Skip to main content
SpringerLink
Log in

Effects of nest predation risk on female incubation behavior and offspring growth in great tits

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Predation risk is a key driver for the evolution of reproductive strategies and life history traits. In birds, incubation behavior represents one form of parental care where trade-offs between time spent in incubation activities and self-maintenance activities are likely to change in response to predator pressure. This can have strong effects on embryonic development, but is still poorly understood. We investigated the effects of the presence of a nest predator on great tit (Parus major) incubation behavior and the subsequent effects of incubation on nestling morphological traits. We manipulated perceived predation risk using models of short-tailed weasels (Mustela erminea) in combination with great tit alarm calls specific to this predator. Directly after hatching, we swapped whole broods from treated nests with broods from untreated nests to disentangle treatment effects acting during the incubation period from potential carry-over effects on parental care acting on nestlings after hatching. In increased predation risk environments, the number of incubation sessions and recesses, but not their duration, was increased compared to the control group, and the nocturnal incubation session was longer when females were exposed to a predator. Eggs incubated by females under increased predation risk lost more mass over the incubation period compared to the control group. Also, male nestlings hatched from nests exposed to predators were lighter at hatching but were equivalent in weight to their control counterparts at fledging. This suggests that nest predation risk can influence some aspects of incubation rhythm and embryonic development, but has no long-term effects on nestling final body size.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Angelier F, Chastel O (2009) Stress, prolactin and parental investment in birds: a review. Gen Comp Endocrinol 163:142–148

    Article  CAS  PubMed  Google Scholar 

  • Ardia DR, Perez JH, Clotfelter ED (2010) Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proc R Soc Lond B 277:1881–1888

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2011) lme4. Linear mixed-effects models using S4 classes R package version 0999375–34. http://CRANR-projectorg/package=lme4

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Bosque C, Bosque MT (1995) Nest predation as a selective factor in the evolution of developmental rates in altricial birds. Am Nat 145:234–260

    Article  Google Scholar 

  • Cheng YR, Martin TE (2012) Nest predation risk and growth strategies of passerine species: grow fast or develop traits to escape risk? Am Nat 180:285–295

    Article  PubMed  Google Scholar 

  • Colombelli-Négrel D, Hauber ME, Kleindorfer S (2014) Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos. Proc R Soc B 281:20141154

    Article  PubMed  Google Scholar 

  • Conway CJ, Martin TE (2000a) Effects of ambient temperature on avian incubation behavior. Behav Ecol 11:178–188

    Article  Google Scholar 

  • Conway CJ, Martin TE (2000b) Evolution of passerine incubation behavior: influence of food, temperature, and nest predation. Evolution 54:670–685

    Article  CAS  PubMed  Google Scholar 

  • Cooper CB, Mills J (2005) New software for quantifying incubation behavior from time-series recordings. J Field Ornithol 76:352–356

    Article  Google Scholar 

  • Coslovsky M, Richner H (2011) Predation risk affects offspring growth via maternal effects. Funct Ecol 25:878–888

    Article  Google Scholar 

  • Coslovsky M, Richner H (2012) An experimental test of predator–parasite interaction in a passerine bird. Oikos 121:1691–1701

    Article  Google Scholar 

  • de Heij ME, van den Hout PJ, Tinbergen JM (2006) Fitness cost of incubation in great tits (Parus major) is related to clutch size. Proc R Soc Lond B 273:2353–2361

    Article  Google Scholar 

  • Deeming DC (2002) Avian incubation. Behaviour, environment, and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Dickman CR (1988) Age-related dietary change in the European hedgehog, Erinaceus europaeus. J Zool 215:1–14

    Article  Google Scholar 

  • DuRant SE, Hopkins WA, Hepp GR, Walters JR (2013) Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds. Biol Rev Camb Philos Soc 88:499–509

    Article  PubMed  Google Scholar 

  • Eggers S, Griesser M, Ekman J (2005) Predator-induced plasticity in nest visitation rates in the Siberian jay (Perisoreus infaustus). Behav Ecol 16:309–315

    Article  Google Scholar 

  • Ellegren H (1996) First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proc R Soc Lond B 263:1635–1641

    Article  CAS  Google Scholar 

  • Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971

    Article  Google Scholar 

  • Fontaine JJ, Martin TE (2006) Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol Lett 9:428–434

    Article  CAS  PubMed  Google Scholar 

  • Ghalambor CK, Martin TE (2002) Comparative manipulation of predation risk in incubating birds reveals variability in the plasticity of responses. Behav Ecol 13:101–108

    Article  Google Scholar 

  • Ghalambor CK, Peluc SI, Martin TE (2013) Plasticity of parental care under the risk of predation: how much should parents reduce care? Biol Lett 9:20130154

    Article  PubMed Central  PubMed  Google Scholar 

  • Gosler A (1993) The great tit. Hamlyn, London

    Google Scholar 

  • Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2005) Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proc R Soc Lond B 272:1039–1046

    Article  Google Scholar 

  • Hawlena D, Schmitz OJ (2010) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556

    Article  PubMed  Google Scholar 

  • Ibáñez-Álamo JD, Soler M (2012) Predator-induced female behavior in the absence of male incubation feeding: an experimental study. Behav Ecol Sociobiol 66:1067–1073

    Article  Google Scholar 

  • Jones G (1989) Optimizing time off the nest during incubation in female swallows (Hirundo rustica L.). Funct Ecol 3:303–309

    Article  Google Scholar 

  • Korpimäki E, Norrdahl K, Rintajaskari T (1991) Responses of stoats and least weasels to fluctuating food abundances — is the low phase of the vole cycle due to mustelid predation. Oecologia 88:552–561

    Article  Google Scholar 

  • Kovarik P, Pavel V (2011) Does threat to the nest affect incubation rhythm in a small passerine? Ethology 117:181–187

    Article  Google Scholar 

  • Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions — what are the ecological effects of anti-predator decision-making? Bioscience 48:25–34

    Article  Google Scholar 

  • Lima SL (2009) Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biol Rev Camb Philos Soc 84:485–513

    Article  PubMed  Google Scholar 

  • Martin TE (1995) Avian life-history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127

    Article  Google Scholar 

  • Martin TE, Briskie JV (2009) Predation on dependent offspring: a review of the consequences for mean expression and phenotypic plasticity in avian life history traits. Ann NY Acad Sci 1168:201–217

    Article  PubMed  Google Scholar 

  • Martin TE, Ghalambor CK (1999) Males feeding females during incubation: I. Required by microclimate or constrained by nest predation. Am Nat 153:131–139

    Article  Google Scholar 

  • Martin TE, Scott J, Menge C (2000) Nest predation increases with parental activity: separating nest site and parental activity effects. Proc R Soc Lond B 267:2287–2293

    Article  CAS  Google Scholar 

  • Martin TE, Auer SK, Bassar RD, Niklison AM, Lloyd P (2007) Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution 61:2558–2569

    Article  PubMed  Google Scholar 

  • Montgomerie RD, Weatherhead PJ (1988) Risks and rewards of nest defense by parent birds. Q Rev Biol 63:167–187

    Article  Google Scholar 

  • Nilsson SG (1984) The evolution of nest-site selection among hole-nesting birds — the importance of nest predation and competition. Ornis Scand 15:167–175

    Article  Google Scholar 

  • Nord A, Nilsson JA (2011) Incubation temperature affects growth and energy metabolism in blue tit nestlings. Am Nat 178:639–651

    Article  PubMed  Google Scholar 

  • Nord A, Nilsson JA (2012) Context-dependent costs of incubation in the pied flycatcher. Anim Behav 84:427–436

    Article  Google Scholar 

  • Oddie KR (2000) Size matters: competition between male and female great tit offspring. J Anim Ecol 69:903–912

    Article  Google Scholar 

  • Olioso G (2004) Les mésanges. Les sentiers du naturaliste. Delachaux et Niestlé, Paris

    Google Scholar 

  • Peluc SI, Sillett TS, Rotenberry JT, Ghalambor CK (2008) Adaptive phenotypic plasticity in an island songbird exposed to a novel predation risk. Behav Ecol 19:830–835

    Article  Google Scholar 

  • Perrins CM (1965) Population fluctuations and clutch-size in the great tit, Parus major L. J Anim Ecol 34:601–647

    Article  Google Scholar 

  • Perrins CM (1979) British tits. Collins, London

    Google Scholar 

  • Pitk M, Tilgar V, Kilgas P, Mand R (2012) Acute stress affects the corticosterone level in bird eggs: a case study with great tits (Parus major). Horm Behav 62:475–479

    Article  CAS  PubMed  Google Scholar 

  • Rastogi AD, Zanette L, Clinchy M (2006) Food availability affects diurnal nest predation and adult antipredator behaviour in song sparrows, Melospiza melodia. Anim Behav 72:933–940

    Article  Google Scholar 

  • Remes V, Martin TE (2002) Environmental influences on the evolution of growth and developmental rates in passerines. Evolution 56:2505–2518

    Article  PubMed  Google Scholar 

  • Royama T (1966) Factors governing feeding rate, food requirement and brood size of nestling great tits Parus major. Ibis 108:313–347

    Article  Google Scholar 

  • Sanz JJ (1997) Clutch size manipulation in the pied flycatcher: effects on nestling growth, parental care and moult. J Avian Biol 28:157–162

    Article  Google Scholar 

  • Schwagmeyer P, Mock DW, Lamey TC, Beecher MD (1991) Effects of sibling contact on hatch timing in an asynchronously hatching bird. Anim Behav 41:887–894

    Article  Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2010) The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91:2983–2994

    Article  PubMed  Google Scholar 

  • Silverin B (1998) Behavioural and hormonal responses of the pied flycatcher to environmental stressors. Anim Behav 55:1411–1420

    Article  PubMed  Google Scholar 

  • Smith PA, Tulp I, Schekkerman H, Gilchrist HG, Forbes MR (2012) Shorebird incubation behaviour and its influence on the risk of nest predation. Anim Behav 84:835–842

    Article  Google Scholar 

  • Travers M, Clinchy M, Zanette L, Boonstra R, Williams TD (2010) Indirect predator effects on clutch size and the cost of egg production. Ecol Lett 13:980–988

    PubMed  Google Scholar 

  • Vince MA (1969) Embryonic communication, respiration and the synchronization of hatching. In: Hinde RA (ed) Bird vocalizations. Cambridge University Press, Cambridge, pp 233–260

    Google Scholar 

  • Wang JM, Beissinger SR (2009) Variation in the onset of incubation and its influence on avian hatching success and asynchrony. Anim Behav 78:601–613

    Article  Google Scholar 

  • Zanette LY, White AF, Allen MC, Clinchy M (2011) Perceived predation risk reduces the number of offspring songbirds produce per year. Science 334:1398–1401

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Henrietta Bellman, Sanne Ruyts, and Fabiano Sartirana for field assistance and Andreas Nord and Michael Coslovsky for useful comments on the manuscript. Taxidermic models were provided by Christian Schneiter (Arche de Noé, Viques). The work was funded by the Swiss National Science Foundation (grant 31003A_122566 to HR).

Ethical standards

This work was conducted under license of the Ethical Committee of the Agricultural Office of the Canton Bern (BE22/11). Bird catching and ringing were performed with a permission of the Federal Agency for the Environment of the Canton of Bern, Switzerland (ringing permit 2992).

Author information

Authors and Affiliations

  1. Evolutionary Ecology Lab, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012, Bern, Switzerland

    Alessandra Basso & Heinz Richner

Authors
  1. Alessandra Basso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heinz Richner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alessandra Basso.

Additional information

Communicated by M. Leonard

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 99 kb)

ESM 2

(DOCX 173 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Basso, A., Richner, H. Effects of nest predation risk on female incubation behavior and offspring growth in great tits. Behav Ecol Sociobiol 69, 977–989 (2015). https://doi.org/10.1007/s00265-015-1910-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-1910-4

Keywords

Search

Navigation