Journal of Comparative Physiology A

, Volume 203, Issue 4, pp 265–273 | Cite as

Vasotocin induces sexually dimorphic effects on acoustically-guided behavior in a tropical frog

  • Alexander T. BaughEmail author
  • Michael J. Ryan
Original Paper


The neuropeptide arginine vasotocin (AVT) promotes sexual advertisement and influences vocalization structure in male anuran amphibians. In the present study, we used wild túngara frogs (Physalaemus pustulosus) to investigate the effects of AVT on phonotaxis in males and females—thereby controlling for potential task differences between the sexes. Using a combined within- and between-subjects design, we showed that acoustic choice behavior in female frogs is not influenced by injection per se (vehicle) or by AVT. Latency to choice in females, however, tends to decrease after AVT injection, supporting the hypothesis that AVT promotes female sexual arousal. In contrast, male choice behavior and latencies are negatively impacted by injection (vehicle) but rescued to pre-injection levels if administered with AVT. The sexes differed in area restricted searching (ARS) following choice—a measure of locomotor perseverance—with females but not males exhibiting ARS. AVT did not influence ARS behavior but ARS frequency was positively associated with the attractiveness of the acoustic stimulus. Finally, we showed that a female’s latency behavior is correlated with her partner’s behavior. Collectively we show that AVT promotes phonotaxis in both sexes in a dimorphic manner—a result that is consistent with sex differences in the neural vasotocin system.


Arginine vasotocin Phonotaxis Physalaemus pustulosus Sex differences Túngara 



The National Science Foundation (IOB 0544096; MJR) funded this research. The Smithsonian Tropical Research Institute provided logistical support for this study and Autoridad Nacional del Ambiente approved scientific permits in the Republic of Panamá. Animal use was approved by the Institutional Animal Care and Use Committee at The University of Texas at Austin.

Supplementary material

359_2017_1155_MOESM1_ESM.pdf (344 kb)
Supplementary material 1 (PDF 343 KB)
359_2017_1155_MOESM2_ESM.pdf (304 kb)
Supplementary material 2 (PDF 303 KB)
359_2017_1155_MOESM3_ESM.pdf (310 kb)
Supplementary material 3 (PDF 309 KB)


  1. Akre KL, Ryan MJ (2010) Complexity increases working memory for mating signals. Curr Biol 20:502–505CrossRefPubMedGoogle Scholar
  2. Baugh AT, Ryan MJ (2010a) The development of sexual behaviour in túngara frogs. J Comp Psychol 124:66–80CrossRefPubMedGoogle Scholar
  3. Baugh AT, Ryan MJ (2010b) Temporal updating during phonotaxis in male túngara frogs (Physalaemus pustulosus). Amphib-Reptil 31:449–454CrossRefGoogle Scholar
  4. Baugh AT, Akre KL, Ryan MJ (2008) Categorical perception of a natural, multivariate signal: mating call recognition in túngara frogs. Proc Nat Acad Sci USA 105:8985–8988.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bee MA (2007) Selective phonotaxis by male wood frogs (Rana sylvatica) to the sound of a chorus. Behav Ecol Sociobiol 61:955–966CrossRefGoogle Scholar
  6. Bernal XE, Rand AS, Ryan MJ (2009) Task differences underlie sexual dimorphism in mating behaviour in túngara frogs, Physalaemus pustulosus. Proc R Soc B 276:1323–1329.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bosch J, Márquez R (2002) Female preference function related to precedence effect in an amphibian anuran (Alytes cisternasii): tests with non-overlapping calls. Behav Ecol 13:149–153CrossRefGoogle Scholar
  8. Boyd SK (1991) Effect of vasotocin on locomotor activity in bullfrogs varies with developmental stage and sex. Horm Behav 25:57–69CrossRefPubMedGoogle Scholar
  9. Boyd SK (1994) Arginine vasotocin facilitation of advertisement calling and call phonotaxis in bullfrogs. Horm Behav 28:232–240CrossRefPubMedGoogle Scholar
  10. Boyd SK (1997) Brain vasotocin pathways and the control of sexual behaviors in the bullfrog. Brain Res Bull 44:345–350CrossRefPubMedGoogle Scholar
  11. Boyd SK (2013) Vasotocin modulation of social behaviors in amphibians. In: Choleris E, Pfaff D, Kavaliers M (eds) Oxytocin, vasopressin and related peptides in the regulation of behavior. Cambridge University Press, Cambridge, pp 97–105CrossRefGoogle Scholar
  12. Boyd SK, Moore FL (1992) Sexually dimorphic concentrations of arginine vasotocin in sensory regions of the amphibian brain. Brain Res 588:304–306CrossRefPubMedGoogle Scholar
  13. Caldwell HK, Young WS III (2006) Oxytocin and vasopressin: genetics and behavioral implications. In: Lajtha A, Lim R (eds) Handbook of neurochemistry and molecular neurobiology: neuroactive proteins and peptides, 3rd edn, Springer, Berlin, pp 573–607.CrossRefGoogle Scholar
  14. Chu J, Marler CA, Wilczynski W (1998) The effects of arginine vasotocin on the calling behavior of male cricket frogs in changing social contexts. Horm Behav 34:248–261CrossRefPubMedGoogle Scholar
  15. Coddington E, Moore F (2003) Neuroendocrinology of context-dependent stress responses: vasotocin alters the effect of corticosterone on amphibian behaviors. Horm Behav 43:222–228CrossRefPubMedGoogle Scholar
  16. Diakow C (1978) A hormonal basis for breeding behavior in female frogs: vasotocin inhibits the release call of Rana pipiens. Science 199:1456–1457CrossRefPubMedGoogle Scholar
  17. Diakow C, Wilcox JN, Woltmann R (1978) Female frog reproductive behavior elicited in the absence of the ovaries. Horm Behav 11:183–189CrossRefPubMedGoogle Scholar
  18. Endepols H, Walkowiak W (1999) Influence of descending forebrain projections on processing of acoustic signals and audiomotor integration in the anuran midbrain. Eur J Morphol 37:182–184.CrossRefPubMedGoogle Scholar
  19. Endepols H, Walkowiak W (2001) Integration of ascending and descending inputs in the auditory midbrain of anurans. J Comp Physiol A 186:1119–1133CrossRefGoogle Scholar
  20. Endepols H, Feng AS, Gerhardt HC, Schul J, Walkowiak W (2003) Roles of the auditory midbrain and thalamus in selective phonotaxis in female gray treefrogs (Hylaversicolor). Behav Brain Res 145:63–77CrossRefPubMedGoogle Scholar
  21. Hills T, Brockie PJ, Maricq AV (2004) Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 24:1217–1225CrossRefPubMedGoogle Scholar
  22. Hyde JF, Jerussi TP (1983) Sexual dimorphism in rats with respect to locomotor activity and circling behavior. Pharmacol Biochem Behav 18:725–729CrossRefPubMedGoogle Scholar
  23. Kabelik D, Klatt JD, Kingsbury MA, Goodson JL (2009) Endogenous vasotocin exerts context-dependent behavioral effects in a semi-naturalistic colony environment. Horm Behav 56:101–107CrossRefPubMedPubMedCentralGoogle Scholar
  24. Keister R (1979) Conspecfics as cues: a mechanism for habitat selection in the Panamanian grass anole (Anolis auratus). Behav Ecol Sociobiol 5:323–330CrossRefGoogle Scholar
  25. Kime NM, Rand AS, Kapfer M, Ryan MJ (1998) Repeatability of female choice in the túngara frog: a permissive preference for complex characters. Anim Behav 55:641–649CrossRefPubMedGoogle Scholar
  26. Kime NM, Whitney TK, Davis ES, Marler CA (2007) Arginine vasotocin promotes calling behavior and call changes in male túngara frogs. Brain Behav Evol 69:254–265CrossRefPubMedGoogle Scholar
  27. Kime NM, Whitney TK, Ryan MJ, Rand AS, Marler CA (2010) Treatment with arginine vasotocin alters mating calls and decreases call attractiveness in male túngara frogs. Gen Comp Endocrinol 165:221–228CrossRefPubMedGoogle Scholar
  28. Leary CJ, Jessop TS, Garcia AM, Knapp R (2004) Steroid hormone profiles and relative body condition of calling and satellite toads: implications for proximate regulation of behavior in anurans. Behav Ecol 15:313–320CrossRefGoogle Scholar
  29. Marler CA, Chu J, Wilczynski W (1995) Arginine vasotocin injection increases probability of calling in cricket frogs, but causes call changes characteristic of less aggressive males. Horm Behav 29:554–570CrossRefPubMedGoogle Scholar
  30. Marler CA, Boyd SK, Wilczynski W (1999) Forebrain neuropeptide correlates of alternative male mating strategies under field conditions. Horm Behav 36:53–61CrossRefPubMedGoogle Scholar
  31. Moore FL, Rose JD (2002) Sensorimotor processing model: how vasotocin and corticosterone interact and control reproductive behaviors in an amphibian. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, Brain and Behavior, 2nd edn, Academic Press, San Diego, pp 515–545.CrossRefGoogle Scholar
  32. Moore FL, Wood RE, Boyd SK (1992) Sex steroids and vasotocin interact in a female amphibian (Taricha granulosa) to elicit female-like egg-laying behavior or male-like courtship. Horm Behav 26:156–166CrossRefPubMedGoogle Scholar
  33. Oldfield RG, Hofmann HA (2011) Neuropeptide regulation of social behavior in a monogamous cichlid fish. Physiol Behav 102:296–303CrossRefPubMedGoogle Scholar
  34. Penna M, Capranica RR, Somers J (1992) Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog, Hyla cinerea. J Comp Physiol A 170:73–82CrossRefPubMedGoogle Scholar
  35. Pfennig KS, Rodriguez Moncalvo VG, Burmeister SS (2013) Diet alters ontogeny of species recognition in juvenile toads. Biol Lett 9:20130599CrossRefPubMedPubMedCentralGoogle Scholar
  36. Propper CR, Dixon TB (1997) Differential effects of arginine vasotocin and gonadotrophin-releasing hormone on sexual behaviors in an anuran amphibian. Horm Behav 32:99–104CrossRefPubMedGoogle Scholar
  37. Rand AS, Ryan MJ, Wilczynski W (1992) Signal redundancy and receiver permissiveness in acoustic mate recognition by the túngara frog, Physalaemus pustulosus. Am Zool 32:81–90.CrossRefGoogle Scholar
  38. Ryan MJ (1985) The túngara frog: a study in sexual selection and communication. University of Chicago Press, ChicagoGoogle Scholar
  39. 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
  40. Ryan MJ, Rand AS (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647–657CrossRefGoogle Scholar
  41. Ryan MJ, Rand W, Hurd PL, Phelps SM, Rand AS (2003) Generalization in response to mate recognition signals. Am Nat 161:380–394CrossRefPubMedGoogle Scholar
  42. Semsar K, Klomberg KF, Marler CA (1998) Arginine vasotocin and calling behaviour and call site retention in frogs. Anim Behav 56:983–987CrossRefPubMedGoogle Scholar
  43. Stamps JA (1988) Conspecific attraction and aggregation in territorial species. Am Nat 131:329–347CrossRefGoogle Scholar
  44. Stamps JA (1991) The effect of conspecifics on habitat selection in territorial species. Behav Ecol Sociobiol 28:29–36CrossRefGoogle Scholar
  45. Ten Eyck GR, Haq AU (2012) Arginine vasotocin activates aggressive calls during paternal care in the Puerto Rican coquí frog, Eleutherodactylus coqui. Neurosci Lett 525:152–156CrossRefPubMedGoogle Scholar
  46. Thompson RR, Moore FL (2003) The effects of sex steroids and vasotocin on behavioral responses to visual and olfactory sexual stimuli in ovariectomized female roughskin newts. Horm Behav 44:311–318CrossRefPubMedGoogle Scholar
  47. Tito MB, Hoover MA, Mingo AM, Boyd SK (1999) Vasotocin maintains multiple call types in the gray treefrog, Hyla versicolor. Horm Behav 36:166–-175CrossRefPubMedGoogle Scholar
  48. Weigt LA, Crawford AJ, Rand AS, Ryan MJ (2005) Biogeography of the túngara frog, Physalaemus pustulosus. Mol Ecol 14:3857–3876CrossRefPubMedGoogle Scholar
  49. Wilczynski W, Lynch KS, O’Bryant EL (2005) Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology. Horm Behav 48:440–450CrossRefPubMedPubMedCentralGoogle Scholar
  50. Young LJ, Wang Z, Insel TR (1998) Neuroendocrine bases of monogamy. Trends Neurosci 21:71–75CrossRefPubMedGoogle Scholar
  51. Beaupre SJ, Jacobson ER, Lillywhite HB, Zamudio K (2004) Guidelines for the use of live amphibians and reptiles in field and laboratory research.

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of BiologySwarthmore CollegeSwarthmoreUSA
  2. 2.Department of Integrative BiologyThe University of Texas at AustinAustinUSA
  3. 3.Smithsonian Tropical Research InstituteBalboa AnconPanama

Personalised recommendations