Advertisement

Environmental heterogeneity alters mate choice behavior for multimodal signals

  • Andrew D. Cronin
  • Michael J. Ryan
  • Rachel A. Page
  • Kimberly L. Hunter
  • Ryan C. TaylorEmail author
Original Article

Abstract

Animals frequently experience changes in their environment, including diel and seasonal shifts in abiotic and biotic factors. In addition to physiological and morphological changes, animals alter their behavior in response to environmental variation. This study examined the impacts of heterogeneous environments on mating behaviors. We examined both male and female túngara frog phonotactic responses to multimodal (audiovisual) and unimodal (acoustic) stimuli. We altered aspects of the physical environment by changing substrate (terrestrial and aquatic) and ambient light levels. Females demonstrated a similar preference for the audiovisual stimulus regardless of substrate but decreased latency to choose in an aquatic environment. When ambient light levels were increased (relative to darker control), females reversed their preference, avoiding the multimodal stimulus, but the latency to choose was unchanged. Males demonstrated no preference for the multimodal signal on either substrate, but like females, male latency was reduced in an aquatic environment. Different environments carry their own associated costs, including varying levels of predation risk. Increased light levels and an aquatic environment likely carry higher predation risk and therefore should lead to changes in female and male responses. Interestingly, these two environments do not cause uniform changes in female responses. The addition of an aquatic environment led to a reduction in latency, whereas an increase in ambient light levels induced a change in female mate preference. These findings demonstrate the importance of the environment on mating responses to multimodal signals.

Significance statement

Responses to conspecific mating signals (e.g., mate preferences) have often been assumed to be static. In this study, we tested responses of both male and female túngara frogs to a multimodal (visual + vocal) advertisement signal under varying environmental conditions. Elevated light levels changed female responses to mating signals. When both sexes were required to swim, rather than walk to a signal, their choices did not change. They did respond faster, however. These results indicate that measuring the strength of sexual selection should be considered as a function of both innate preferences and the environmental conditions experienced by the animals.

Keywords

Multimodal signaling Environmental heterogeneity Sexual selection Túngara frog 

Notes

Acknowledgments

Kyle Davis provided help with data collection and logistics. Two anonymous reviewers provided valuable comments, improving the manuscript. The Smithsonian Tropical Research Institute provided logistical support and laboratory space.

Funding information

Funding for equipment was provided by NSF grant (no. 0517328) to RCT, MJR, and RAP. Salisbury University provided travel funding for ADC, RCT, and KLH. Travel funds were facilitated by Stephen Gehnrich and Clifton Griffin at Salisbury University.

Compliance with ethical standards

Ethical standards

Handling and toe clip procedures were conducted in accordance with The American Society of Ichthyologists and Herpetologists’ Guidelines for Use of Live Amphibians and Reptiles in Field and Laboratory Research. All experiments were conducted in accordance with Smithsonian Tropical Research Institute guidelines and approved by the Institutional Animal Care and Use Committee (protocol no. 2015-0209-2018). All necessary permits were obtained from the Panamanian government including collecting permit numbers SE/A-30-16 and SE/AO-1-17.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akre KL, Ryan MJ (2010a) Proximity-dependent response to variably complex mating signals in túngara frogs (Physalaemus pustulosus). Ethology 116:1138–1145CrossRefGoogle Scholar
  2. Akre KL, Ryan MJ (2010b) Complexity increases working memory for mating signals. Curr Biol 20:502–505CrossRefGoogle Scholar
  3. Aspbury AS, Espinedo CM, Gabor CR (2010) Lack of species discrimination based on chemical cues by male sailfin mollies, Poecilia latipinna. Evol Ecol 24:69–82CrossRefGoogle Scholar
  4. Baugh AT, Ryan MJ (2010) Ambient light alters temporal-updating behaviour during mate choice in a Neotropical frog. Can J Zool 88:448–453CrossRefGoogle Scholar
  5. Bernal XE, Rand AS, Ryan MJ (2007) Sex differences in response to nonconspecific advertisement calls: receiver permissiveness in male and female túngara frogs. Anim Behav 73:955–964CrossRefGoogle Scholar
  6. Bernal XE, Rand AS, Ryan MJ (2009) Task differences confound sex differences in receiver permissiveness in túngara frogs. Proc R Soc Lond B 276:1323–1329CrossRefGoogle Scholar
  7. Bonachea LA, Ryan MJ (2011a) Predation risk increases permissiveness for heterospecific advertisement calls in túngara frogs, Physalaemus pustulosus. Anim Behav 82:347–352CrossRefGoogle Scholar
  8. Bonachea LA, Ryan MJ (2011b) Simulated predation risk influences female choice in túngara frogs, Physalaemus pustulosus. Ethology 117:400–407CrossRefGoogle Scholar
  9. Botero CA, Rubenstein DR (2012) Fluctuating environments, sexual selection and the evolution of flexible mate choice in birds. PLoS One 7:e32311CrossRefGoogle Scholar
  10. Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 17:571–577CrossRefGoogle Scholar
  11. Bro-Jørgensen J (2010) Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol Evol 25:292–300CrossRefGoogle Scholar
  12. Buchanan BW (1992) Bimodal nocturnal activity pattern of Hyla squirella. J Herpetol 26:521–523CrossRefGoogle Scholar
  13. Campbell-Staton SC, Cheviron ZA, Rochette N, Catchen J, Losos JB, Edwards SV (2017) Winter storms drive rapid phenotypic, regulatory, and genomic shifts in the green anole lizard. Science 357:495–498CrossRefGoogle Scholar
  14. Chaine AS, Lyon BE (2008) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462CrossRefGoogle Scholar
  15. Chittka L, Skorupski P, Raine NE (2009) Speed-accuracy trade-offs in animal decision-making. Trends Ecol Evol 24:400–407CrossRefGoogle Scholar
  16. Cummings ME, Bernal XE, Reynaga R, Rand AS, Ryan MJ (2008) Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females. J Exp Biol 211:1203–1210CrossRefGoogle Scholar
  17. deRivera CE, Backwell PR, Christy JH, Vehrencamp SL (2003) Density affects female and male mate searching in the fiddler crab, Uca beebei. Behav Ecol Sociobiol 53:72–83Google Scholar
  18. Endler JA (1987) Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Anim Behav 35:1376–1385CrossRefGoogle Scholar
  19. Farris HE, Ryan MJ (2011) Relative comparisons enable auditory grouping in frogs. Nat Commun 2:410CrossRefGoogle Scholar
  20. Forstmeier W, Martin K, Bolund E, Schielzeth H, Kempenaers B (2011) Female extrapair mating behavior can evolve via indirect selection on males. P Natl Acad Sci USA 108:10608–10613CrossRefGoogle Scholar
  21. Forsgren E (1992) Predation risk affects mate choice in a gobiid fish. Am Nat 140:1041–1049CrossRefGoogle Scholar
  22. Gong A, Gibson RM (1996) Reversal of a female preference after visual exposure to a predator in the guppy, Poecilia reticulata. Anim Behav 52:1007–1015CrossRefGoogle Scholar
  23. Gomes D, Geipel I, Page RA, Taylor RC, Ryan MJ, Halfwerk W (2016) Bats perceptually weight prey cues across sensory systems when hunting in noise. Science 353:1277–1280CrossRefGoogle Scholar
  24. Gordon SD, Uetz GW (2011) Multimodal communication of wolf spiders on different substrates: evidence for behavioural plasticity. Anim Behav 81:367–375CrossRefGoogle Scholar
  25. Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711CrossRefGoogle Scholar
  26. Halfwerk W, Bot S, Buikx J, van der Velde M, Komdeur J, ten Cate C, Slabbekoorn H (2011) Low-frequency songs lose their potency in noisy urban conditions. P Natl Acad Sci USA 108:14549–14554CrossRefGoogle Scholar
  27. 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 343:413–416CrossRefGoogle Scholar
  28. Halfwerk W, Slabbekoorn H (2015) Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol Lett 11:20141051CrossRefGoogle Scholar
  29. Halfwerk W, Smit JAH, Loning H, Lea AM, Geipel I, Ellers J, Ryan MJ (2017) Environmental conditions limit attractiveness of a complex sexual signal in the túngara frog. Nat Commun 8:1891CrossRefGoogle Scholar
  30. Hebets EA, Barron AB, Balakrishnan CN, Hauber ME, Mason PH, Hoke KL (2016) A systems approach to animal communication. Proc R Soc B 283:20152889CrossRefGoogle Scholar
  31. Hedrick AV, Dill LM (1993) Mate choice by female crickets is influenced by predation risk. Anim Behav 46:193–196CrossRefGoogle Scholar
  32. Higham JP, Hebets EA (2013) An introduction to multimodal communication. Behav Ecol Sociobiol 67:1381–1388CrossRefGoogle Scholar
  33. Höbel G, Kolodziej RC (2013) Wood frogs (Lithobates sylvaticus) use water surface waves in their reproductive behaviour. Behaviour 150:471–483CrossRefGoogle Scholar
  34. Hoke KL, Ryan MJ, Wilczynski W (2008) Candidate neural locus for sex differences in reproductive decisions. Biol Lett 4:518–521CrossRefGoogle Scholar
  35. Johnson JB, Basolo AL (2003) Predator exposure alters female mate choice in the green swordtail. Behav Ecol 14:619–625CrossRefGoogle Scholar
  36. Kaczorowski RL, Leonard AS, Dornhaus A, Papaj DR (2012) Floral signal complexity as a possible adaptation to environmental variability: a test using nectar-foraging bumblebees, Bombus impatiens. Anim Behav 83:905–913CrossRefGoogle Scholar
  37. Karino K, Kuwamura T, Nakashima Y, Sakai Y (2000) Predation risk and the opportunity for female mate choice in a coral reef fish. J Ethol 18:109–114CrossRefGoogle Scholar
  38. Kim TW, Christy JH, Choe JC (2007) A preference for a sexual signal keeps females safe. PLoS One 2:e422CrossRefGoogle Scholar
  39. Klein BA, Stein J, Taylor RC (2012) Robots in the service of animal behavior. Commun Integr Biol 5:466–472CrossRefGoogle Scholar
  40. Lawler SP (1989) Behavioural responses to predators and predation risk in four species of larval anurans. Anim Behav 38:1039–1047CrossRefGoogle Scholar
  41. Lea AM, Ryan MJ (2015) Irrationality in mate choice revealed by túngara frogs. Science. 349:964–966CrossRefGoogle Scholar
  42. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  43. Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2:191–198CrossRefGoogle Scholar
  44. Lynch KS, Crews D, Ryan MJ, Wilczynski W (2006) Hormonal state influences aspects of female mate choice in the túngara frog (Physalaemus pustulosus). Horm Behav 49:450–457CrossRefGoogle Scholar
  45. Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos Trans R Soc B 363:321–339CrossRefGoogle Scholar
  46. Milinski M, Bakker TCM (1992) Costs influence sequential mate choice in sticklebacks, Gasterosteus aculeatus. Proc R Soc Lond B 250:229–233CrossRefGoogle Scholar
  47. Partan SR, Marler P (1999) Communication goes multimodal. Science 283:1272–1273CrossRefGoogle Scholar
  48. Perry G, Buchanan BW, Fisher RN, Salmon M, Wise SE (2008) Effects of artificial night lighting on amphibians and reptiles in urban environments. In: Mitchell JC, Jung Brown RE, Bartholomew B (eds) Herpetological conservation 3: urban herpetology: ecology, conservation and management of amphibians and reptiles in urban and suburban environments. Society for the Study of Amphibians and Reptiles, Salt Lake City, pp 239–256Google Scholar
  49. Peters SE, Kamel LT, Bashor DP (1996) Hopping and swimming in the leopard frog, Rana pipiens. I. Step cycles and kinematics. J Morphol 230:1–16CrossRefGoogle Scholar
  50. Pilakouta N, Alonzo SH (2013) Predator exposure leads to a short-term reversal in female mate preferences in the green swordtail, Xiphophorus helleri. Behav Ecol 25:306–312CrossRefGoogle Scholar
  51. Pilakouta N, Correa MA, Alonzo SH (2017) Predation risk reduces a female preference for heterospecific males in the green swordtail. Ethology 123:95–104CrossRefGoogle Scholar
  52. Pocklington R, Dill LM (1995) Predation on females or males: who pays for bright male traits? Anim Behav 49:1122–1124CrossRefGoogle Scholar
  53. Qvarnström A, Pärt T, Sheldon BC (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347CrossRefGoogle Scholar
  54. Rand AS, Bridarolli ME, Dries L, Ryan MJ (1997) Light levels influence female choice in túngara frogs: predation risk assessment? Copeia 1997:447–450CrossRefGoogle Scholar
  55. Relyea RA (2002) Local population differences in phenotypic plasticity: predator induced changes in wood frog tadpoles. Ecol Monogr 72:77–93CrossRefGoogle Scholar
  56. Richardson JM (2001) A comparative study of activity levels in larval anurans and response to the presence of different predators. Behav Ecol 12:51–58CrossRefGoogle Scholar
  57. Rosenthal GG (2017) Mate choice: the evolution of sexual decision making from microbes to humans. Princeton University Press, PrincetonCrossRefGoogle Scholar
  58. Ryan MJ (1985) The túngara frog: a study in sexual selection and communication. University of Chicago Press, ChicagoGoogle Scholar
  59. Ryan MJ, Fox JH, Wilczynski W, Rand AS (1990) Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature 343:66–67CrossRefGoogle Scholar
  60. 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 44:305–314CrossRefGoogle Scholar
  61. 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
  62. Segami Marzal JC, Rudh A, Rogell B, Ödeen A, Løvlie H, Rosher C, Qvarnström A (2017) Cryptic female strawberry poison frogs experience elevated predation risk when associating with an aposematic partner. Ecol Evol 7:744–750CrossRefGoogle Scholar
  63. Stafstrom JA, Hebets EA (2013) Female mate choice for multimodal courtship and the importance of the signaling background for selection on male ornamentation. Curr Zool 59:200–209CrossRefGoogle Scholar
  64. Stange N, Page RA, Ryan MJ, Taylor RC (2016) Interactions between complex multisensory signal components result in unexpected mate choice responses. Anim Behav 134:239–247CrossRefGoogle Scholar
  65. Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, Huey RB (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. P Natl Acad Sci USA 111:5610–5615CrossRefGoogle Scholar
  66. Taylor RC, Buchanan BW, Doherty JL (2007) Sexual selection in the squirrel treefrog Hyla squirella: the role of multimodal cue assessment in female choice. Anim Behav 74:1753–1763CrossRefGoogle Scholar
  67. Taylor RC, Klein B, Stein J, Ryan MJ (2008) Faux frogs: multimodal signalling and the value of robotics in animal behaviour. Anim Behav 76:1089–1097CrossRefGoogle Scholar
  68. Taylor RC, Klein BA, Stein J, Ryan MJ (2011) Multimodal signal variation in space and time: how important is matching a signal with its signaler? J Exp Biol 214:815–820CrossRefGoogle Scholar
  69. Taylor RC, Ryan MJ (2013) Interactions of multisensory components perceptually rescue túngara frog mating signals. Science 341:273–274CrossRefGoogle Scholar
  70. Uitenbroek DG (1997) SISA binomial, http://home.clara.net/sisa/binomial.htm
  71. Underhill VA, Höbel G (2017) Variation in nocturnal light levels does not alter mate choice behavior in female eastern gray treefrogs (Hyla versicolor). Behav Ecol Sociobiol 71:151CrossRefGoogle Scholar
  72. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278CrossRefGoogle Scholar
  73. Wilgers DJ, Hebets EA (2011) Complex courtship displays facilitate male reproductive success and plasticity in signaling across variable environments. Curr Zool 57:175–186CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologySalisbury UniversitySalisburyUSA
  2. 2.Department of Ecological ScienceVrije UniversiteitAmsterdamThe Netherlands
  3. 3.Department of Integrative BiologyUniversity of Texas at AustinAustinUSA
  4. 4.Smithsonian Tropical Research InstituteBalboaRepublic of Panama

Personalised recommendations