Behavioral Ecology and Sociobiology

, Volume 69, Issue 8, pp 1353–1364 | Cite as

Perceptual bias does not explain preference for prey call adornment in the frog-eating bat

  • Vincent Fugère
  • M. Teague O’Mara
  • Rachel A. Page
Original Paper


Eavesdropping predators sometimes show preferences for certain prey signal variants, yet the ultimate and proximate reasons for such preferences are often unclear. The fringe-lipped bat, Trachops cirrhosus, eavesdrops on the advertisement calls of male túngara frogs, Physalaemus pustulosus, and shows a marked preference for complex (adorned) calls over simple (non-adorned) calls. We hypothesized that this preference stems from perceptual biases in the sensory and/or cognitive systems of T. cirrhosus. To test this hypothesis, we conducted a series of preference experiments in which we presented bats with various modified simple calls, each altered to possess one of the acoustic properties that distinguish complex calls from simple calls. We reasoned that if perceptual bias accounts for the bat’s preference for complex calls, then a novel stimulus with similar acoustic properties to the complex call should be attractive as well (i.e., the preference should be permissive). Except for weak evidence suggesting that the longer duration of complex calls could contribute to their greater attractiveness to T. cirrhosus, we did not find any indication that perceptual biases account for this eavesdropper preference. Instead, we suggest that T. cirrhosus developed their preference for call complexity because eavesdropping on complex calls provides greater fitness benefits than eavesdropping on simple calls, for example, because eavesdropping on complex calls may increase probability of prey capture and/or lead to more profitable food patches.


Eavesdropping Perceptual bias Receiver bias Prey detection Predator-prey interaction Fringe-lipped bat Túngara frog 



The authors would like to thank the government of the Republic of Panamá for their permission to work in Gamboa and Soberanía National Park and the Smithsonian Tropical Research Institute for providing critical logistical support and infrastructure. Sara Troxell, Sean Griffin, Martha Moscoso, and Patricia Jones helped with capturing and caring for bats. The authors are also grateful to Michael J. Ryan for supplying the túngara frog recordings and to Ximena Bernal, Patricia Jones, Michael Caldwell, Michael J. Ryan, Christian Voigt, Gloriana Chaverri, and two anonymous reviewers for their constructive comments on previous versions of the manuscript. This study was supported by the Smithsonian Tropical Research Institute, the Fonds de Recherche du Québec-Nature et Technologies, the Natural Sciences and Engineering Research Council of Canada, and the Vanier Canada Graduate Fellowship Program.

Ethical standards

The authors declare that the experiments conducted in this research comply with the current laws in the Republic of Panamá. All work was approved by the Panamanian Autoridad Nacional del Ambiente (ANAM permits: SEA-95-10 and SEA-46-11) and the Smithsonian Institution (IACUC permit: 20100816-1012-16).


  1. Akre KL, Ryan MJ (2010) Complexity increases working memory for mating signals. Curr Biol 20:502–505PubMedCrossRefGoogle Scholar
  2. Akre KL, Farris HE, Lea AM, Page RA, Ryan MJ (2011) Signal perception in frogs and bats and the evolution of mating signals. Science 333:751–752PubMedCrossRefGoogle Scholar
  3. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  4. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302PubMedCrossRefGoogle Scholar
  5. Basolo AL (1990) Female preference pre-dates the evolution of the sword in swordtail fish. Science 250:808–810PubMedCrossRefGoogle Scholar
  6. Bernal XE, Rand AS, Ryan MJ (2006) Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett). Behav Ecol 17:709–715CrossRefGoogle Scholar
  7. Bernal XE, Page RA, Rand AS, Ryan MJ (2007) Cues for eavesdroppers: do frog calls indicate prey density and quality? Am Nat 169:409–415PubMedCrossRefGoogle Scholar
  8. Bruns V, Burda H, Ryan MJ (1989) Ear morphology of the frog-eating bat (Trachops cirrhosus, family: Phyllostomidae): apparent specializations for low-frequency hearing. J Morphol 199:103–119CrossRefGoogle Scholar
  9. Cade WH (1975) Acoustically orienting parasitoids: fly phonotaxis to cricket song. Science 190:1312–1313CrossRefGoogle Scholar
  10. Campbell JA (1999) Distributional patterns of amphibians in Middle America. In: Duellman WE (ed) Patterns of distribution of amphibians: a global perspective. Johns Hopkins University Press, Baltimore, pp 111–210Google Scholar
  11. Careau V, Bininda-Emonds ORP, Thomas DW, Réale D, Humphries MM (2009) Exploration strategies map along fast-slow metabolic and life-history continua in muroid rodents. Funct Ecol 23:150–156CrossRefGoogle Scholar
  12. Darwin C (1871) The descent of man and selection in relation to sex. J. Murray, LondonCrossRefGoogle Scholar
  13. Endler JA (1986) Natural selection in the wild. Princeton University Press, PrincetonGoogle Scholar
  14. Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–420PubMedCrossRefGoogle Scholar
  15. Farris HE, Ryan MJ (2011) Relative comparisons of call parameters enable auditory grouping in frogs. Nat Commun 2:410PubMedCrossRefGoogle Scholar
  16. Giannini NP, Kalko EK (2004) Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105:209–220CrossRefGoogle Scholar
  17. Giannini NP, Kalko EK (2005) The guild structure of animalivorous leaf-nosed bats of Barro Colorado Island, Panama, revisited. Acta Chiropterol 7:131–146CrossRefGoogle Scholar
  18. Godin JGJ, McDonough HE (2003) Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav Ecol 14:194–200CrossRefGoogle Scholar
  19. Goerlitz HR, Siemers BM (2007) Sensory ecology of prey rustling sounds: acoustical features and their classification by wild grey mouse lemurs. Funct Ecol 21:143–153CrossRefGoogle Scholar
  20. Halfwerk W, Jones PL, Taylor RC, Ryan MJ, Page RA (2014) Risky ripples allow bats and frogs to eavesdrop on a multisensory sexual display. Science 342:413–416CrossRefGoogle Scholar
  21. Ibáñez R, Rand AS, Jaramillo C (1999) Los anfibios del monumento natural barro colorado, parque nacional soberanía y áreas adyacentes. The amphibians of barro Colorado nature monument, soberanía national park and adjacent areas. Editorial Mizrachi and Pujol, PanamáGoogle Scholar
  22. Jones PL, Farris HE, Ryan MJ, Page RA (2013a) Do frog-eating bats perceptually bind the complex components of frog calls? J Comp Physiol A 199:279–283CrossRefGoogle Scholar
  23. Jones PL, Ryan MJ, Flores V, Page RA (2013b) When to approach novel prey cues? Social learning strategies in frog-eating bats. Proc R Soc B 280:20132330PubMedCentralPubMedCrossRefGoogle Scholar
  24. Jones PL, Ryan MJ, Page RA (2014) Population and seasonal variation in response to prey calls by an eavesdropping bat. Behav Ecol Sociobiol 68:605–615CrossRefGoogle Scholar
  25. Kalko EKV, Friemel D, Handley CO, Schnitzler HU (1999) Roosting and foraging behavior of two neotropical gleaning bats, Tonatia silvicola and Trachops cirrhosus (Phyllostomidae). Biotropica 31:344–353CrossRefGoogle Scholar
  26. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38CrossRefGoogle Scholar
  27. Knörnschild M, von Helversen O (2008) Nonmutual vocal mother–pup recognition in the greater sac-winged bat. Anim Behav 76:1001–1009CrossRefGoogle Scholar
  28. Marler P (1955) Characteristics of some animal calls. Nature 176:6–8CrossRefGoogle Scholar
  29. O’Mara MT, Dechmann DK, Page RA (2014) Frugivorous bats evaluate the quality of social information when choosing novel foods. Behav Ecol 25:1233–1239CrossRefGoogle Scholar
  30. Page RA, Ryan MJ (2005) Flexibility in assessment of prey cues: frog-eating bats and frog calls. Proc R Soc Lond B 272:841–847CrossRefGoogle Scholar
  31. Page RA, Ryan MJ (2006) Social transmission of novel foraging behavior in bats: frog calls and their referents. Curr Biol 16:1201–1205PubMedCrossRefGoogle Scholar
  32. Page RA, Ryan MJ (2008) The effect of signal complexity on localization performance in bats that localize frog calls. Anim Behav 76:761–769CrossRefGoogle Scholar
  33. Page RA, Schnelle T, Kalko EK, Bunge T, Bernal XE (2012a) Sequential assessment of prey through the use of multiple sensory cues by an eavesdropping bat. Naturwissenschaften 99:505–509PubMedCrossRefGoogle Scholar
  34. Page RA, von Merten S, Siemers BM (2012b) Associative memory or algorithmic search: a comparative study on learning strategies of bats and shrews. Anim Cogn 15:495–504PubMedCrossRefGoogle Scholar
  35. Page RA, Ryan MJ, Bernal XE (2014) Be loved, be prey, be eaten. In: Yasukawa K (ed) Animal behavior, vol 3, Case studies: integration and application of animal behavior. Praeger, New York, pp 123–154Google Scholar
  36. Phillips CJ, Tandler B, Pinkstaff CA (1987) Unique salivary glands in two genera of tropical microchiropteran bats an example of evolutionary convergence in histology and histochemistry. J Mammal 68:235–242CrossRefGoogle Scholar
  37. Rand AS, Ryan MJ (1981) The adaptive significance of a complex vocal repertoire in a neotropical frog. Z Tierpsychol 57:209–214CrossRefGoogle Scholar
  38. Ratcliffe JM, ter Hofstede HM (2005) Roosts as information centres: social learning of food preferences in bats. Biol Lett 1:72–74PubMedCentralPubMedCrossRefGoogle Scholar
  39. Rodd FH, Hughes KA, Grether GF, Baril CT (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc R Soc Lond B 269:475–481CrossRefGoogle Scholar
  40. Ron SR (2008) The evolution of female mate choice for complex calls in túngara frogs. Anim Behav 76:1783–1794CrossRefGoogle Scholar
  41. Ryan MJ (1985) The túngara frog, a study in sexual selection and communication. University of Chicago Press, ChicagoGoogle Scholar
  42. Ryan MJ, Cummings ME (2013) Perceptual biases and mate choice. Annu Rev Ecol Evol Syst 44:437–459CrossRefGoogle Scholar
  43. Ryan MJ, Rand AS (2003) Sexual selection in female perceptual space: how female túngara frogs perceive and respond to complex population variation in acoustic mating signals. Evolution 57:2608–2618PubMedGoogle Scholar
  44. Ryan MJ, Tuttle MD (1983) The ability of the frog-eating bat to discriminate among novel and potentially poisonous frog species using acoustic cues. Anim Behav 31:827–833CrossRefGoogle Scholar
  45. Ryan MJ, Tuttle MD, Taft LK (1981) The costs and benefits of frog chorusing behavior. Behav Ecol Sociobiol 8:273–278CrossRefGoogle Scholar
  46. Ryan MJ, Tuttle MD, Rand AS (1982) Sexual advertisement and bat predation in a neotropical frog. Am Nat 110:136–139CrossRefGoogle Scholar
  47. Ryan MJ, Tuttle MD, Barclay RMR (1983) Behavioral responses of the frog-eating bat, Trachops cirrhosus, to sonic frequencies. J Comp Physiol A 150:413–418CrossRefGoogle Scholar
  48. Ryan MJ, Fox JH, Wilczynski W, Rand AS (1990) Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343:66–67PubMedCrossRefGoogle Scholar
  49. Ryan MJ, Bernal XE, Rand AS (2010) Female mate choice and the potential for ornament evolution in the túngara frog Physalaemus pustulosus. Curr Zool 56:343–357Google Scholar
  50. Siemers BM (2001) Finding prey by associative learning in gleaning bats: experiments with Natterer’s bat Myotis nattereri. Acta Chiropterol 3:211–215Google Scholar
  51. Siemers BM, Güttinger R (2006) Prey conspicuousness can explain apparent prey selectivity. Curr Biol 16:R157–R159PubMedCrossRefGoogle Scholar
  52. Siemers BM, Schnitzler HU (2004) Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429:657–661PubMedCrossRefGoogle Scholar
  53. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378PubMedCrossRefGoogle Scholar
  54. Smith C, Barber I, Wootton RJ, Chittka L (2004) A receiver bias in the origin of three-spined stickleback mate choice. Proc R Soc Lond B 271:949–955CrossRefGoogle Scholar
  55. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  56. Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  57. Tandler B, Nagato T, Phillips CJ (1997) Ultrastructure of the unusual accessory submandibular gland in the fringe-lipped bat, Trachops cirrhosus. Anat Rec 248:164–175PubMedCrossRefGoogle Scholar
  58. Trillo PA, Athanas KA, Goldhill DH, Hoke KL, Funk WC (2013) The influence of geographic heterogeneity in predation pressure on sexual signal divergence in an Amazonian frog species complex. J Evol Biol 26:216–222PubMedCrossRefGoogle Scholar
  59. Tuttle MD, Ryan MJ (1981) Bat predation and the evolution of frog vocalizations in the Neotropics. Science 214:677–678PubMedCrossRefGoogle Scholar
  60. Tuttle MD, Taft LK, Ryan MJ (1982) Evasive behavior of a frog in response to bat predation. Anim Behav 30:393–397CrossRefGoogle Scholar
  61. Wagner WE (1995) Convergent song preferences between female field crickets and acoustically orienting parasitoid flies. Behav Ecol Sociobiol 7:279–285CrossRefGoogle Scholar
  62. Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Q Rev Biol 73:415–438CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Vincent Fugère
    • 1
    • 2
  • M. Teague O’Mara
    • 2
    • 3
    • 4
  • Rachel A. Page
    • 2
  1. 1.Department of BiologyMcGill UniversityMontrealCanada
  2. 2.Smithsonian Tropical Research InstituteAncónRepublic of Panamá
  3. 3.Department of Migration and Immuno-EcologyMax Planck Institute for OrnithologyRadolfzellGermany
  4. 4.Department of Biology & ZukunftskollegUniversity of KonstanzKonstanzGermany

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