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Incubating terns modify risk-taking according to diurnal variations in egg camouflage and ambient temperature

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Abstract

Studies of risk-taking by breeding birds have frequently addressed the effect of brood value on the decisions taken by incubating birds when predators approach their nests. However, leaving eggs unattended during predator disturbance may expose embryos to other potentially harmful factors, to which parent birds should respond when making decisions about when to leave or return to their nest. In this study, we show that diurnal changes in flushing behaviour of incubating terns from nests during predator approach were affected by egg camouflage, the terns allowing a closer approach to individual nests when the eggs appeared better camouflaged. Return times to the nests were affected by ambient temperature, with the terns shortening such times at high ambient temperatures, thus diminishing the risk of egg overheating. As a whole, our results show that the decisions of the birds on when to leave or return to their nests depended on shifting payoffs, as a consequence of diurnal variations in both the thermal risks incurred by embryos and egg crypsis. Environmental costs of risk-taking, such as those considered here, should be addressed in studies of risk-taking by breeding birds. This type of study may have implications for our knowledge of cognitive processes that affect risk-taking.

Significance statement

When a predator approaches a nest, the incubating bird has to decide at which moment to leave the nest, which may be affected by environmental factors that may hamper embryo viability. We studied flushing/returning behaviour of incubating little terns Sternula albifrons in response to disturbance and show that risk-taking was affected by the occurrence of simultaneous environmental threats according to shifting fitness payoffs. When the eggs appeared better camouflaged, which usually occurred around midday, the terns allowed closer approach to individual nests. The terns shortened the return to their nests with increasing ambient temperature, which took place at midday. Thus, our results show that, by adjusting their responses to shifting payoffs, the terns modulated the risks incurred by their offspring, as eggs were less time exposed to direct solar radiation in midday, when the risk of overheating was higher.

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References

  • Amat JA, Masero JA (2004a) Predation risk on incubating adults constrains the choice of thermally favourable nest sites in a plover. Anim Behav 67:293–300

    Article  Google Scholar 

  • Amat JA, Masero JA (2004b) How Kentish plovers, Charadrius alexandrinus, cope with heat stress during incubation. Behav Ecol Sociobiol 56:26–33

    Article  Google Scholar 

  • Amat JA, Masero JA (2007) The functions of belly-soaking in Kentish plovers Charadrius alexandrinus. Ibis 149:91–97

    Article  Google Scholar 

  • Amat JA, Carrascal LM, Moreno J (1996) Nest defence by chinstrap penguins in relation to offspring number and age. J Avian Biol 27:177–179

    Article  Google Scholar 

  • Amat JA, Monsa R, Masero JA (2012) Dual function of egg-covering in the Kentish plover Charadrius alexandrinus. Behaviour 149:881–895

    Article  Google Scholar 

  • Brown M, Brown K (2004) Nest defence in crowned lapwings (Vanellus coronatus)—influences of nesting stage and ambient temperature. Ostrich 75:162–164

    Article  Google Scholar 

  • Brunton DH (1986) Fatal antipredator behavior of a killdeer. Wilson Bull 98:605–607

    Google Scholar 

  • Burham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Cantarero A, López-Arrabé J, Plaza M, Saavedra-Garcés I, Moreno J (2016) Males feed their mates more and take more risks for nestlings with larger female-built nests: an experimental study in the nuthatch Sitta europaea. Behav Ecol Sociobiol 70:1141–1150

    Article  Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Colwell MA, Meyer JJ, Hardy MA, MacAllister SE, Transou AN, Levalley RR, Dinsmore SJ (2011) Western snowy plover Charadrius alexandrinus nivosus select nesting substrates that enhance egg crypsis and improve nest survival. Ibis 153:303–311

    Article  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 

  • Cramp S (ed) (1985) The birds of the western Palearctic, vol IV. Oxford University Press, Oxford

    Google Scholar 

  • Dell Inc (2015) STATISTICA (data analysis software system), version 12. www.statsoft.com

  • Ekanayake KB, Weston MA, Nimmo DG, Maguire GS, Endler JA, Küpper C (2015) The bright incubate at night: sexual dichromatism and adaptive incubation division in an open-nesting shorebird. Proc R Soc B 282:20143026

    Article  PubMed  PubMed Central  Google Scholar 

  • Endler JA (1991) Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vis Res 31:587–608

    Article  CAS  PubMed  Google Scholar 

  • Endler JA, Thery M (1996) Interacting effects of lek placement, display behavior, ambient light, and color patterns in three neotropical forest dwelling birds. Am Nat 148:421–452

    Article  Google Scholar 

  • Enquist M, Leimar O, Ljungberg T, Mallner Y, Segerdahl N (1990) A test of the sequential assessment game: fighting in the cichlid fish Nannacara anomala. Anim Behav 40:1–14

    Article  Google Scholar 

  • Faillace CA, Smith BW (2016) Incubating snowy plovers (Charadrius nivosus) exhibit site-specific patterns of disturbance from human activities. Wildlife Res 43:288–297

    Article  Google Scholar 

  • Fasola M, Saino N (1995) Sex-biased parental care allocation in three tern species (Laridae, Aves). Can J Zool 73:1461–1467

    Article  Google Scholar 

  • Forbes MRL, Clark RG, Weatherhead PJ, Armstrong T (1994) Risk-taking by female ducks: intra- and interspecific tests of nest defense theory. Behav Ecol Sociobiol 34:79–85

    Article  Google Scholar 

  • Fraga RM, Amat JA (1996) Breeding biology of a Kentish plover (Charadrius alexandrinus) population in an inland saline lake. Ardeola 43:69–85

    Google Scholar 

  • Gómez J, Pereira AI, Pérez-Hurtado A, Castro M, Ramo C, Amat JA (2016) A trade-off between overheating and camouflage on shorebird eggshell colouration. J Avian Biol 47:346–353

  • Gómez-Serrano MA, López-López P (2017) Deceiving predators: linking distraction behavior with nest survival in a ground-nesting bird. Behav Ecol 28:260–269

    Article  Google Scholar 

  • Grant GS (1982) Avian incubation: egg temperature, nest humidity, and behavioral thermoregulation in a hot environment. Ornithol Monogr 30:1–75

    Google Scholar 

  • Kleindorfer S, Fessl B, Hoi H (2005) Avian nest defence behaviour: assessment in relation to predator distance and type, and nest height. Anim Behav 69:307–313

    Article  Google Scholar 

  • Knight RL, Temple SA (1986) Why does intensity of nest defense increase during the nesting cycle. Auk 103:318–327

    Google Scholar 

  • Lee WS, Kwon YS, Yoo JC (2010) Egg survival is related to the colour matching of eggs to nest background in black-tailed gulls. J Ornithol 151:765–770

    Article  Google Scholar 

  • Lord A, Waas JR, Innes J, Whittingham MJ (2001) Effects of human approaches to nests of northern New Zealand dotterels. Biol Conserv 98:233–240

    Article  Google Scholar 

  • Lovell PG, Ruxton GD, Landgridge KV, Spencer AA (2013) Egg-laying substrate selection for optimal camouflage by quail. Curr Biol 23:260–264

    Article  CAS  PubMed  Google Scholar 

  • Maclean GL (1967) The breeding biology and behaviour of the double-banded courser Rhynoptilus africanus (Temminck). Ibis 109:556–569

    Article  Google Scholar 

  • MATLAB (2013) MATLAB release. The MathWorks Inc, Natick

    Google Scholar 

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

    Article  Google Scholar 

  • Nguyen LP, Nol E, Abraham KF (2007) Using digital photographs to evaluate the effectiveness of plover egg crypsis. J Wildlife Manage 71:2084–2089

    Article  Google Scholar 

  • Palestis BG (2005) Nesting stage and nest defense by common terns. Waterbirds 28:87–94

    Article  Google Scholar 

  • Pereira AI, Amat JA (2010) Nesting of the double-striped thick-knee (Burhinus bistriatus) in a hot environment. Ornithol Neotrop 21:149–154

    Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New York

    Book  Google Scholar 

  • Pinheiro JC, Bates DM, DebRoy S, Sarkar D (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1–125, http://CRAN.Rproject.org/package=nlme

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/

    Google Scholar 

  • Redondo T (1989) Avian nest defence: theoretical models and evidence. Behaviour 111:161–195

    Article  Google Scholar 

  • Redondo T, Carranza J (1989) Offspring reproductive value and nest defense in the magpie (Pica pica). Behav Ecol Sociobiol 25:369–378

    Article  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. The evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford

    Book  Google Scholar 

  • Sergio F, Bogliani G (2001) Nest defense as parental care in the northern hobby (Falco subbuteo). Auk 118:1047–1052

    Article  Google Scholar 

  • Serra J (1983) Image analysis and mathematical morphology. Academic, Orlando

    Google Scholar 

  • Skrade PDB, Dinsmore SJ (2013) Egg crypsis in a ground-nesting shorebird influences nest survival. Ecosphere 4:151

    Article  Google Scholar 

  • Smith PA, Wilson S (2010) Intraseasonal patterns in shorebird nest survival are related to nest age and defence behaviour. Oecologia 163:613–624

    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 

  • Solís JC, de Lope F (1995) Nest and egg crypsis in the ground-nesting stone curlew Burhinus oedicnemus. J Avian Biol 26:135–138

    Article  Google Scholar 

  • St Clair JJH, García-Peña GE, Woods RW, Székely T (2010) Presence of mammalian predators decreases tolerance to human disturbance in a breeding shorebird. Behav Ecol 21:1285–1292

    Article  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  • Troscianko J, Wilson-Aggarwal J, Stevens M, Sppottiswoode CN (2016) Camouflage predicts survival in ground-nesting birds. Sci Rep 6:19966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valverde JA (1960) Vertebrados de las marismas del Guadalquivir. (Introducción a su estudio ecológico). Arch Inst Aclim Almería 9:1–168

    Google Scholar 

  • Ward D (1990) Incubation temperatures of crowned, black-winged, and lesser black-winged plovers. Auk 107:10–17

    Google Scholar 

  • Webb DR (1987) Thermal tolerance of avian embryos: a review. Condor 89:874–898

    Article  Google Scholar 

  • Weston MA, McLeod EM, Blumstein DT, Guay P-J (2012) A review of flight initiation distances and their application to managing disturbance to Australian birds. Emu 112:269–286

    Article  Google Scholar 

  • Wilson-Aggarwal JK, Troscianko JT, Stevens M, Spottiswoode CN (2016) Escape distance in ground-nesting birds differs with individual level of camouflage. Am Nat 188:231–239

    Article  PubMed  Google Scholar 

  • Yasué M, Dearden P (2006) The effects of heat stress, predation risk and parental investment on Malaysian plover nest return times following a human disturbance. Biol Conserv 132:472–480

    Article  Google Scholar 

  • Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Stud Behav 16:229–249

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

We thank Enríque Martínez, Director of Paraje Natural Marismas del Odiel (Consejería de Medio Ambiente, Junta de Anadalucía), for facilities. Kate Lessells and anonymous referees commented on previous versions.

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Authors and Affiliations

  1. Estación Biológica de Doñana (EBD-CSIC), Seville, Spain

    Juan A. Amat, Jesús Gómez, Miguel A. Rendón & Cristina Ramo

  2. Instituto de Microelectrónica de Sevilla (IMSE-CNM CSIC), Universidad de Sevilla, Seville, Spain

    Gustavo Liñán-Cembrano

Authors
  1. Juan A. Amat
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  2. Jesús Gómez
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  3. Gustavo Liñán-Cembrano
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  4. Miguel A. Rendón
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  5. Cristina Ramo
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Correspondence to Juan A. Amat.

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Funding

Financial support was received from Consejería de Innovación, Ciencia y Empresa of the Junta de Andalucía (PAIDI research group RNM361) and partly from Ministerio de Ciencia e Innovación/EU-ERDF (Grant CGL2011-24230). JG was supported by a predoctoral fellowship from Ministerio de Educación, Cultura y Deporte (FPU12/01616).

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The authors declare that they have no conflict of interest.

Ethical approval

Consejería de Medio Ambiente from the Junta de Andalucía (Regional Government) gave permission to conduct the study.

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Communicated by M. Leonard

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Amat, J.A., Gómez, J., Liñán-Cembrano, G. et al. Incubating terns modify risk-taking according to diurnal variations in egg camouflage and ambient temperature. Behav Ecol Sociobiol 71, 72 (2017). https://doi.org/10.1007/s00265-017-2306-4

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  • DOI: https://doi.org/10.1007/s00265-017-2306-4

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