Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Bird embryos perceive vibratory cues of predation risk from clutch mates

Nature Ecology & Evolution volume 3, pages 1225–1232 (2019)Cite this article

Subjects

Abstract

During development in fluctuating environments, phenotypes can be adjusted to the conditions that individuals will probably encounter later in life. As developing embryos have a limited capacity to fully capture environmental information, theory predicts that they should integrate relevant information from all reliable sources, including the social environment. In many oviparous species, embryos are able to perceive cues of predator presence in some circumstances, but whether this information is socially transmitted among clutch mates—promoting phenotypic adjustments in the whole clutch—is unknown. Here, using an experimental design for which we modified the exposure to some, but not all, embryos of the same clutch to cues of predator presence (that is, alarm calls), we show that exposed embryos of the yellow-legged gull (Larus michahellis) and their unexposed clutch mates showed similar developmental changes that were absent in embryos from control clutches. Compared with the control broods, both embryos that were exposed to alarm calls and their unexposed clutch mates showed altered prenatal and postnatal behaviours, higher levels of DNA methylation and stress hormones, and reduced growth and numbers of mitochondria (which may be indicative of the capacity for energy production of cells). These results strongly suggest that gull embryos are able to acquire relevant environmental information from their siblings. Together, our results highlight the importance of socially acquired information during the prenatal stage as a non-genetic mechanism promoting developmental plasticity.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Schematic of prenatal and postnatal exposure of gull embryos to social cues that indicate the presence of predators
Fig. 2: Prenatal exposure to adult alarm calls delayed hatching, increased the rate of egg vibration, promoted a higher level of global DNA methylation and basal corticosterone, and enhanced prenatal and postnatal antipredator responses.
Fig. 3: Prenatal exposure to adult alarm calls reduced mitochondrial content and the growth of the chicks

Data availability

All of the data needed to evaluate the conclusions in the paper are presented in the paper and/or the Supplementary Information. The raw data can also be found in the Figshare digital repository: https://doi.org/10.6084/m9.figshare.6510092.

References

  1. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003).

  2. Uller, T. Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol. 23, 432–438 (2008).

    Article  Google Scholar 

  3. Nettle, D. & Bateson, M. Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proc. R. Soc. B 282, 20151005 (2015).

    Article  Google Scholar 

  4. Jablonka, E. & Raz, G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84, 131–176 (2009).

    Article  Google Scholar 

  5. Laubach, Z. M. et al. Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework. Biol. Rev. 93, 1323–1338 (2018).

    Article  Google Scholar 

  6. Champagne, F. A. Epigenetic influence of social experiences across the lifespan. Dev. Psychobiol. 52, 299–311 (2010).

    Article  CAS  Google Scholar 

  7. Harris, K. D., Bartlett, N. J. & Lloyd, V. K. Daphnia as an emerging epigenetic model organism. Genet. Res. Int. 2012, 147892 (2012).

    PubMed  PubMed Central  Google Scholar 

  8. Groothuis, T. G. G., Müller, W., von Engelhardt, N., Carere, C. & Eising, C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29, 329–352 (2005).

    Article  CAS  Google Scholar 

  9. Marshall, D. & Uller, T. When is a maternal effect adaptive? Oikos 116, 1957–1963 (2007).

    Article  Google Scholar 

  10. Mousseau, T. A., Uller, T., Wapstra, E. & Badyaev, A. V. Evolution of maternal effects: past and present. Philos. Trans. R. Soc. B 364, 1035–1038 (2009).

    Article  Google Scholar 

  11. Mariette, M. M. & Buchanan, K. L. Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird. Science 353, 812–814 (2016).

    Article  CAS  Google Scholar 

  12. Aubret, F., Blanvillain, G., Bignon, F. & Kok, P. J. Heartbeat, embryo communication and hatching synchrony in snake eggs. Sci. Rep. 6, 23519 (2016).

    Article  CAS  Google Scholar 

  13. Doody, J. S., Stewart, B., Camacho, C. & Christian, K. Good vibrations? Sibling embryos expedite hatching in a turtle. Anim. Behav. 83, 645–651 (2012).

    Article  Google Scholar 

  14. McGlashan, J. K., Spencer, R.-J. & Old, J. M. Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings. Proc. R. Soc. B 279, 1709–1715 (2012).

    Article  Google Scholar 

  15. Vince, M. in Bird Vocalizations (ed. Hinde, R. A.) 88–89 (Cambridge Univ. Press, 1969).

  16. Warkentin, K. M. How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs. Anim. Behav. 70, 59–71 (2005).

    Article  Google Scholar 

  17. Middlemis Maher, J., Werner, E. E. & Denver, R. J. Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc. R. Soc. B 280, 20123075 (2013).

    Article  Google Scholar 

  18. Warkentin, K. M. Wasp predation and wasp-induced hatching of red-eyed treefrog eggs. Anim. Behav. 60, 503–510 (2000).

    Article  CAS  Google Scholar 

  19. Benard, M. F. Predator-induced phenotypic plasticity in organisms with complex life histories. Annu. Rev. Ecol. Evol. Syst. 35, 651–673 (2004).

    Article  Google Scholar 

  20. Noguera, J. C., Kim, S.-Y. & Velando, A. Family-transmitted stress in a wild bird. Proc. Natl Acad. Sci. USA 114, 6794–6799 (2017).

    Article  CAS  Google Scholar 

  21. Harvell, C. D. The ecology and evolution of inducible defenses. Q. Rev. Biol. 65, 323–340 (1990).

    Article  CAS  Google Scholar 

  22. McNamara, J. M., Dall, S. R., Hammerstein, P. & Leimar, O. Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments. Ecol. Lett. 19, 1267–1276 (2016).

    Article  Google Scholar 

  23. Munoz, N. E. & Blumstein, D. T. Multisensory perception in uncertain environments. Behav. Ecol. 23, 457–462 (2012).

    Article  Google Scholar 

  24. Stamps, J. A. & Frankenhuis, W. E. Bayesian models of development. Trends Ecol. Evol. 31, 260–268 (2016).

    Article  Google Scholar 

  25. Freeman, B. M. & Vince, M. A. Development of the Avian Embryo: A Behavioural and Physiological Study (Chapman and Hall, 1974).

  26. Persson, I. & Andersson, G. Intraclutch hatch synchronization in pheasants and mallard ducks. Ethology 105, 1087–1096 (1999).

    Article  Google Scholar 

  27. Spencer, R. J., Thompson, M. B. & Banks, P. B. Hatch or wait? A dilemma in reptilian incubation. Oikos 93, 401–406 (2001).

    Article  Google Scholar 

  28. Velando, A., Morán, P., Romero, R., Fernández, J. & Piorno, V. Invasion and eradication of the American mink in the Atlantic Islands National Park (NW Spain): a retrospective analysis. Biol. Invasions 19, 1227–1241 (2017).

    Article  Google Scholar 

  29. Tinbergen, N. The Herring Gull’s World: A Study of the Social Behaviour of Birds (Collins, 1953).

  30. Morales, J., Lucas, A. & Velando, A. Maternal programming of offspring antipredator behavior in a seabird. Behav. Ecol. 29, 479–485 (2018).

    Article  Google Scholar 

  31. Rumpf, M. & Tzschentke, B. Perinatal acoustic communication in birds: why do birds vocalize in the egg? Open Ornithol. J. 3, 141–149 (2010).

    Article  Google Scholar 

  32. Impekoven, M. & Gold, P. S. in Studies on the Development of Behavior and the Nervous System (eds Whitsett, J. M., Vandenbergh, J. G. and Gottlieb, G.) 325–356 (Elsevier, 1973).

  33. Manoli, I. et al. Mitochondria as key components of the stress response. Trends Endrocrinol. Metab. 18, 190–198 (2007).

    Article  CAS  Google Scholar 

  34. Herborn, K. A. et al. Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird. Proc. R. Soc. B 281, 20133151 (2014).

    Article  Google Scholar 

  35. Tona, K. et al. Effects of storage time on incubating egg gas pressure, thyroid hormones, and corticosterone levels in embryos and on their hatching parameters. Poult. Sci. 82, 840–845 (2003).

    Article  CAS  Google Scholar 

  36. Tawa, R., Ono, T., Kurishita, A., Okada, S. & Hirose, S. Changes of DNA methylation level during pre‐and postnatal periods in mice. Differentiation 45, 44–48 (1990).

    Article  CAS  Google Scholar 

  37. Reik, W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425–432 (2007).

    Article  CAS  Google Scholar 

  38. Yan, X.-p et al. Evidence in duck for supporting alteration of incubation temperature may have influence on methylation of genomic DNA. Poult. Sci. 94, 2537–2545 (2015).

    Article  CAS  Google Scholar 

  39. Laine, V. N. et al. Evolutionary signals of selection on cognition from the great tit genome and methylome. Nat. Commun. 7, 10474 (2016).

    Article  CAS  Google Scholar 

  40. Derks, M. F. et al. Gene and transposable element methylation in great tit (Parus major) brain and blood. BMC Genom. 17, 332 (2016).

    Article  Google Scholar 

  41. Baker-Andresen, D., Ratnu, V. S. & Bredy, T. W. Dynamic DNA methylation: a prime candidate for genomic metaplasticity and behavioral adaptation. Trends Neurosci. 36, 3–13 (2013).

    Article  CAS  Google Scholar 

  42. Paoli-Iseppi, D. et al. Measuring animal age with DNA methylation: from humans to wild animals. Front. Genet. 8, 106 (2017).

    Article  Google Scholar 

  43. Ostlund, B. D. et al. Prenatal stress, fearfulness, and the epigenome: exploratory analysis of sex differences in DNA methylation of the glucocorticoid receptor gene. Front. Behav. Neurosci. 10, 147 (2016).

    Article  Google Scholar 

  44. Morales, J. & Velando, A. Signals in family conflicts. Anim. Behav. 86, 11–16 (2013).

    Article  Google Scholar 

  45. Mariette, M. M. et al. Parent-embryo acoustic communication: a specialised heat vocalisation allowing embryonic eavesdropping. Sci. Rep. 8, 17721 (2018).

    Article  Google Scholar 

  46. Lickliter, R. Prenatal sensory ecology and experience: implications for perceptual and behavioral development in precocial birds. Adv. Study Behav. 35, 235–274 (2005).

    Article  Google Scholar 

  47. Gottlieb, G Behavioral Embryology: Studies on the Development of Behavior and the Nervous System Vol. 1 (Academic Press, 2013).

  48. Schwagmeyer, P., Mock, D., Lamey, T., Lamey, C. & Beecher, M. Effects of sibling contact on hatch timing in an asynchronously hatching bird. Anim. Behav. 41, 887–894 (1991).

    Article  Google Scholar 

  49. Müller, G. B. Embryonic motility: environmental influences and evolutionary innovation. Evol. Dev. 5, 56–60 (2003).

    Article  Google Scholar 

  50. Impekoven, M. Responses of laughing gull chicks (Larus atricilla) to parental attraction- and alarm-calls, and effects of prenatal auditory experience on the responsiveness to such calls. Behaviour 56, 250–277 (1976).

    Article  Google Scholar 

  51. Dall, S. R., Giraldeau, L.-A., Olsson, O., McNamara, J. M. & Stephens, D. W. Information and its use by animals in evolutionary ecology. Trends Ecol. Evol. 20, 187–193 (2005).

    Article  Google Scholar 

  52. Ward, A. J. & Mehner, T. Multimodal mixed messages: the use of multiple cues allows greater accuracy in social recognition and predator detection decisions in the mosquitofish, Gambusia holbrooki. Behav. Ecol. 21, 1315–1320 (2010).

    Article  Google Scholar 

  53. Haff, T. M. & Magrath, R. D. Calling at a cost: elevated nestling calling attracts predators to active nests. Biol. Lett. 7, 493–495 (2011).

    Article  Google Scholar 

  54. Caro, T. Antipredator Defenses in Birds and Mammals (Univ. Chicago Press, 2005).

  55. Krause, J. & Ruxton, G. D. Living in Groups (Oxford Univ. Press, 2002).

  56. Schoech, S. J., Rensel, M. A. & Heiss, R. S. Short- and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: a review. Curr. Zool. 57, 514–530 (2011).

    Article  CAS  Google Scholar 

  57. Scanes, C. G. Perspectives on the endocrinology of poultry growth and metabolism. Gen. Comp. Endocrinol. 163, 24–32 (2009).

    Article  CAS  Google Scholar 

  58. Jeng, J. Y. et al. Maintenance of mitochondrial DNA copy number and expression are essential for preservation of mitochondrial function and cell growth. J. Cell. Biochem. 103, 347–357 (2008).

    Article  CAS  Google Scholar 

  59. Velando, A., Noguera, J. C., da Silva, A. & Kim, S.-Y. Redox-regulation and life-history trade-offs: scavenging mitochondrial ROS improves growth in a wild bird. Sci. Rep. 9, 2203 (2019).

    Article  Google Scholar 

  60. Schwagmeyer, P. & Mock, D. W. Parental provisioning and offspring fitness: size matters. Anim. Behav. 75, 291–298 (2008).

    Article  Google Scholar 

  61. Monaghan, P. & Metcalfe, N. On being the right size: natural selection and body size in the herring gull. Evolution 40, 1096–1099 (1986).

    Article  CAS  Google Scholar 

  62. Reiss, M. J. The Allometry of Growth and Reproduction (Cambridge Univ. Press, 1991).

  63. Tong, Q. et al. Effect of species-specific sound stimulation on the development and hatching of broiler chicks. Br. Poult. Sci. 56, 143–148 (2015).

    Article  CAS  Google Scholar 

  64. Noguera, J. C., Lores, M., Alonso‐Álvarez, C. & Velando, A. Thrifty development: early‐life diet restriction reduces oxidative damage during later growth. Funct. Ecol. 25, 1144–1153 (2011).

    Article  Google Scholar 

  65. Noguera, J. C., Morales, J., Perez, C. & Velando, A. On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks. Behav. Ecol. 21, 479–484 (2010).

    Article  Google Scholar 

  66. Boersma, D. C., Ellenton, J. A. & Yagminas, A. Investigation of the hepatic mixed‐function oxidase system in herring gull embryos in relation to environmental contaminants. Environ. Toxicol. Chem. 5, 309–318 (1986).

    Article  CAS  Google Scholar 

  67. Jones, T. A., Jones, S. M. & Paggett, K. C. Emergence of hearing in the chicken embryo. J. Neurophysiol. 96, 128–141 (2006).

    Article  Google Scholar 

  68. Sviderskaya, G. Possible pathways for the effect of vibration on motor activity of chick embryos. Bull. Exp. Biol. Med. 66, 1301–1303 (1968).

    Google Scholar 

  69. Burger, J. & Gochfeld, M. Discrimination of the threat of direct versus tangential approach to the nest by incubating herring and great black-backed gulls. J. Comp. Physiol. Psychol. 95, 676–684 (1981).

    Article  Google Scholar 

  70. Kim, S. Y., Noguera, J., Tato, A. & Velando, A. Vitamins, stress and growth: the availability of antioxidants in early life influences the expression of cryptic genetic variation. J. Evol. Biol. 26, 1341–1352 (2013).

    Article  CAS  Google Scholar 

  71. Romero, L. M. & Reed, J. M. Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp. Biochem. Physiol. A 140, 73–79 (2005).

    Article  Google Scholar 

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

    Article  Google Scholar 

  73. Pike, N. Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol. Evol. 2, 278–282 (2011).

    Article  Google Scholar 

Download references

Acknowledgements

We thank the staff at the Atlantic Islands of Galicia National Park, especially to P. Mallo, R. Castiñeira and J. Arcas; A. da Silva for their help with the laboratory analyses; B. Otero and H. Martinez for their support during the fieldwork; P. Monaghan, N. B. Metcalfe, S.-Y. Kim for their comments on an earlier version of the manuscript. J.C.N. was supported by the Juan de la Cierva Research Program (IJI-2014-20246) and the project was supported by MINECO and MICINN (CGL2015-69338-C2-1-P and PGC2018-095412-B-I00).

Author information

Authors and Affiliations

  1. Departamento de Ecología y Biología Animal, Universidad de Vigo, Vigo, Spain

    Jose C. Noguera & Alberto Velando

Authors
  1. Jose C. Noguera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alberto Velando
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.C.N. and A.V. conceived the study and designed the experiment. J.C.N. collected the field data, performed the laboratory analyses and analysed the data. J.C.N. and A.V. discussed the results and wrote the paper.

Corresponding author

Correspondence to Jose C. Noguera.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figs. 1–5, Supplementary Tables 1–8, Supplementary references

Reporting Summary

Supplementary Video 1

An example of experimental eggs vibrating inside the incubator

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Noguera, J.C., Velando, A. Bird embryos perceive vibratory cues of predation risk from clutch mates. Nat Ecol Evol 3, 1225–1232 (2019). https://doi.org/10.1038/s41559-019-0929-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-0929-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing