Wild Birds Learn to Eavesdrop on Heterospecific Alarm Calls

Many vertebrates gain critical information about danger by eavesdropping on other species' alarm calls [1], providing an excellent context in which to study information flow among species in animal communities [2-4]. A fundamental but unresolved question is how individuals recognize other species' alarm calls. Although individuals respond to heterospecific calls that are acoustically similar to their own, alarms vary greatly among species, and eavesdropping probably also requires learning [1]. Surprisingly, however, we lack studies demonstrating such learning. Here, we show experimentally that individual wild superb fairy-wrens, Malurus cyaneus, can learn to recognize previously unfamiliar alarm calls. We trained individuals by broadcasting unfamiliar sounds while simultaneously presenting gliding predatory birds. Fairy-wrens in the experiment originally ignored these sounds, but most fled in response to the sounds after two days' training. The learned response was not due to increased responsiveness in general or to sensitization following repeated exposure and was independent of sound structure. Learning can therefore help explain the taxonomic diversity of eavesdropping and the refining of behavior to suit the local community. In combination with previous work on unfamiliar predator recognition (e.g., [5]), our results imply rapid spread of anti-predator behavior within wild populations and suggest methods for training captive-bred animals before release into the wild [6]. A remaining challenge is to assess the importance and consequences of direct association of unfamiliar sounds with predators, compared with social learning-such as associating unfamiliar sounds with conspecific alarms.

[1]  R. Holt THE UNRAVELING OF NATURE'S INFORMATION WEBS: THE NExT dEpRESSING FRONTIER IN cONSERVATION? , 2007 .

[2]  R. A. Garcia,et al.  Multiple Dimensions of Climate Change and Their Implications for Biodiversity , 2014, Science.

[3]  F. J. Sulloway,et al.  Extended parental care of fledglings: parent birds adjust anti-predator response according to predator type and distance , 2010 .

[4]  Robert D. Magrath,et al.  Communicating about danger: urgency alarm calling in a bird , 2005, Animal Behaviour.

[5]  N. Davies,et al.  A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species , 2006, Proceedings of the Royal Society B: Biological Sciences.

[6]  P. Racey,et al.  Interspecific responses to distress calls in bats (Chiroptera: Vespertilionidae): a function for convergence in call design? , 2004, Animal Behaviour.

[7]  David Wheatcroft,et al.  Learning and signal copying facilitate communication among bird species , 2013, Proceedings of the Royal Society B: Biological Sciences.

[8]  Paul A. Carlile,et al.  Detection of a looming stimulus by the Jacky dragon: selective sensitivity to characteristics of an aerial predator , 2006, Animal Behaviour.

[9]  Donald H. Owings,et al.  The effects of wind turbines on antipredator behavior in California ground squirrels (Spermophilus beecheyi) , 2006 .

[10]  Erich Seifritz,et al.  Looming sounds as warning signals: the function of motion cues. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  Graeme D Ruxton,et al.  Interspecific information transfer influences animal community structure. , 2010, Trends in ecology & evolution.

[12]  Benjamin J. Pitcher,et al.  A mutual understanding? Interspecific responses by birds to each other's aerial alarm calls , 2007 .

[13]  A. Radford,et al.  The value of constant surveillance in a risky environment , 2009, Proceedings of the Royal Society B: Biological Sciences.

[14]  Antoine Guisan,et al.  Unifying niche shift studies: insights from biological invasions. , 2014, Trends in ecology & evolution.

[15]  D. Prawiradilaga Foraging ecology of pied currawongs Strepera graculina in recently colonised areas of their range , 1996 .

[16]  U. Ramakrishnan,et al.  Recognition of heterospecific alarm vocalizations by bonnet macaques (Macaca radiata). , 2000, Journal of comparative psychology.

[17]  K. Kotrschal John Dittami (1949–2014) , 2015 .

[18]  Current Biology , 2012, Current Biology.

[19]  W. Shriner Antipredator Responses to a Previously Neutral Sound by Free-living Adult Golden-mantled Ground Squirrels, Spermophilus lateralis (Sciuridae) , 1999 .

[20]  Andrew N. Radford,et al.  The development of alarm call behaviour in mammals and birds , 2009, Animal Behaviour.

[21]  D. Moore,et al.  Auditory Neuroscience: The Salience of Looming Sounds , 2003, Current Biology.

[22]  Jacqueline L. Frair,et al.  Know Thy Enemy: Experience Affects Elk Translocation Success in Risky Landscapes , 2007 .

[23]  J. Gardner,et al.  Sound familiar? Acoustic similarity provokes responses to unfamiliar heterospecific alarm calls , 2011 .

[24]  R. Mulder,et al.  Can we measure the benefits of help in cooperatively breeding birds: the case of superb fairy-wrens Malurus cyaneus? , 2008, The Journal of animal ecology.

[25]  A. S. Griffin,et al.  Social learning about predators: a review and prospectus , 2004, Learning & behavior.

[26]  Mikko Mönkkönen,et al.  Social information use is a process across time, space, and ecology, reaching heterospecifics. , 2007, Ecology.

[27]  R. Holt IJEE Soapbox: The Unraveling of Nature's Information Webs: The Next Depresing Frontier in Conservation? , 2007 .

[28]  A possible phylogenetically conserved urgency response of great tits (Parus major) towards allopatric mobbing calls , 2012, Behavioral Ecology and Sociobiology.

[29]  M. Considine,et al.  Handbook of Australian, New Zealand and Antarctic birds. Volume 2: raptors to lapwings , 2007 .

[30]  Robert D. Magrath,et al.  Eavesdropping on other species: mutual interspecific understanding of urgency information in avian alarm calls , 2010, Animal Behaviour.

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

[32]  B. Pitcher,et al.  Alarming features: birds use specific acoustic properties to identify heterospecific alarm calls , 2013, Proceedings of the Royal Society B: Biological Sciences.

[33]  R. D. Magrath,et al.  Eavesdropping on the neighbours: fledglings learn to respond to heterospecific alarm calls , 2013, Animal Behaviour.

[34]  A. Radford,et al.  Eavesdropping on heterospecific alarm calls: from mechanisms to consequences , 2015, Biological reviews of the Cambridge Philosophical Society.

[35]  K. Laland,et al.  Social Learning: An Introduction to Mechanisms, Methods, and Models , 2013 .

[36]  Robert D Magrath,et al.  A micro-geography of fear: learning to eavesdrop on alarm calls of neighbouring heterospecifics , 2012, Proceedings of the Royal Society B: Biological Sciences.

[37]  P. J. Higgins,et al.  Handbook of Australian, New Zealand and Antarctic birds. Volume 5: trant-Flycatchers to chats , 2001 .

[38]  Junko Kondo,et al.  From nestling calls to fledgling silence: adaptive timing of change in response to aerial alarm calls , 2006, Proceedings of the Royal Society B: Biological Sciences.

[39]  Sasha R. X. Dall,et al.  The ecology of information: an overview on the ecological significance of making informed decisions , 2010 .

[40]  R. D. Magrath,et al.  Calling at a cost: elevated nestling calling attracts predators to active nests , 2011, Biology Letters.

[41]  U. Ernst,et al.  Cultural Transmission of Enemy Recognition: One Function of Mobbing , 1978, Science.

[42]  Torben Dabelsteen,et al.  Animal Communication Networks: Public, private or anonymous? Facilitating and countering eavesdropping , 2005 .

[43]  Breaking down the Species Boundaries: Selective Pressures behind Interspecific Communication in Vertebrates , 2015 .

[44]  Robert D Magrath,et al.  Recognition of other species' aerial alarm calls: speaking the same language or learning another? , 2009, Proceedings of the Royal Society B: Biological Sciences.

[45]  Daniel T. Blumstein,et al.  Training Captive‐Bred or Translocated Animals to Avoid Predators , 2000 .

[46]  Klaus Zuberbühler,et al.  Causal knowledge of predators' behaviour in wild Diana monkeys , 2000, Animal Behaviour.

[47]  D. Blumstein,et al.  Mechanisms of heterospecific recognition in avian mobbing calls , 2003 .

[48]  T. Riede,et al.  Fundamental frequency is key to response of female deer to juvenile distress calls , 2013, Behavioural Processes.

[49]  Francesc Salvador Beltran,et al.  Social Learning: An Introduction to Mechanisms, Methods, and Models by William Hoppitt and Kevin N. Laland , 2014, J. Artif. Soc. Soc. Simul..

[50]  Benjamin J. Pitcher,et al.  An avian eavesdropping network: alarm signal reliability and heterospecific response , 2009 .

[51]  S. Shettleworth Cognition, evolution, and behavior , 1998 .

[52]  Doug P Armstrong,et al.  Developing the Science of Reintroduction Biology , 2007, Conservation biology : the journal of the Society for Conservation Biology.