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Oecologia

, Volume 191, Issue 1, pp 73–81 | Cite as

Avian and rodent responses to the olfactory landscape in a Mediterranean cavity community

  • Jesús M. AvilésEmail author
  • Deseada Parejo
  • Mónica Expósito-Granados
Behavioral ecology – original research

Abstract

Animals rely on cues informing about future predation risk when selecting habitats to breed in. Olfactory information may play a fundamental role in the assessment of predation threats, because predators produce characteristic body odours, but the role of odours in habitat selection has seldom been considered. Here, we test whether fear of predation induced by odour cues may affect the settlement pattern of a Mediterranean cavity-dependent community of rodents and non-excavator hole-nesting birds. To test this hypothesis, we experimentally manipulated the perception of predation risk on a scale of patch by applying either odours of a carnivore predator (risky odour treatment), lemon essence (non-risky odour treatment) and a control non-odorous treatment and studied bird and rodent settlement patterns. Nest-box occupation probability differed across treatments so that species in the community settled in more numbers in control than in non-risky and than in risky odour-treated nest boxes. Concerning settlement patterns, control nest boxes were occupied more rapidly than nest boxes with odour information. Birds and rodents settled earlier in control than in risky odour-treated nest boxes, but their settlement pattern did not significantly vary between risky odour and non-risky odour-treated nest boxes. Our findings demonstrate that olfactory cues may be used to assess habitat quality by settling species in this community, but we cannot pinpoint the exact mechanism that has given rise to the pattern of preference by nest boxes.

Keywords

Birds Cavity community Fear ecology Habitat selection Olfactory landscape Predation risk 

Notes

Acknowledgements

We thank Juan Rodríguez-Ruiz for help during data collection and Robert L. Thomson, Jere Tolvanen and Liana Zanette for their very useful comments on previous drafts of the manuscript. This study was funded by the Spanish Ministries of Education and Science/FEDER and of Economy and Competitiveness, respectively, through the projects CGL2011-27561/BOS, CGL2014-56769-P to JMA and DP and by the Government of Extremadura through the contract TA13002 to DP. MEG was supported by the Spanish Ministry of Economy and Competitiveness (grant number BES-2012-051898).

Author contribution statement

JMA and DP conceived, designed and coordinated the study. MEG participated in data analysis and in the design of the study and collected field data together with JMA and DP. JMA carried out the statistical analyses and drafted the manuscript. All authors gave final approval for publication.

Supplementary material

442_2019_4487_MOESM1_ESM.docx (55 kb)
Supplementary material 1 (DOCX 55 kb)

References

  1. Amo L, Galvan I, Tomas G, Sanz JJ (2008) Predator odour recognition and avoidance in a songbird. Funct Ecol 22:289–293CrossRefGoogle Scholar
  2. Amo L, Visser ME, van Oers K (2011) Smelling out predators is innate in birds. Ardea 99:177–184CrossRefGoogle Scholar
  3. Amo L, Aviles JM, Parejo D, Pena A, Rodriguez J, Tomas G (2012) Sex recognition by odour and variation in the uropygial gland secretion in starlings. J Anim Ecol 81:605–613CrossRefGoogle Scholar
  4. Amo L, Jansen JJ, van Dam NM, Dicke M, Visser ME (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecol Lett 16:1348–1355CrossRefGoogle Scholar
  5. Amo L, Tomás G, Saavedra I, Visser ME (2018) Wild great and blue tits do not avoid chemical cues of predators when selecting cavities for roosting. PLoS One 13:e0203269CrossRefGoogle Scholar
  6. 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. Neurosci Biobehav Rev 29:1123–1144CrossRefGoogle Scholar
  7. Austin PC (2017) A tutorial on multilevel survival analysis: methods, models and applications. Int Stat Rev 85:185–203CrossRefGoogle Scholar
  8. Aviles JM, Amo L (2018) The evolution of olfactory capabilities in wild birds: a comparative study. Evol Biol 45:27–36CrossRefGoogle Scholar
  9. Aviles JM, Parejo D (2018) Origen y adecuación de cavidades para aves no-excavadoras en los encinares del Conejo. Efectos de la instalación de cajas nido. In: Navarro FBG (ed) Finca experimental Cortijos del Conejo y Albarrán y Cortijo Becerra (Guadix, Granada): Área de referencia en investigación del medio natural en el SE semiárido ibérico. University of Granada, GranadaGoogle Scholar
  10. Bang BG (1971) Functional anatomy of the olfactory system in 23 orders of birds. Acta Anat 79:1–76CrossRefGoogle Scholar
  11. Blackwell BF, Seamans TW, Pfeiffer MB, Buckingham BN (2018) European starling (Sturnus vulgaris) reproduction undeterred by predator scent inside nest boxes. Can J Zool 96:980–986CrossRefGoogle Scholar
  12. Bodey TW, Bearhop S, McDonald RA (2011) The diet of an invasive nonnative predator, the feral ferret Mustela furo, and implications for the conservation of ground-nesting birds. J Eur J Wildl Res 57:107–117CrossRefGoogle Scholar
  13. Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science 306:835CrossRefGoogle Scholar
  14. Brinck C, Erlinge S, Sandell M (1983) Anal sac secretion in mustelids—a comparison. J Chem Ecol 9:727–745CrossRefGoogle Scholar
  15. Brinkerhoff RJ, Haddad NM, Orrock JL (2005) Corridors and olfactory predator cues affect small mammal behavior. J Mammal 86:662–669CrossRefGoogle Scholar
  16. Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, ChicagoGoogle Scholar
  17. Caro SP, Balthazart J (2010) Pheromones in birds: myth or reality? J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:751–766CrossRefGoogle Scholar
  18. Caspers BA, Hagelin JC, Paul M, Bock S, Willeke S, Krause ET (2017) Zebra Finch chicks recognise parental scent, and retain chemosensory knowledge of their genetic mother, even after egg cross-fostering. Sci Rep 7:12859CrossRefGoogle Scholar
  19. Cohen J (2013) Statistical power analysis for the behavioral sciences. Routledge, LondonCrossRefGoogle Scholar
  20. Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214CrossRefGoogle Scholar
  21. da Camara CAG, Akhtar Y, Isman MB, Seffrin RC, Born FS (2015) Repellent activity of essential oils from two species of citrus against Tetranychus urticae in the laboratory and greenhouse. Crop Protection 74:110–115CrossRefGoogle Scholar
  22. Dhondt, A. A. 2012. Interspecific competition in birds. Oxford University PressGoogle Scholar
  23. Dickman CR (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313–322CrossRefGoogle Scholar
  24. Eggers S, Griesser M, Nystrand M, Ekman J (2006) Predation risk induces changes in nest-site selection and clutch size in the Siberian jay. Proc R Soc B Biol Sci 273:701–706CrossRefGoogle Scholar
  25. 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
  26. Elton CS (2001) Animal ecology. University of Chicago Press, ChicagoGoogle Scholar
  27. Emmering QC, Schmidt KA (2011) Nesting songbirds assess spatial heterogeneity of predatory chipmunks by eavesdropping on their vocalizations. J Anim Ecol 80:1305–1312CrossRefGoogle Scholar
  28. Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ, Datta SR, Spehr M, Fendt M, Liberles SD (2011) Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci USA 108:11235–11240CrossRefGoogle Scholar
  29. Fontaine JJ, Martin TE (2006) Habitat selection responses of parents to offspring predation risk: an experimental test. Am Nat 168:811–818CrossRefGoogle Scholar
  30. Forsman JT, Monkkonen M, Korpimaki E, Thomson RL (2013) Mammalian nest predator feces as a cue in avian habitat selection decisions. Behav Ecol 24:262–266CrossRefGoogle Scholar
  31. Gagliardo A (2013) Forty years of olfactory navigation in birds. J Exp Biol 216:2165–2171CrossRefGoogle Scholar
  32. Hagelin JC, Jones IL (2007) Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 124:741–761CrossRefGoogle Scholar
  33. Kavaliers M, Choleris E, Pfaff DW (2005) Recognition and avoidance of the odors of parasitized conspecifics and predators: differential genomic correlates. Neurosci Biobehav Rev 29:1347–1359CrossRefGoogle Scholar
  34. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  35. Martin TE (1993) Nest predation among vegetation layers and habitat types—revising the dogmas. Am Nat 141:897–913CrossRefGoogle Scholar
  36. Monkkonen M, Forsman JT, Kananoja T, Ylonen H (2009) Indirect cues of nest predation risk and avian reproductive decisions. Biol Let 5:176–178CrossRefGoogle Scholar
  37. Nevitt GA, Bonadonna F (2005) Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol Let 1:303–305CrossRefGoogle Scholar
  38. Nevitt GA, Veit RR, Kareiva P (1995) Dimethyl sulfide as a foraging cue for Antarctic Procellariiform seabirds. Nature 376:680–682CrossRefGoogle Scholar
  39. Nice MM (1957) Nesting success in altricial birds. Auk 74:305–321CrossRefGoogle Scholar
  40. Parejo D, Aviles JM (2011) Predation risk determines breeding territory choice in a Mediterranean cavity-nesting bird community. Oecologia 165:185–191CrossRefGoogle Scholar
  41. Parejo D, Danchin E, Aviles JM (2005) The heterospecific habitat copying hypothesis: can competitors indicate habitat quality? Behav Ecol 16:96–105CrossRefGoogle Scholar
  42. Parejo D, Amo L, Rodriguez J, Aviles JM (2012a) Rollers smell the fear of nestlings. Biol Let 8:502–504CrossRefGoogle Scholar
  43. Parejo D, Aviles JM, Rodriguez J (2012b) Alarm calls modulate the spatial structure of a breeding owl community. Proc R Soc B Biol Sci 279:2135–2141CrossRefGoogle Scholar
  44. Parejo D, Aviles JM, Exposito-Granados M (2018) Receivers matter: the meaning of alarm calls and competition for nest sites in a bird community. Oecologia 187:707–717CrossRefGoogle Scholar
  45. Parsons MH, Apfelbach R, Banks PB, Cameron EZ, Dickman CR, Frank ASK, Jones ME, McGregor IS, McLean S, Muller-Schwarze D, Sparrow EE, Blumstein DT (2018) Biologically meaningful scents: a framework for understanding predator-prey research across disciplines. Biol Rev 93:98–114CrossRefGoogle Scholar
  46. Peluc SI, Sillett TS, Rotenberry JT, Ghalambor CK (2008) Adaptive phenotypic plasticity in an island songbird exposed to a novel predation risk. Behav Ecol 19:830–835CrossRefGoogle Scholar
  47. Petit C, Hossaert-McKey M, Perret P, Blondel J, Lambrechts MM (2002) Blue tits use selected plants and olfaction to maintain an aromatic environment for nestlings. Ecol Lett 5:585–589CrossRefGoogle Scholar
  48. Rodriguez J, Aviles JM, Parejo D (2011) The value of nestboxes in the conservation of Eurasian Rollers Coracias garrulus in southern Spain. Ibis 153:735–745CrossRefGoogle Scholar
  49. Rossi M, Marfull R, Goluke S, Komdeur J, Korsten P, Caspers BA (2017) Begging blue tit nestlings discriminate between the odour of familiar and unfamiliar conspecifics. Funct Ecol 31:1761–1769CrossRefGoogle Scholar
  50. Seppanen JT, Forsman JT, Monkkonen M, Thomson RL (2007) Social information use is a process across time, space, and ecology, reaching heterospecifics. Ecology 88:1622–1633CrossRefGoogle Scholar
  51. Sharp JG, Garnick S, Elgar MA, Coulson G (2015) Parasite and predator risk assessment: nuanced use of olfactory cues. Proc R Soc B Biol Sci 282:5CrossRefGoogle Scholar
  52. Stanbury M, Briskie JV (2015) I smell a rat: can New Zealand birds recognize the odor of an invasive mammalian predator? Curr Zool 61:34–41CrossRefGoogle Scholar
  53. Sunyer P, Munoz A, Bonal R, Espelta JM (2013) The ecology of seed dispersal by small rodents: a role for predator and conspecific scents. Funct Ecol 27:1313–1321CrossRefGoogle Scholar
  54. Taraborelli PA, Moreno P, Srur A, Sandobal AJ, Martinez MG, Giannoni SM (2008) Different antipredator responses by Microcavia australis (Rodentia, Hystricognate, Caviidae) under predation risk. Behaviour 145:829–842CrossRefGoogle Scholar
  55. Veiga JP, Polo V, Vinuela J (2006) Nest green plants as a male status signal and courtship display in the spotless starling. Ethology 112:196–204CrossRefGoogle Scholar
  56. Wenzel BM, Sieck MH (1972) Olfactory perception and bulbar electrical-activity in several avian species. Physiol Behav 9:287–293CrossRefGoogle Scholar
  57. Werner SJ, Cummings JL, Pipas PA, Tupper SK, Byrd RW (2008) Registered pesticides and citrus terpenes as blackbird repellents for rice. J Wildl Manag 72:1863–1868CrossRefGoogle Scholar
  58. Whittaker DJ, Reichard DG, Dapper AL, Ketterson ED (2009) Behavioral responses of nesting female dark-eyed juncos Junco hyemalis to hetero- and conspecific passerine preen oils. J Avian Biol 40:579–583CrossRefGoogle Scholar
  59. Zelenitsky DK, Therrien FO, Ridgely RC, Mcgee AR, Witmer LM (2011) Evolution of olfaction in non-avian theropod dinosaurs and birds. Proc R Soc B Biol Sci 278:3625–3634CrossRefGoogle Scholar
  60. Zuur AF (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Functional and Evolutionary EcologyEEZA-CSICAlmeríaSpain
  2. 2.Department of Anatomy, Cellular Biology and ZoologyUniversity of ExtremaduraBadajozSpain

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