Alarm calls evoke a visual search image of a predator in birds

Significance In human speech, words often cause listeners to retrieve visual mental images of target objects. In nonhuman animal communication systems, many key, language-like features have been demonstrated, but there is still no evidence that animal signals evoke mental images of objects in receivers. Japanese tits produce specific alarm calls when encountering a predatory snake. Here, I show that simply hearing these calls causes tits to become more visually perceptive to objects resembling snakes (moving sticks). This result indicates that before having detected a real snake, tits retrieve its visual image from snake-specific alarm calls and uses this to search out snakes. This study provides evidence for a call-evoked visual search image in a nonhuman animal. One of the core features of human speech is that words cause listeners to retrieve corresponding visual mental images. However, whether vocalizations similarly evoke mental images in animal communication systems is surprisingly unknown. Japanese tits (Parus minor) produce specific alarm calls when and only when encountering a predatory snake. Here, I show that simply hearing these calls causes tits to become more visually perceptive to objects resembling snakes. During playback of snake-specific alarm calls, tits approach a wooden stick being moved in a snake-like fashion. However, tits do not respond to the same stick when hearing other call types or if the stick’s movement is dissimilar to that of a snake. Thus, before detecting a real snake, tits retrieve its visual image from snake-specific alarm calls and use this to search out snakes. This study provides evidence for a call-evoked visual search image in a nonhuman animal, offering a paradigm to explore the cognitive basis for animal vocal communication in the wild.

[1]  Gary Lupyan,et al.  Language can boost otherwise unseen objects into visual awareness , 2013, Proceedings of the National Academy of Sciences.

[2]  Andrea M.-K. Bierema,et al.  On the Meaning of Alarm Calls: A Review of Functional Reference in Avian Alarm Calling , 2013 .

[3]  Brandon C. Wheeler,et al.  Functionally referential signals: A promising paradigm whose time has passed , 2012, Evolutionary anthropology.

[4]  Toshitaka N. Suzuki,et al.  Mobbing Calls of Japanese Tits Signal Predator Type: Field Observations of Natural Predator Encounters , 2013 .

[5]  L. Sneddon,et al.  Guidelines for the treatment of animals in behavioural research and teaching , 2012, Animal Behaviour.

[6]  Robert M. Seyfarth,et al.  Conceptual Semantics in a Nonhuman Primate , 1999 .

[7]  The Origins of Meaning: Language in the Light of Evolution , 2009 .

[8]  S. Kosslyn,et al.  Mental Imagery: Functional Mechanisms and Clinical Applications , 2015, Trends in Cognitive Sciences.

[9]  Floris P de Lange,et al.  Prior expectations induce prestimulus sensory templates , 2017, Proceedings of the National Academy of Sciences.

[10]  Robert Rosenthal,et al.  Can you believe my eyes? The importance of interobserver reliability statistics in observations of animal behaviour , 2009, Animal Behaviour.

[11]  Klaus Zuberbühler,et al.  Causal cognition in a non-human primate: field playback experiments with Diana monkeys , 2000, Cognition.

[12]  N. Logothetis,et al.  Neuroperception: Facial expressions linked to monkey calls , 2003, Nature.

[13]  M. Ryan,et al.  What do animal signals mean? , 2009, Animal Behaviour.

[14]  M. Hausberger,et al.  No need to Talk, I Know You: Familiarity Influences Early Multisensory Integration in a Songbird's Brain , 2011, Front. Behav. Neurosci..

[15]  C. Koch,et al.  Imagery neurons in the human brain , 2000, Nature.

[16]  Noam Chomsky,et al.  The faculty of language: what is it, who has it, and how did it evolve? , 2002, Science.

[17]  Toshitaka N. Suzuki Parental alarm calls warn nestlings about different predatory threats , 2011, Current Biology.

[18]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[19]  Felipe De Brigard,et al.  The Origins of Meaning: Language in the Light of Evolution , 2009 .

[20]  Toshitaka N. Suzuki Referential mobbing calls elicit different predator-searching behaviours in Japanese great tits , 2012, Animal Behaviour.

[21]  Toshitaka N. Suzuki Long-Distance Calling by the Willow Tit, Poecile montanus, Facilitates Formation of Mixed-Species Foraging Flocks , 2012 .

[22]  R. Seyfarth,et al.  The assessment by vervet monkeys of their own and another species' alarm calls , 1990, Animal Behaviour.

[23]  O. Pascalis,et al.  Spontaneous voice–face identity matching by rhesus monkeys for familiar conspecifics and humans , 2011, Proceedings of the National Academy of Sciences.

[24]  Toshitaka N. Suzuki Assessment of predation risk through referential communication in incubating birds , 2015, Scientific Reports.

[25]  Donald E. Kroodsma,et al.  Pseudoreplication in playback experiments, revisited a decade later , 2001, Animal Behaviour.

[26]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[27]  Toshitaka N. Suzuki Communication about predator type by a bird using discrete, graded and combinatorial variation in alarm calls , 2014, Animal Behaviour.

[28]  Toshitaka N. Suzuki Semantic communication in birds: evidence from field research over the past two decades , 2016, Ecological Research.

[29]  Toshitaka N Suzuki,et al.  Experimental evidence for compositional syntax in bird calls , 2016, Nature Communications.

[30]  David Reby,et al.  Cross-modal individual recognition in domestic horses (Equus caballus) , 2009, Proceedings of the National Academy of Sciences.

[31]  Shigeru Watanabe,et al.  Crows cross-modally recognize group members but not non-group members , 2012, Proceedings of the Royal Society B: Biological Sciences.

[32]  Individual recognition through olfactory–auditory matching in lemurs , 2014, Proceedings of the Royal Society B: Biological Sciences.

[33]  Linda Evans,et al.  Representational signalling in birds , 2007, Biology Letters.

[34]  K. Zuberbühler Referential Signaling in Non-Human Primates: Cognitive Precursors and Limitations for the Evolution of Language , 2003 .

[35]  Cheng Li,et al.  Adjusting batch effects in microarray expression data using empirical Bayes methods. , 2007, Biostatistics.

[36]  W. Fitch The Evolution of Language , 2010 .