Advertisement

Rationality in decision-making in the fringe-lipped bat, Trachops cirrhosus

  • Claire T. HemingwayEmail author
  • Michael J. Ryan
  • Rachel A. Page
Original Article

Abstract

Most models of animal behavior assume rationality in animal’s decisions, with animals maintaining strict preferences for different options (e.g., optimal foraging theory). In the wild, however, animals often choose among several options simultaneously, and their evaluation of each prey type may depend on the perceived relative values of other choices. Fringe-lipped bats (Trachops cirrhosus) are promising subjects for studying how animals make decisions. When given a choice between the calls of two species of frogs, T. cirrhosus will choose the more salient call that is associated with the higher capture rate. Although in the wild T. cirrhosus often choose among multiple call options, most tests of prey preferences in this system include only two options. In this experiment, we tested whether T. cirrhosus alters relative preference for two call types that differ along two acoustic dimensions (amplitude and complexity) when presented with a third, “decoy” option, inferior to the two original options along either one or both dimensions. Results from this study demonstrate that under these circumstances, T. cirrhosus evaluates all three options independently of one another, and thus, preferences remain consistent and rational in both the presence and absence of a decoy. These results counter many other experiments suggesting irrationality in animal decision-making.

Significance statement

A fundamental assumption of animal behavior is that animals make rational decisions. However, most animals are tested in ways that rely on simple binary choice experiments. Because animals are often faced with multiple options simultaneously in the wild, these tests may often fail to capture the complexity necessary to understand cognitive limitations that naturally influence animal decisions. In certain cases, complex decisions can result in irrational behavior that is inconsistent with what is found in binary choice studies. Here, we conducted a test with fringe-lipped bats to determine whether their choices for specific frog calls were influenced by the number of options in a choice set. We found that, unlike many other animals, the fringe-lipped bats appear to make consistent decisions, even with more complex choice sets. Our results indicate that there are likely to be strong selective pressures on rational decision-making in this species, perhaps shaped by high metabolic requirements.

Keywords

Bats Túngara frogs Rationality Regularity Decoy effect Decision-making 

Notes

Acknowledgments

We thank the Smithsonian Tropical Research Institute for assistance with permits and logistics. This research was approved by the Smithsonian Tropical Research Institute (STRI IACUC protocol 2014-0101-2017) and the University of Texas, Austin (AUP-2015-00048) and by the Government of Panama (Ministerio de Ambiente permit SE/A 69-15). Special thanks to Paige Johnson, Dallas Miller, and Sebastian Stockmaier for help with capture and caring for bats. We are grateful to Cindy Blanco for her statistical advice and to Stephen Pratt and two other anonymous reviewers for their insightful comments on the manuscript. CTH was funded by fellowship support from the Smithsonian Tropical Research Institute.

Compliance with ethical standards

All authors of this manuscript have read and agree on the content. There are no known financial or nonfinancial conflicts of interest with reviews recommended for this manuscript. All experiments were licensed and approved by the Smithsonian Tropical Research Institute (STRI IACUC protocol 2014-0101-2017) and the University of Texas, Austin (AUP-2015-00048) and by the Government of Panama (Ministerio de Ambiente permit SE/A 69-15). This article does not contain any studies with human participants performed by any of the authors. This work was funded by a Smithsonian Tropical Research Institute Short-term Fellowship Award.

Supplementary material

265_2017_2321_MOESM1_ESM.csv (5 kb)
ESM 1 (CSV 4 kb).
265_2017_2321_MOESM2_ESM.csv (2 kb)
ESM 2 (CSV 1 kb).

References

  1. Ariely D (2010) Predictably irrational: the hidden forces that shape our decisions. New York Harper Perennial, New YorkGoogle 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 333:751–752CrossRefPubMedGoogle Scholar
  3. Bateson M (2002) Context-dependent foraging choices in risk-sensitive starlings. Anim Behav 64:251–260CrossRefGoogle Scholar
  4. Bateson M, Healy SD (2005) Comparative evaluation and its implications for mate choice. Trends Ecol Evol 20:659–664CrossRefPubMedGoogle Scholar
  5. Bateson M, Healy SD, Hurly TA (2002) Irrational choices in hummingbird foraging behaviour. Anim Behav 63:587–596CrossRefGoogle Scholar
  6. Bateson M, Healy SD, Hurly TA (2003) Context-dependent foraging decisions in rufous hummingbirds. Proc R Soc Lond B 270:1271–1276CrossRefGoogle Scholar
  7. Bernal XE, Page RA, Rand AS, Ryan MJ (2007) Cues for eavesdroppers: do frog calls indicate prey density and quality? Am Nat 169:409–415CrossRefPubMedGoogle Scholar
  8. Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197:41–50CrossRefPubMedGoogle Scholar
  9. Dukas R, Kamil AC (2000) The costs of limited attention in blue jays. Behav Ecol 11:502–506CrossRefGoogle Scholar
  10. Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463CrossRefPubMedGoogle Scholar
  11. Edwards SC, Pratt SC (2009) Rationality in collective decision-making by ant colonies. Proc R Soc Lond B 276:3655–3661CrossRefGoogle Scholar
  12. Fleming TH (1986) The structure of Neotropical bat communities: a preliminary analysis. Rev Chilena Hist Nat 59:135–150Google Scholar
  13. Fugère V, O’Mara MT, Page RA (2015) Perceptual bias does not explain preference for prey call adornment in the frog-eating bat. Behav Ecol Sociobiol 69:1353–1364CrossRefGoogle Scholar
  14. Ghose K, Moss CF (2006) Steering by hearing: a bat’s acoustic gaze is linked to its flight motor output by a delayed, adaptive linear law. J Neurol 26:1704–1710Google Scholar
  15. Gigerenzer G, Goldstein DG (1996) Reasoning the fast and frugal way: models of bounded rationality. Psychol Rev 103:650–669CrossRefPubMedGoogle Scholar
  16. Gomes DGE, Page RA, Geipel I, Taylor RC, Ryan MJ, Halfwerk W (2016) Bats perceptually weight cues across sensory systems when hunting in noise. Science 353:1277–1280CrossRefPubMedGoogle Scholar
  17. Heath TB, Chatterjee S (1995) Asymmetric decoy effects on lower-quality versus higher-quality brands: meta-analytical and experimental evidence. J Consum Res 22:268–284CrossRefGoogle Scholar
  18. Huber J, Payne JW, Puto C (1982) Adding asymmetrically dominated alternatives: violations of regularity and the similarity hypothesis. J Consum Res 9:90–98CrossRefGoogle Scholar
  19. Hurly TA, Oseen MD (1999) Context-dependent, risk sensitive foraging preferences in wild rufous hummingbirds. Anim Behav 58:59–66CrossRefPubMedGoogle Scholar
  20. Johnson DDP, Blumstein DT, Fowler JH, Haselton MG (2013) The evolution of error: error management, cognitive constraints, and adaptive decision-making biases. Trends Ecol Evol 28:474–481CrossRefPubMedGoogle Scholar
  21. Jones P, 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
  22. Kacelnik A (2006) Meanings of rationality. In: Hurley SL, Nudds M (eds) Rational animals? Oxford University Press, Oxford, pp 87–106CrossRefGoogle Scholar
  23. 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
  24. Latty T, Beekman M (2011) Irrational decision-making in an amoeboid organism: transitivity and context-dependent preferences. Proc R Soc Lond B 278:307–312CrossRefGoogle Scholar
  25. Lea AM, Ryan MJ (2015) Irrationality in mate choice revealed by túngara frogs. Science 349:964–966CrossRefPubMedGoogle Scholar
  26. Locatello L, Poli F, Rasotto MB (2015) Context-dependent evaluation of prospective mates in a fish. Behav Ecol Sociobiol 69:1119–1126CrossRefPubMedPubMedCentralGoogle Scholar
  27. Luce RP (1959) Individual choice behaviour: a theoretical analysis. Wiley, New YorkGoogle Scholar
  28. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609CrossRefGoogle Scholar
  29. McCleery RH (1978) Optimal behavior sequences and decision making. In: Krebs JR, Davies NB (eds) Behavioral ecology: an evolutionary approach. Sinauer Associates, Sunderland, Massachusetts, pp 377–410Google Scholar
  30. McNamara JM, Trimmer PC, Houston AI (2014) Natural selection can favour ‘irrational’ behavior. Biol Lett 10:20130935CrossRefPubMedPubMedCentralGoogle Scholar
  31. Monteiro T, Vasconcelos M, Kacelnik A (2013) Starlings uphold principles of economic rationality for delay and probability of reward. Proc R Soc B 280:20122386CrossRefPubMedPubMedCentralGoogle Scholar
  32. Morgan KV, Hurly TA, Bateson M, Asher L, Healy SD (2012) Context-dependent decisions among options varying in a single dimension. Behav Process 89:115–120CrossRefGoogle Scholar
  33. Morgan KV, Hurly TA, Healy SD (2014) Individual differences in decision making by foraging hummingbirds. Behav Process 109:195–200CrossRefGoogle Scholar
  34. Navarick DJ, Fantino E (1972) Transitivity as a property of choice. J Exp Anal Behav 18:389–401CrossRefPubMedPubMedCentralGoogle Scholar
  35. Orr AH (2007) Absolute fitness, relative fitness, and utility. Evolution 61:2997–3000CrossRefPubMedGoogle Scholar
  36. 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
  37. Page RA, Ryan MJ (2008) The effect of signal complexity on localization performance in bats that localize frogs. Anim Behav 76:761–769CrossRefGoogle Scholar
  38. Parrish AE, Evans TA, Beran MJ (2015) Rhesus macaques (Macaca mulatta) exhibit the decoy effect in a perceptual discrimination task. Atten Percept Psychophys 77:1715–1725CrossRefPubMedPubMedCentralGoogle Scholar
  39. Pompilio L, Kacelnik A (2005) State-dependent learning and suboptimal choice: when starlings prefer long over short delays to food. Anim Behav 70:571–578CrossRefGoogle Scholar
  40. Pompilio L, Kacelnik A, Behmer ST (2006) State-dependent learned valuation drives choice in an invertebrate. Science 311:1613–1615CrossRefPubMedGoogle Scholar
  41. Developmental Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/ Google Scholar
  42. Reany LT (2009) Female preference for male phenotypic traits in a fiddler crab: do females use absolute or comparative evaluation? Anim Behav 77:139–143CrossRefGoogle Scholar
  43. Royle NJ, Lindström J, Metcalfe NB (2008) Context-dependent mate choice in relation to social composition in green swordtails Xiphophorus helleri. Behav Ecol 19:998–1005CrossRefGoogle Scholar
  44. Ryan MJ (1985) The túngara frog: a study in sexual selection and communication. University of Chicago Press, ChicagoGoogle Scholar
  45. Ryan MJ, Akre KL, Kirkpatrick M (2009) Cognitive mate choice. In: Dukas R, Ratcliffe J (eds) Cognitive ecology II. University of Chicago Press, Chicago, pp 137–155CrossRefGoogle Scholar
  46. Ryan MJ, Rand AS (1981) The adaptive significance of a complex vocal repertoire in a neotropical frog. Z Tierpsychol 57:209–214Google Scholar
  47. Ryan MJ, Rand AS (1990) The sensory basis of sexual selection for complex calls in the túngara frog: Physalaemus pustulosus (sexual selection for sensory exploitation). Evolution 44:305–314CrossRefPubMedGoogle Scholar
  48. 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
  49. Ryan MJ, Tuttle MD, Rand AS (1982) Bat predation and sexual advertisement in a neotropical anuran. Am Nat 119:136–139CrossRefGoogle Scholar
  50. Ryan MJ, Tuttle MD (1987) The role of prey-generated sounds, vision, and echolocation in prey localization by the African batCardioderma cor (Megadermatidae). J Comp Physiol A 161(1):59–66Google Scholar
  51. Ryan MJ, Tuttle MD, Taft LK (1981) The costs and benefits of frog chorusing behavior. Behav Ecol Soc 8:273–278CrossRefGoogle Scholar
  52. Sanfey AG, Loewenstein G, McClure SM, Cohen JD (2006) Neuroeconomics: cross-currents in research on decision-making. Trends Cogn Sci 10:108–116CrossRefPubMedGoogle Scholar
  53. Sasaki T, Pratt SC (2011) Emergence of group rationality from irrational individuals. Behav Ecol 22:276–281CrossRefGoogle Scholar
  54. Scarpi D (2011) The impact of phantom decoys on choice in cats. Anim Cogn 14:127–136CrossRefPubMedGoogle Scholar
  55. Schuck-Paim C, Pompilio L, Kacelnik A (2004) State-dependent decisions cause apparent violations of rationality in animal choice. PLoS Biol 12:e402Google Scholar
  56. Shampanier K, Mazar N, Ariely D (2007) Zero as a special price: the true value of free products. Mark Sci 26:742–757CrossRefGoogle Scholar
  57. Shafir S (1994) Intransitivity of preferences in honeybees: support for ‘comparative’ evaluation of foraging options. Anim Behav 48:55–67CrossRefGoogle Scholar
  58. Shafir S, Waite TA, Smith BH (2002) Context-dependent violations of rational choice in honeybees (Apis mellifera) and gray jays (Perisoreus canadensis). Behav Ecol Sociobiol 51:180–187CrossRefGoogle Scholar
  59. Shen YY, Liang L, Zhu ZH, Zhou WP, Irwin DM, Zhang YP (2010) Adaptive evolution of energy metabolism genes and the origin of flight in bats. P Natl Acad Sci USA 107:8666–8671CrossRefGoogle Scholar
  60. Shettleworth S (2010) Cognition, evolution, and behavior. Oxford University Press, OxfordGoogle Scholar
  61. Simmons JA, Moss CF, Ferragamo M (1990) Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus. J Comp Physiol A 166:449–470PubMedGoogle Scholar
  62. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  63. Tuttle MD, Ryan MJ (1981) Bat predation and the evolution of frog vocalizations in the Neotropics. Science 214:677–678CrossRefPubMedGoogle Scholar
  64. Tuttle MD, Taft LK, Ryan MJ (1982) Evasive behaviour of a frog in response to bat predation. Anim Behav 30:393–397CrossRefGoogle Scholar
  65. Waite TA, Nevai AL, Passino KM (2007) State subsidies induce gray jays to accept greater danger: an ecologically rational response? Behav Ecol Sociobiol 61:1261–1266CrossRefGoogle Scholar
  66. Winter Y, Stich KP (2005) Foraging in a complex naturalistic environment: capacity of spatial working memory in flower bats. J Exp Biol 208:539–548CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Claire T. Hemingway
    • 1
    • 2
    Email author
  • Michael J. Ryan
    • 1
    • 2
  • Rachel A. Page
    • 2
  1. 1.Department of Integrative BiologyUniversity of TexasAustinUSA
  2. 2.Smithsonian Tropical Research InstituteBalboaPanamá

Personalised recommendations