Inter-signal interaction and uncertain information in anuran multimodal signals

Disentangling the influence of multiple signal components on receivers and elucidating general processes influencing complex signal evolution are difficult tasks. In this study we test mate preferences of female squirrel treefrogs Hyla squirella and female tungara frogs Physalaemus pustulosus for similar combinations of acoustic and visual components of their multimodal courtship signals. In a two-choice playback experiment with squirrel treefrogs, the visual stimulus of a male model significantly increased the attractivness of a relatively unattractive slow call rate. A previous study demonstrated that faster call rates are more attractive to female squirrel treefrogs, and all else being equal, models of male frogs with large body stripes are more attractive. In a similar experiment with female tungara frogs, the visual stimulus of a robotic frog failed to increase the attractiveness of a rela- tively unattractive call. Females also showed no preference for the distinct stripe on the robot that males commonly bear on their throat. Thus, features of conspicuous signal components such as body stripes are not universally important and signal function is likely to differ even among species with similar ecologies and communication systems. Finally, we discuss the putative informa- tion content of anuran signals and suggest that the categorization of redundant versus multiple messages may not be sufficient as a general explanation for the evolution of multimodal signaling. Instead of relying on untested assumptions concerning the infor- mation content of signals, we discuss the value of initially collecting comparative empirical data sets related to receiver responses (Current Zoology 57 (2): 153-161, 2011).

[1]  M. Ryan,et al.  Female and male behavioral response to advertisement calls of graded complexity in túngara frogs, Physalaemus pustulosus , 2009, Behavioral Ecology and Sociobiology.

[2]  Michael J. Ryan,et al.  The effects of time, space and spectrum on auditory grouping in túngara frogs , 2005, Journal of Comparative Physiology A.

[3]  Joshua J. Schwartz Male calling behavior, female discrimination and acoustic interference in the Neotropical treefrog Hyla microcephala under realistic acoustic conditions , 2004, Behavioral Ecology and Sociobiology.

[4]  Visual Signaling in Anuran Amphibians , 2004 .

[5]  R. D. Semlitsch,et al.  Call duration as an indicator of genetic quality in male gray tree frogs. , 1998, Science.

[6]  D. Papaj,et al.  Complex signal function: developing a framework of testable hypotheses , 2004, Behavioral Ecology and Sociobiology.

[7]  Ryan C. Taylor,et al.  Faux frogs: multimodal signalling and the value of robotics in animal behaviour , 2008, Animal Behaviour.

[8]  M. Ryan,et al.  Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to túngara frog calls , 2006 .

[9]  E. Hebets Attention-altering Signal Interactions in the Multimodal Courtship Display of the Wolf Spider Schizocosa Uetzi , 2004 .

[10]  E. Hebets Seismic signal dominance in the multimodal courtship display of the wolf spider Schizocosa stridulans Stratton 1991. , 2008, Behavioral ecology : official journal of the International Society for Behavioral Ecology.

[11]  E. C. Cherry Some Experiments on the Recognition of Speech, with One and with Two Ears , 1953 .

[12]  Sasha R. X. Dall,et al.  Information and its use by animals in evolutionary ecology. , 2005, Trends in ecology & evolution.

[13]  P. Marler,et al.  Communication Goes Multimodal , 1999, Science.

[14]  K. Pfennig,et al.  Looking on the bright side: females prefer coloration indicative of male size and condition in the sexually dichromatic spadefoot toad, Scaphiopus couchii , 2007, Behavioral Ecology and Sociobiology.

[15]  M. Ryan,et al.  The Effects of Spatially Separated Call Components on Phonotaxis in Túngara Frogs: Evidence for Auditory Grouping , 2002, Brain, Behavior and Evolution.

[16]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[17]  M. Ryan,et al.  Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females , 2008, Journal of Experimental Biology.

[18]  W. Hödl,et al.  Colour, size and movement as visual subcomponents in multimodal communication by the frog Allobates femoralis , 2010, Animal Behaviour.

[19]  M. Théry,et al.  Hearing is not necessarily believing in nocturnal anurans , 2010, Biology Letters.

[20]  Ryan C. Taylor,et al.  Sexual selection in the squirrel treefrog Hyla squirella: the role of multimodal cue assessment in female choice , 2007, Animal Behaviour.

[21]  V. Framenau,et al.  A REVIEW OF LEG ORNAMENTATION IN MALE WOLF SPIDERS, WITH THE DESCRIPTION OF A NEW SPECIES FROM AUSTRALIA, ARTORIA SCHIZOCOIDES (ARANEAE, LYCOSIDAE) , 2007 .

[22]  A. Baierl,et al.  Chin up: are the bright throats of male common frogs a condition-independent visual cue? , 2010, Animal Behaviour.

[23]  D. H. Owings,et al.  Ground squirrels use an infrared signal to deter rattlesnake predation , 2007, Proceedings of the National Academy of Sciences.

[24]  M. Ryan,et al.  Oxygen Consumption during Resting, Calling, and Nest Building in the Frog Physalaemus Pustulosus , 1982, Physiological Zoology.

[25]  N. Tinbergen,et al.  The Study of Instinct , 1953 .

[26]  M. Ryan The Tungara Frog: A Study in Sexual Selection and Communication , 1986 .

[27]  P. Narins,et al.  Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Rufus A. Johnstone,et al.  Multiple Displays in Animal Communication:`Backup Signals' and `Multiple Messages' , 1996 .

[29]  M. Ryan,et al.  Animal communication: Complex call production in the túngara frog , 2006, Nature.

[30]  T. Hetherington,et al.  Field Studies on Visual and Acoustic Signaling in the "Earless" Panamanian Golden Frog, Atelopus zeteki , 1996 .

[31]  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.

[32]  Sarah R Partan,et al.  Issues in the Classification of Multimodal Communication Signals , 2005, The American Naturalist.

[33]  D. Blumstein Acoustic Communication in Insects and Anurans : Common Problems and Diverse Solutions , 2002 .

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

[35]  W. H. Sumby,et al.  Visual contribution to speech intelligibility in noise , 1954 .

[36]  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.

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

[38]  M. Cummings SENSORY TRADE-OFFS PREDICT SIGNAL DIVERGENCE IN SURFPERCH , 2007, Evolution; international journal of organic evolution.

[39]  William Rowan,et al.  The Study of Instinct , 1953 .

[40]  K. Summers,et al.  Visual mate choice in poison frogs , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  Amots Zehavi,et al.  The Handicap Principle: A Missing Piece of Darwin's Puzzle , 1997 .

[42]  W. Hödl,et al.  VISUAL SIGNALING IN PHRYNOBATRACHUS KREFFTII BOULENGER, 1909 (ANURA: RANIDAE) , 2006 .

[43]  F. Trillmich,et al.  The mating systems of pinnipeds and marine iguanas : convergent evolution of polygyny , 1984 .

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

[45]  M. Wiener,et al.  Animal eyes. , 1957, The American orthoptic journal.

[46]  C. Rowe Receiver psychology and the evolution of multicomponent signals , 1999, Animal Behaviour.

[47]  H. Brockmann,et al.  The Evolution of Animal Communication: Reliability and Deception in Signaling Systems , 2006 .

[48]  Francis L. W. Ratnieks,et al.  Convergent evolution of worker policing by egg eating in the honeybee and common wasp , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  Ryan C. Taylor,et al.  Multimodal signal variation in space and time: how important is matching a signal with its signaler? , 2011, Journal of Experimental Biology.

[50]  Timothy F. Wright,et al.  The Evolution of Animal Communication: Reliability and Deception in Signaling Systems , 2006 .

[51]  W. Hödl,et al.  HOW, WHEN, AND WHERE TO PERFORM VISUAL DISPLAYS: THE CASE OF THE AMAZONIAN FROG HYLA PARVICEPS , 2004 .

[52]  Christopher G. Murphy ANURAN COMMUNICATION , 2002, Copeia.

[53]  M. Ryan,et al.  The Vocal Sac Increases Call Rate in the Túngara Frog Physalaemus pustulosus , 2006, Physiological and Biochemical Zoology.

[54]  M. Ryan,et al.  The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback , 2004, Animal Behaviour.

[55]  R R Hoy,et al.  The evolutionary convergence of hearing in a parasitoid fly and its cricket host. , 1992, Science.

[56]  G. Uetz,et al.  Leg ornamentation and the efficacy of courtship display in four species of wolf spider (Araneae: Lycosidae) , 2000, Behavioral Ecology and Sociobiology.

[57]  H. McGurk,et al.  Hearing lips and seeing voices , 1976, Nature.

[58]  M. Morris,et al.  Defining Vertical Bars in Relation to Female Preference in the Swordtail Fish Xiphophorus cortezi (Cyprinodontiformes, Poeciliidae) , 2001 .