Hissing like a snake: bird hisses are similar to snake hisses and prompt similar anxiety behavior in a mammalian model

A Correction to this article was published on 16 January 2020

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Abstract

Batesian mimicry refers to a harmless species protecting itself from predators by mimicking a harmful species. A case of acoustic Batesian mimicry has been proposed in the naturalist literature: it is suspected that birds called like a snake when disturbed in their cavities to deter mammalian predators or repel competitors. To evaluate this hypothesis, we first test the assumption that the hissing sound produced by adult females of a wild cavity-nesting species – the blue tit (Cyanistes caeruleus) – is acoustically similar to the hisses of three wild sympatric snake species. Then, we tested one prediction of this hypothesis which is that the receiver of the signal should react similarly to the snake and bird hisses. To do so, we used, hiss-naïve individuals, without any past experience with predators: the house mouse (Mus musculus domesticus), representing a model of a possible nest competitor. We quantified mouse responses to blue tit and snake hisses and two non-hiss sounds (other blue tit vocalizations and human voices). Our results show that snake hisses and blue tit hisses are structurally more similar to each other than to other blue tit vocalizations and that both hisses provoke comparable levels of anxiety behavior in mice. Taken together, these results are compatible with the hypothesis that blue tits have evolved to mimic the sound of snakes, i.e., the Batesian mimicry hypothesis. We also note however that our results also agree with another hypothesis, suggesting that mechanisms underlying the production and perception of hisses are conserved across vertebrates. Further research is needed to disentangle these two hypotheses.

Significance statement

Mimicry is a fascinating illustration of the principles of evolution in communication. In the case of Batesian mimicry, species evolve to resemble other species as a mean of deterring harmful receivers. While visual mimicry has been thoroughly investigated across a wide range of species, vocal mimicry remains less studied. In the present study, we compared the acoustic similarity of the hissing sound produced by female blue tits, a cavity-nesting species, to the hisses of three snake species. Then, we exposed mice, a model of a possible cavity competitor, to bird and snake hisses. We showed that snake and blue tit hisses are acoustically similar and provoke comparable anxiety behaviors in mice. These results are compatible with the hypothesis that blue tits utilize an innate fear response to hisses in mammals, a result that may explain why blue tit hisses have been linked to increased survival by other authors. Furthermore, the results also suggest a conserved function of, and response to, hiss vocalizations across vertebrates.

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  • 16 January 2020

    After publication of this paper, the authors determined an error in the article title.

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Acknowledgments

The recordings of snake hisses were obtained thanks to Anthony Olivier, Marc Thibault, Aurélien Guay from Regard du vivant, and Cornélius De Haan. We thank Aurélie Célérier for helping in behavioral experiment. We thank Leen Gorissen for the recordings of non-hissing vocalizations by females and Jessica Pearce and Sarah Walsh for English language editing. We thank the editor and reviewers for constructive comments on an earlier version of this manuscript.

Funding

This work was supported by a French ANR (ANR-09-JCJC-0050-01) and by funds from OSU-OREME.

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Correspondence to Mylène Dutour.

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All study protocols involving mice were approved authorization certificate for animal experimentation (A34–402) from the Direction Départementale de la Protection des Populations de l’Hérault to Aurélie Célérier, University of Montpellier – CECEMA. Regarding bleu tit acoustic productions, even if noninvasive (no necessity to handle individuals), the data were collected under permits given by the Hérault local government office and the Regional Direction of Environment (DREAL) committee to our research program (permit 2006-01-2014), to our research institute (permit B34–172-204 11), and to ourselves (permit 3467). Regarding the snake acoustic productions, even if noninvasive, the sounds were collected with specialists on two field sites where research programs including Capture Mark Recapture on snakes are conducted, under the permit given by the Hérault local government office and the DREAL committee (number: 2015-12-17-01415) for the Mejean reserve and with the reserve ranger for the Tour du Valat Nature Reserve.

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Claire Doutrelant and Arnaud Grégoire are Joint last authors.

The original version of this article was revised: This article was published with an incorrect article title introduced by production.

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Dutour, M., Lévy, L., Lengagne, T. et al. Hissing like a snake: bird hisses are similar to snake hisses and prompt similar anxiety behavior in a mammalian model. Behav Ecol Sociobiol 74, 1 (2020). https://doi.org/10.1007/s00265-019-2778-5

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Keywords

  • Antipredator strategy
  • Blue tit
  • Hissing call
  • Mimicry
  • Nest defense