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

Behavioral Ecology and Sociobiology(2019)

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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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Key words
Antipredator strategy,Blue tit,Hissing call,Mimicry,Nest defense
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