Dip listening and the cocktail party problem in grey treefrogs: signal recognition in temporally fluctuating noise

Dip listening refers to our ability to catch brief "acoustic glimpses" of speech and other sounds when fluctuating background noise levels momentarily decrease. Exploiting dips in natural fluctuations of noise contributes to our ability to overcome the "cocktail party problem" of understanding speech in multi-talker social environments. We presently know little about how nonhuman animals solve analogous communication problems. Here, we asked whether female grey treefrogs (Hyla chrysoscelis) might benefit from dip listening in selecting a mate in the noisy social setting of a breeding chorus. Consistent with a dip listening hypothesis, subjects recognized conspecific calls at lower thresholds when the dips in a chorus-like noise masker were long enough to allow glimpses of nine or more consecutive pulses. No benefits of dip listening were observed when dips were shorter and included five or fewer pulses. Recognition thresholds were higher when the noise fluctuated at a rate similar to the pulse rate of the call. In a second experiment, advertisement calls comprising six to nine pulses were necessary to elicit responses under quiet conditions. Together, these results suggest that in frogs, the benefits of dip listening are constrained by neural mechanisms underlying temporal pattern recognition. These constraints have important implications for the evolution of male signalling strategies in noisy social environments.

[1]  B. Ronacher,et al.  Influence of amplitude modulated noise on the recognition of communication signals in the grasshopper Chorthippus biguttulus , 2003, Journal of Comparative Physiology A.

[2]  Mark A. Bee,et al.  Do female frogs exploit inadvertent social information to locate breeding aggregations , 2007 .

[3]  C E Schreiner,et al.  Neural processing of amplitude-modulated sounds. , 2004, Physiological reviews.

[4]  Franz Huber,et al.  Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions , 2002 .

[5]  Ruth Y Litovsky,et al.  The benefit of binaural hearing in a cocktail party: effect of location and type of interferer. , 2004, The Journal of the Acoustical Society of America.

[6]  Josh H. McDermott The cocktail party problem , 2009, Current Biology.

[7]  H. Gerhardt,et al.  Effects of heterospecific call overlap on the phonotactic behaviour of grey treefrogs , 2006, Animal Behaviour.

[8]  R. H. Wiley,et al.  Reverberations and Amplitude Fluctuations in the Propagation of Sound in a Forest: Implications for Animal Communication , 1980, The American Naturalist.

[9]  H. Carl Gerhardt,et al.  Phonotaxis in Female Frogs and Toads: Execution and Design of Experiments , 1995 .

[10]  Thierry Aubin,et al.  Cocktail–party effect in king penguin colonies , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  Mark A. Bee,et al.  An experimental test of noise-dependent voice amplitude regulation in Cope’s grey treefrog, Hyla chrysoscelis , 2010, Animal Behaviour.

[12]  H. Carl Gerhardt,et al.  Spatially mediated release from auditory masking in an anuran amphibian , 1989, Journal of Comparative Physiology A.

[13]  Gary J. Rose,et al.  Long-term temporal integration in the anuran auditory system , 1998, Nature Neuroscience.

[14]  M. A. Bee,et al.  Sound source segregation in grey treefrogs: spatial release from masking by the sound of a chorus , 2007, Animal Behaviour.

[15]  J. Schwartz,et al.  FORMS OF CALL OVERLAP AND THEIR IMPACT ON ADVERTISEMENT CALL ATTRACTIVENESS TO FEMALES OF THE GRAY TREEFROG, HYLA VERSICOLOR , 2006 .

[16]  H. Gerhardt,et al.  Acoustic interactions among male gray treefrogs, Hyla versicolor, in a chorus setting , 2002, Behavioral Ecology and Sociobiology.

[17]  D. Grantham,et al.  Modulation masking: effects of modulation frequency, depth, and phase. , 1989, The Journal of the Acoustical Society of America.

[18]  Mark A Bee,et al.  Behavioral measures of signal recognition thresholds in frogs in the presence and absence of chorus-shaped noise. , 2009, The Journal of the Acoustical Society of America.

[19]  H. Gustafsson,et al.  Masking of speech by amplitude-modulated noise. , 1994, The Journal of the Acoustical Society of America.

[20]  LORI WOLLERMAN,et al.  Acoustic interference limits call detection in a Neotropical frogHyla ebraccata , 1999, Animal Behaviour.

[21]  H. Brumm,et al.  Acoustic Communication in Noise , 2005 .

[22]  Martin Cooke,et al.  A glimpsing model of speech perception in noise. , 2006, The Journal of the Acoustical Society of America.

[23]  Georg M. Klump,et al.  Phonotactic responses and selectivity of barking treefrogs (Hyla gratiosa) to chorus sounds , 1988, Journal of Comparative Physiology A.

[24]  H. Carl Gerhardt,et al.  Sound pressure levels and radiation patterns of the vocalizations of some North American frogs and toads , 1975, Journal of comparative physiology.

[25]  B J Kwon,et al.  Consonant identification under maskers with sinusoidal modulation: masking release or modulation interference? , 2001, The Journal of the Acoustical Society of America.

[26]  H. Carl Gerhardt,et al.  Female preference functions based on call duration in the gray tree frog (Hyla versicolor) , 2000 .

[27]  Johannes Schul,et al.  Phonotaxis to male’s calls embedded within a chorus by female gray treefrogs, Hyla versicolor , 2010, Journal of Comparative Physiology A.

[28]  G. Rose,et al.  Auditory midbrain neurons that count , 2002, Nature Neuroscience.

[29]  T. Lengagne,et al.  Multiple signals and male spacing affect female preference at cocktail parties in treefrogs , 2010, Proceedings of the Royal Society B: Biological Sciences.

[30]  S. Bacon,et al.  The effects of hearing loss and noise masking on the masking release for speech in temporally complex backgrounds. , 1998, Journal of speech, language, and hearing research : JSLHR.

[31]  G. Fellers Aggression, territoriality, and mating behaviour in North American treefrogs , 1979, Animal Behaviour.

[32]  Alejandro Vélez,et al.  Signal recognition by frogs in the presence of temporally fluctuating chorus-shaped noise , 2010, Behavioral Ecology and Sociobiology.

[33]  Brandon Lentine,et al.  Effect of anomalous pulse timing on call discrimination by females of the gray treefrog (Hyla versicolor): behavioral correlates of neurobiology , 2010, Journal of Experimental Biology.

[34]  Mark A. Bee,et al.  Parallel female preferences for call duration in a diploid ancestor of an allotetraploid treefrog , 2008, Animal Behaviour.

[35]  P. K. McGregor,et al.  Animal Communication Networks: Behaviours specific to communication networks , 2005 .

[36]  Stewart H. Hulse,et al.  Auditory scene analysis in animal communication , 2002 .

[37]  J. Schwartz,et al.  Interference risk and the function of dynamic shifts in calling in the gray treefrog (Hyla versicolor). , 2008, Journal of comparative psychology.

[38]  Johannes Schul,et al.  Pattern recognition and call preferences in treefrogs (Anura: Hylidae): a quantitative analysis using a no-choice paradigm , 2002, Animal Behaviour.

[39]  Israel Nelken,et al.  Responses of auditory-cortex neurons to structural features of natural sounds , 1999, Nature.

[40]  Georg M. Klump,et al.  Methods in Comparative Psychoacoustics , 1995, BioMethods.

[41]  Ulrike Langemann,et al.  Animal Communication Networks: Perception and acoustic communication networks , 2005 .

[42]  Roy D Patterson,et al.  The mutual roles of temporal glimpsing and vocal characteristics in cocktail-party listening. , 2011, The Journal of the Acoustical Society of America.

[43]  Georg M. Klump,et al.  Masking of acoustic signals by the chorus background noise in the green tree frog: A limitation on mate choice , 1988, Animal Behaviour.

[44]  H. Carl Gerhardt,et al.  Female mate choice in the gray treefrog (Hyla versicolor) in three experimental environments , 2001, Behavioral Ecology and Sociobiology.

[45]  Mark A. Bee,et al.  Finding a mate at a cocktail party: spatial release from masking improves acoustic mate recognition in grey treefrogs , 2008, Animal Behaviour.

[46]  D. Kroodsma,et al.  Ecology and evolution of acoustic communication in birds , 1997 .

[47]  Mark A. Bee,et al.  Selective phonotaxis by male wood frogs (Rana sylvatica) to the sound of a chorus , 2007, Behavioral Ecology and Sociobiology.

[48]  M. A. Bee,et al.  The cocktail party problem: what is it? How can it be solved? And why should animal behaviorists study it? , 2008, Journal of comparative psychology.

[49]  Anthony Arak,et al.  Sexual selection by male–male competition in natterjack toad choruses , 1983, Nature.

[50]  Todd M Freeberg,et al.  Acoustic interaction in animal groups: signaling in noisy and social contexts. , 2008, Journal of comparative psychology.

[51]  J. Schul,et al.  Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[52]  R. Haven Wiley,et al.  Background noise from a natural chorus alters female discrimination of male calls in a Neotropical frog , 2002, Animal Behaviour.

[53]  Mark A. Bee,et al.  Spatial release from masking in a free-field source identification task by gray treefrogs , 2012, Hearing Research.