of predator diet on life history shifts of red-legged frogs, Rana aurora. J Chem Ecol 28:1007–1015CrossRefPubMedGoogle Scholar
  28. Knight RL, Temple SA (1986) Why does intensity of avian nest defense increase during the nesting cycle? Auk 103:318–327Google Scholar
  29. Krams I, Krama T, Igaune K, Mänd R (2007) Long-lasting mobbing of the pied flycatcher increases the risk of nest predation. Behav Ecol 18:1082–1084CrossRefGoogle Scholar
  30. Krystofkova M, Haas M, Exnerova A (2011) Nest defense in blackbirds Turdus merula: effect of predator distance and parental sex. Acta Ornithol 46:55–63CrossRefGoogle Scholar
  31. Lohrey AK, Clark DL, Gordon SD, Uetz GW (2009) Antipredator responses of wolf spiders (Araneae: Lycosidae) to sensory cues representing an avian predator. Anim Behav 77:813–821CrossRefGoogle Scholar
  32. López-Rull I, Macías Garcia C (2015) Control of invertebrate occupants of nests. In: Deeming DC, Reynolds SJ (eds) Nests, eggs, and incubation. Oxford University Press, Oxford, pp 82–96CrossRefGoogle Scholar
  33. MacLean SA, Bonter DN (2013) The sound of danger: threat sensitivity to predator vocalizations, alarm calls, and novelty in gulls. PLoS One 8:e82384CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mathis A, Vincent F (2000) Differential use of visual and chemical cues in predator recognition and threat-sensitive predator-avoidance responses by larval newts (Notophthalmus viridescens). Can J Zool 78:1646–1652CrossRefGoogle Scholar
  35. Merino S (2010) Immunocompetence and parasitism in nestlings from wild populations. Open Ornithol J 3:27–32CrossRefGoogle Scholar
  36. Møller AP, Arriero E, Lobato E, Merino S (2009) A review of parasite virulence in nestling birds. Biol Rev 84:561–588CrossRefGoogle Scholar
  37. Mönkkönen M, Forsman JT, Kananoja T, Ylönen H (2009) Indirect cues of nest predation risk and avian reproductive decisions. Biol Let 5:176–178CrossRefGoogle Scholar
  38. Mutzel A, Blom MPK, Spagopoulou F, Wright J, Dingemanse NJ, Kempenaers B (2013) Temporal trade-offs between nestling provisioning and defence against nest predators in blue tits. Anim Behav 85:1459–1469CrossRefGoogle Scholar
  39. R Development Core Team (2012) R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna,
  40. Roth TC, Cox JG, Lima SL (2008) Can foraging birds assess predation risk by scent? Anim Behav 76:2021–2027CrossRefGoogle Scholar
  41. Seppänen JT, Forsman JT, Mönkkönen M, Krams I, Salmi T (2011) New behavioural trait adopted or rejected by observing heterospecific tutor fitness. Proc R Soc Lond B 278:1736–1741CrossRefGoogle Scholar
  42. Smith ME, Belk MC (2001) Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects? Behav Ecol Sociobiol 51:101–107CrossRefGoogle Scholar
  43. Suzuki TN (2014) Communication about predator type by a bird using discrete, graded and combinatorial variation in alarm calls. Anim Behav 87:59–65CrossRefGoogle Scholar
  44. Suzuki TN, Ueda K (2013) Mobbing calls of Japanese tits signal predator type: field observations of natural predator encounters. Wilson J Ornithol 125:412–415CrossRefGoogle Scholar
  45. Takahara T, Kohmatsu Y, Maruyama A, Doi H, Yamanaka H, Yamaoka R (2012) Inducible defense behavior of an anuran tadpole: cue-detection range and cue types used against predator. Behav Ecol 23:863–868CrossRefGoogle Scholar
  46. Tang L, Schwarzkopf L (2013) Foraging behaviour of the peaceful dove (Geopelia striata) in relation to predation risk: group size and predator cues in a natural environment. Emu 113:1–7CrossRefGoogle Scholar
  47. Thomson RL, Forsman JT, Mönkkönen M (2011) Risk taking in natural predation risk gradients: support for risk allocation from breeding pied flycatchers. Anim Behav 82:1443–1447CrossRefGoogle Scholar
  48. Tvardíková K, Fuchs R (2011) Tits recognize the potential dangers of predators and harmless birds in feeder experiments. J Ethol 30:157–165CrossRefGoogle Scholar
  49. Vilhunen S, Hirvonen H (2003) Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet. Behav Ecol Sociobiol 55:1–10CrossRefGoogle Scholar
  50. Wegmann M, Voegeli B, Richner H (2015) Physiological responses to increased brood size and ectoparasite infestation: adult great tits favour self-maintenance. Physiol Behav 141:127–134CrossRefPubMedGoogle Scholar
  51. Wesolowski T, Maziarz M (2012) Dark tree cavities—a challenge for hole nesting birds? J Avian Biol 43:454–460CrossRefGoogle Scholar
  52. Wiklund C, Andersson M (1980) Nest predation selects for colonial breeding among fieldfares Turdus pilaris. Ibis 122:363–366CrossRefGoogle Scholar
  53. Zhang JX, Sun LX, Novotny M (2007) Mice respond differently to urine and its major volatile constituents from male and female ferrets. J Chem Ecol 33:603–612CrossRefPubMedGoogle Scholar
  54. Zidar J, Løvlie H (2012) Scent of the enemy: behavioural responses to predator faecal odour in the fowl. Anim Behav 84:547–554CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Luisa Amo
    • 1
  • Gustavo Tomás
    • 2
  • Alejandro López-García
    • 1
  1. 1.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales (MNCN-CSIC)MadridSpain
  2. 2.Departamento de Ecología Funcional y EvolutivaEstación Experimental de Zonas Áridas (EEZA-CSIC)AlmeríaSpain

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