Advertisement

Journal of Comparative Physiology A

, Volume 205, Issue 4, pp 505–513 | Cite as

Effects of intracerebroventricular arginine vasotocin on a female amphibian proceptive behavior

  • Sunny K. BoydEmail author
Original Paper
  • 63 Downloads

Abstract

Mate choice decisions of animals show significant variability—both among and within individuals. Clearly, such variability can profoundly impact individual fitness, as well as subtly alter sexual selection processes, but we know little about the neural mechanisms underlying such variability. We examined the influence of the neuropeptide arginine vasotocin (AVT) on the strength of attraction of female gray treefrogs (Hyla versicolor) showing positive phonotaxis to the call of a conspecific male. Female treefrogs received intracerebroventricular injections with either saline, AVT (five doses), or the AVT receptor antagonist Manning compound (two doses). By 30 min after injection, AVT significantly increased the speed with which females approached the speaker, at doses of 1, 10 and 50 ng per frog. At the highest dose, the average speed was doubled. The AVT antagonist significantly inhibited phonotaxis at both doses (50 and 100 ng). The effects of AVT on treefrog phonotaxis were shorter lived (disappearing within 60–90 min), compared to Manning compound (effects persisted at least 90 min). These findings support the hypothesis that endogenous AVT is critical to the display of female phonotaxis behavior. AVT may thus contribute to variability in female mate choices by modulating proceptive behaviors.

Keywords

Vasotocin Amphibian Phonotaxis Hyla versicolor Mate choice 

Notes

Acknowledgements

The author gratefully acknowledges the support of the National Science Foundation (IOS # 0725187, 1257777) and the helpful comments of two anonymous reviewers. All applicable national and institutional guidelines for the care and use of animals were followed.

Compliance with ethical standards

Conflict of interest

The author declares no conflicts of interest.

References

  1. Baran NM, Sklar NC, Adkins-Regan E (2016) Developmental effects of vasotocin and nonapeptide receptors on early social attachment and affiliative behavior in the zebra finch. Horm Behav 78:20–31.  https://doi.org/10.1016/j.yhbeh.2015.10.005 Google Scholar
  2. Baugh AT, Ryan MJ (2010a) Mate choice in response to dynamic presentation of male advertisement signals in tungara frogs. Anim Behav 79:145–152.  https://doi.org/10.1016/j.anbehav.2009.10.015 Google Scholar
  3. Baugh AT, Ryan MJ (2010b) Temporal updating during phonotaxis in male tungara frogs (Physalaemus pustulosus). Amphib Reptil 31:449–454.  https://doi.org/10.1163/017353710x518388 Google Scholar
  4. Baugh AT, Ryan MJ (2017) Vasotocin induces sexually dimorphic effects on acoustically-guided behavior in a tropical frog. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 203:265–273.  https://doi.org/10.1007/s00359-017-1155-y Google Scholar
  5. Beckers OM, Schul J (2004) Phonotaxis in Hyla versicolor (Anura, Hylidae): the effect of absolute call amplitude. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:869–876Google Scholar
  6. Bernal XE, Page RA, Rand AS, Ryan MJ (2007) Natural history miscellany—cues for eavesdroppers: do frog calls indicate prey density and quality? Am Nat 169:409–415Google Scholar
  7. Bosch J, Boyero L (2004) Reproductive stage and phonotactic preferences of female midwife toads (Alytes cisternasii). Behav Ecol Sociobiol 55:251–256Google Scholar
  8. Boyd SK (1991) Effect of vasotocin on locomotor activity in bullfrogs varies with developmental stage and sex. Horm Behav 25:57–69Google Scholar
  9. Boyd SK (1992) Sexual differences in hormonal control of release calls in bullfrogs. Horm Behav 26:522–535Google Scholar
  10. Boyd SK (1994a) Arginine vasotocin facilitation of advertisement calling and call phonotaxis in bullfrogs. Horm Behav 28:232–240Google Scholar
  11. Boyd SK (1994b) Gonadal steroid modulation of vasotocin concentrations in the bullfrog brain. Neuroendocrinol 60:150–156.  https://doi.org/10.1159/000126745 Google Scholar
  12. Boyd SK (1997) Brain vasotocin pathways and the control of sexual behaviors in the bullfrog. Brain Res Bull 44:345–350Google Scholar
  13. Boyd SK (2013) Amphibian neurohypophysial peptides Chapter 52. In: Kastin AJ (ed) Handbook of biologically active peptides, 2nd edn. Elsevier, Berlin, pp 371–375Google Scholar
  14. Boyd SK, Tyler CJ, De Vries GJ (1992) Sexual dimorphism in the vasotocin system of the bullfrog (Rana catesbeiana). J Comp Neurol 325:313–325.  https://doi.org/10.1002/cne.903250213 Google Scholar
  15. Brenowitz EA, Wilczynski W, Zakon HH (1984) Acoustic communication in spring peepers. Environmental and behavioral aspects. J Comp Physiol A 155:585–592Google Scholar
  16. Burmeister SS (2017) Neurobiology of female mate choice in frogs: auditory filtering and valuation. Integr Comp Biol 57:857–864.  https://doi.org/10.1093/icb/icx098 Google Scholar
  17. Bush SL, Gerhardt HC, Schul J (2002) Pattern recognition and call preferences in treefrogs (Anura: Hylidae): a quantitative analysis using a no-choice paradigm. Anim Behav 63:7–14Google Scholar
  18. Caldwell HK, Albers HE (2016) Oxytocin, vasopressin, and the motivational forces that drive social behaviors. In: Simpson EH, Balsam PD (eds) Behavioral Neuroscience of Motivation. Springer International Publishing, Cham, pp 51–103.  https://doi.org/10.1007/7854_2015_390 Google Scholar
  19. Campbell P, Ophir AG, Phelps SM (2009) Central vasopressin and oxytocin receptor distributions in two species of singing mice. J Comp Neurol 516:321–333.  https://doi.org/10.1002/cne.22116 Google Scholar
  20. Carnevali O, Mosconi G, Sabbieti MG, Murri CA, Vilani P, Polzonetti-Magni AM (1993) Some aspects of the reproductive biology of Rana esculenta at sea-level and montane habitats. Amphib Reptil 14:381–388Google Scholar
  21. Casseday JH, Covey E (1996) A neuroethological theory of the operation of the inferior colliculus. Brain Behav Evol 47:311–336Google Scholar
  22. Castellano S, Rosso A, Laoretti F, Doglio S, Giacoma C (2000) Call intensity and female preferences in the European green toad. Ethology 106:1129–1141Google Scholar
  23. Chakraborty M, Burmeister SS (2009) Estradiol induces sexual behavior in female tungara frogs. Horm Behav 55:106–112.  https://doi.org/10.1016/j.yhbeh.2008.09.001 Google Scholar
  24. Chakraborty M, Burmeister SS (2010) Sexually dimorphic androgen and estrogen receptor mRNA expression in the brain of tungara frogs. Horm Behav 58:619–627.  https://doi.org/10.1016/j.yhbeh.2010.06.013 Google Scholar
  25. Chakraborty M, Burmeister SS (2015) Effects of estradiol on neural responses to social signals in female tungara frogs. J Exp Biol 218:3671–3677.  https://doi.org/10.1242/jeb.127738 Google Scholar
  26. Cho HJ, Acharjee S, Moon MJ, Oh DY, Vaudry H, Kwon HB, Seong JY (2007) Molecular evolution of neuropeptide receptors with regard to maintaining high affinity to their authentic ligands. Gen Comp Endocrinol 153:98–107.  https://doi.org/10.1016/j.ygcen.2006.12.013 Google Scholar
  27. Collins EJ, McNamara JM, Ramsey DM (2006) Learning rules for optimal selection in a varying environment: mate choice revisited. Behav Ecol 17:799–809Google Scholar
  28. Dewan AK, Ramey ML, Tricas TC (2011) Arginine vasotocin neuronal phenotypes, telencephalic fiber varicosities, and social behavior in butterflyfishes (Chaetodontidae): potential similarities to birds and mammals. Horm Behav 59:56–66.  https://doi.org/10.1016/j.yhbeh.2010.10.002 Google Scholar
  29. Diakow C (1978) Hormonal basis for breeding behavior in female frogs—vasotocin inhibits release call of Rana pipiens. Science 199:1456–1457Google Scholar
  30. Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900–904.  https://doi.org/10.1126/science.1158668 Google Scholar
  31. 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 37:182–184Google Scholar
  32. 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 (Hyla versicolor). Behav Brain Res 145:63–77Google Scholar
  33. Fawcett TW, Johnstone RA (2003) Mate choice in the face of costly competition. Behav Ecol 14:771–779Google Scholar
  34. Feng AS, Lin WY (1991) Differential innervation patterns of 3 divisions of frog auditory midbrain (torus semicircularis). J Comp Neurol 306:613–630Google Scholar
  35. Figler RA, Mackenzie DS, Owens DW, Licht P, Amoss MS (1989) Increased levels of arginine vasotocin and neurophysin during nesting in sea turtles. Gen Comp Endocrinol 73:223–232.  https://doi.org/10.1016/0016-6480(89)90095-6 Google Scholar
  36. Forlano PM, Sisneros JA, Rohmann KN, Bass AH (2015) Neuroendocrine control of seasonal plasticity in the auditory and vocal systems of fish. Front Neuroendocrinol 37:129–145.  https://doi.org/10.1016/j.yfrne.2014.08.002 Google Scholar
  37. Gerhardt HC (1991) Female mate choice in treefrogs—static and dynamic acoustic criteria. Anim Behav 42:615–635Google Scholar
  38. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, ChicagoGoogle Scholar
  39. Gerhardt HC, Dyson ML, Tanner SD (1996) Dynamic properties of the advertisement calls of gray tree frogs: patterns of variability and female choice. Behav Ecol 7:7–18Google Scholar
  40. Gobbetti A, Zerani M (1992) A possible involvement of prostaglandin F2-alpha (PGF2-alpha) in Rana esculenta ovulation—effects of mammalian gonadotropin releasing hormone on in vitro PGF2-alpha and 17-beta-estradiol production from ovary and oviduct. Gen Comp Endocrinol 87:163–170.  https://doi.org/10.1016/0016-6480(92)90018-f Google Scholar
  41. Godwin J, Thompson R (2012) Nonapeptides and social behavior in fishes. Horm Behav 61:230–238.  https://doi.org/10.1016/j.yhbeh.2011.12.016 Google Scholar
  42. Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48:11–22Google Scholar
  43. Goodson JL (2008) Nonapeptides and the evolutionary patterning of sociality. In: Neumann ID, Landgraf R (eds) Advances in vasopressin and oxytocin: from genes to behaviour to disease, vol 170. Progress in Brain Research, pp 3–15.  https://doi.org/10.1016/s0079-6123(08)00401-9
  44. Goodson JL, Bass AH (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Rev 35:246–265Google Scholar
  45. Goodson JL, Kingsbury MA (2013) What’s in a name? Considerations of homologies and nomenclature for vertebrate social behavior networks. Horm Behav 64:103–112.  https://doi.org/10.1016/j.yhbeh.2013.05.006 Google Scholar
  46. Gordon NM, Gerhardt HC (2009) Hormonal modulation of phonotaxis and advertisement-call preferences in the gray treefrog (Hyla versicolor). Horm Behav 55:121–127Google Scholar
  47. Gordon NM, Hellman M (2015) Dispersal distance, gonadal steroid levels, and body condition in gray treefrogs (Hyla versicolor): seasonal and breeding night variation in females. J Herpetol 49:655–661.  https://doi.org/10.1670/13-119 Google Scholar
  48. Guerriero G, Ciarcia G (2001) Progesterone receptor: some viewpoints on hypothalamic seasonal fluctuations in a lower vertebrate. Brain Res Rev 37:172–177Google Scholar
  49. Guerriero G, Roselli CE, Paolucci M, Botte V, Ciarcia G (2000) Estrogen receptors and aromatase activity in the hypothalamus of the female frog, Rana esculenta. Fluctuations throughout the reproductive cycle. Brain Res 880:92–101Google Scholar
  50. Guillette LJ, Norris DO, Norman MF (1985) Response of amphibian (Ambystoma tigrinum) oviduct to arginine vasotocin and acetylcholine in vitro—influence of steroid hormone pretreatment in vivo. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 80:151–154.  https://doi.org/10.1016/0742-8413(85)90147-1 Google Scholar
  51. Hall IC, Woolley SMN, Kwong-Brown U, Kelley DB (2016) Sex differences and endocrine regulation of auditory-evoked, neural responses in African clawed frogs (Xenopus). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 202:17–34.  https://doi.org/10.1007/s00359-015-1049-9 Google Scholar
  52. Harvey LA, Propper CR, Woodley SK, Moore MC (1997) Reproductive endocrinology of the explosively breeding desert spadefoot toad, Scaphiopus couchii. Gen Comp Endocrinol 105:102–113Google Scholar
  53. Heller H, Ferreri E, Leathers DHG (1970) The effect of neurohypophysial hormones on the amphibian oviduct in vitro, with some remarks on the histology of this organ. J Endocrinol 47:495–509Google Scholar
  54. Hoke KL, Pitts NL (2012) Modulation of sensory-motor integration as a general mechanism for context dependence of behavior. Gen Comp Endocrinol 176:465–471.  https://doi.org/10.1016/j.ygcen.2012.02.014 Google Scholar
  55. Hoke KL, Burmeister SS, Fernald RD, Rand AS, Ryan MJ, Wilczynski W (2004) Functional mapping of the auditory midbrain during mate call reception. J Neurosci 24:11264–11272Google Scholar
  56. Hoke KL, Ryan MJ, Wilczynski W (2007) Integration of sensory and motor processing underlying social behaviour in tungara frogs. Proc R Soc B Biol Sci 274:641–649Google Scholar
  57. Hunt J, Brooks R, Jennions MD (2005) Female mate choice as a condition-dependent life-history trait. Am Nat 166:79–92Google Scholar
  58. Itoh MaI S (1990) Changes in plasma levels of gonadotropins and sex steroids in the toad, Bufo japonicus, in association with behavior during the breeding season. Gen Comp Endocrinol 80:451–464Google Scholar
  59. Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev Cambridge Philosophic Soc 72:283–327Google Scholar
  60. Jones RE, Guillette LJ (1982) Hormonal control of oviposition and parturition in lizards. Herpetologica 38:80–93Google Scholar
  61. Kelly AM, Goodson JL (2014) Social functions of individual vasopressin-oxytocin cell groups in vertebrates: what do we really know? Front Neuroendocrinol 35:512–529.  https://doi.org/10.1016/j.yfrne.2014.04.005 Google Scholar
  62. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38Google Scholar
  63. Kirkpatrick M, Rand AS, Ryan MJ (2006) Mate choice rules in animals. Anim Behav 71:1215–1225Google Scholar
  64. Kuczynski MC, Gering E, Getty T (2016) Context and condition dependent plasticity in sexual signaling in gray treefrogs. Behav Processes 124:74–79.  https://doi.org/10.1016/j.beproc.2015.11.020 Google Scholar
  65. Lea J, Halliday T, Dyson M (2000) Reproductive stage and history affect the phonotactic preferences of female midwife toads, Alytes muletensis. Anim Behav 60:423–427Google Scholar
  66. Leary CJ (2009) Hormones and acoustic communication in anuran amphibians. Integr Comp Biol 49:452–470.  https://doi.org/10.1093/icb/icp027 Google Scholar
  67. LeBlanc MM, Goode CT, MacDougall-Shackleton EA, Maney DL (2007) Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res 1171:93–103.  https://doi.org/10.1016/j.brainres.2007.06.086 Google Scholar
  68. Lowry CA, Richardson CF, Zoeller TR, Miller LJ, Muske LE, Moore FL (1997) Neuroanatomical distribution of vasotocin in a urodele amphibian (Taricha granulosa) revealed by immunohistochemical and in situ hybridization techniques. J Comp Neurol 385:43–70Google Scholar
  69. Lynch KS (2017) Understanding female receiver psychology in reproductive contexts. Integr Comp Biol 57:797–807.  https://doi.org/10.1093/icb/icx018 Google Scholar
  70. Lynch KS, Wilczynski W (2005) Gonadal steroids vary with reproductive stage in a tropically breeding female anuran. Gen Comp Endocrinol 143:51–56Google Scholar
  71. Lynch KS, Wilczynski W (2008) Reproductive hormones modify reception of species-typical communication signals in a female anuran. Brain Behav Evol 71:143–150.  https://doi.org/10.1159/000111460 Google Scholar
  72. Lynch KS, Rand AS, Ryan MJ, Wilczynski W (2005) Plasticity in female mate choice associated with changing reproductive states. Anim Behav 69:689–699Google Scholar
  73. Lynch KS, Crews D, Ryan MJ, Wilczynski W (2006) Hormonal state influences aspects of female mate choice in the tungara frog (Physalaemus pustulosus). Horm Behav 49:450–457Google Scholar
  74. Maney DL, Goode CT, Wingfield JC (1997) Intraventricular infusion of arginine vasotocin induces singing in a female songbird. J Neuroendocrinol 9:487–491Google Scholar
  75. Manning M et al (2012) Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J Neuroendocrinol 24:609–628.  https://doi.org/10.1111/j.1365-2826.2012.02303.x Google Scholar
  76. Marler CA, Boyd SK, Wilczynski W (1999) Forebrain arginine vasotocin correlates of alternative mating strategies in cricket frogs. Horm Behav 36:53–61Google Scholar
  77. Marshall VT, Humfeld SC, Bee MA (2003) Plasticity of aggressive signalling and its evolution in male spring peepers, Pseudacris crucifer. Anim Behav 65:1223–1234Google Scholar
  78. Medina MF, Ramos L, Crespo CA, Gonzalez-Calvar S, Fernandez SN (2004) Changes in serum sex steroid levels throughout the reproductive cycle of Bufo arenarum females. Gen Comp Endocrinol 136:143–151.  https://doi.org/10.1016/j.ygcen.2003.11.013 Google Scholar
  79. Miranda RA, Searcy BT, Propper CR (2015) Arginine vasotocin induces calling behavior with a female social stimulus and interacts with gonadotropins to affect sexual behaviors in male Xenopus tropicalis. Physiol Behav 151:72–80.  https://doi.org/10.1016/j.physbeh.2015.06.031 Google Scholar
  80. Moore FL, Boyd SK, Kelley DB (2005) Historical perspective: hormonal regulation of behaviors in amphibians. Horm Behav 48:373–383Google Scholar
  81. Oldfield RG, Harris RM, Hendrickson DA, Hofmann HA (2013) Arginine vasotocin and androgen pathways are associated with mating system variation in North American cichlid fishes. Horm Behav 64:44–52.  https://doi.org/10.1016/j.yhbeh.2013.04.006 Google Scholar
  82. Ondrasek NR (2016) Emerging frontiers in social neuroendocrinology and the study of nonapeptides. Ethology 122:443–455.  https://doi.org/10.1111/eth.12493 Google Scholar
  83. Page RA, Ryan MJ (2008) The effect of signal complexity on localization performance in bats that localize frog calls. Anim Behav 76:761–769.  https://doi.org/10.1016/j.anbehav.2008.05.006 Google Scholar
  84. Parris KM (2002) More bang for your buck: the effect of caller position, habitat and chorus noise on the efficiency of calling in the spring peeper. Ecol Model 156:213–224Google Scholar
  85. 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 Sens Neural Behav Physiol 170:73–82Google Scholar
  86. Petersen CL, Hurley LM (2017) Putting it in context: linking auditory processing with social behavior circuits in the vertebrate brain. Integr Comp Biol 57:865–877.  https://doi.org/10.1093/icb/icx055 Google Scholar
  87. Picker MD (1983) Hormonal induction of the aquatic phonotactic response of Xenopus. Behaviour 84:74–90Google Scholar
  88. Ramsey ME, Vu W, Cummings ME (2014) Testing synaptic plasticity in dynamic mate choice decisions: N-methyl d-aspartate receptor blockade disrupts female preference. Proc R Soc B Biol Sci.  https://doi.org/10.1098/rspb.2014.0047 Google Scholar
  89. Ross HE, Young LJ (2009) Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 30:534–547.  https://doi.org/10.1016/j.yfrne.2009.05.004 Google Scholar
  90. Rosso A, Castellano S, Giacoma C (2006) Preferences for call spectral properties in Hyla intermedia. Ethology 112:599–607Google Scholar
  91. Schmidt RS (1969) Preoptic activation of mating call orientation in female anurans. Behaviour 35:114–127Google Scholar
  92. Schwartz JJ, Buchanan BW, Gerhardt HC (2002) Acoustic interactions among male gray treefrogs, Hyla versicolor, in a chorus setting. Behav Ecol Sociobiol 53:9–19Google Scholar
  93. Searcy BT, Bradford CS, Thompson RR, Filtz TM, Moore FL (2011) Identification and characterization of mesotocin and V1a-like vasotocin receptors in a urodele amphibian, Taricha granulosa. Gen Comp Endocrinol 170:131–143.  https://doi.org/10.1016/j.ygcen.2010.09.017 Google Scholar
  94. Smeets W, Gonzalez A (2001) Vasotocin and mesotocin in the brains of amphibians: state of the art. Microsc Res Tech 54:125–136Google Scholar
  95. Sullivan BK, Hinshaw SH (1990) Variation in advertisement calls and male calling behavior in the spring peeper (Pseudacris crucifer). Copeia 1990:1146–1150Google Scholar
  96. Tito MB, Hoover MA, Mingo AM, Boyd SK (1999) Vasotocin maintains multiple call types in the gray treefrog, Hyla versicolor. Horm Behav 36:166–175Google Scholar
  97. Tripp SK, Moore FL (1988) Autoradiographic characterization of binding sites labeled with vasopressin in the brain of a urodele amphibian. Neuroendocrinol 48:87–92Google Scholar
  98. Vu M, Trudeau VL (2016) Neuroendocrine control of spawning in amphibians and its practical applications. Gen Comp Endocrinol 234:28–39.  https://doi.org/10.1016/j.ygcen.2016.03.024 Google Scholar
  99. Vu M, Weiler B, Trudeau VL (2017) Time- and dose-related effects of a gonadotropin-releasing hormone agonist and dopamine antagonist on reproduction in the Northern leopard frog (Lithobates pipiens). Gen Comp Endocrinol 254:86–96.  https://doi.org/10.1016/j.ygcen.2017.09.023 Google Scholar
  100. Wagner WE (1998) Measuring female mating preferences. Anim Behav 55:1029–1042Google Scholar
  101. Walkowiak W, Berlinger M, Schul J, Gerhardt HC (1999) Significance of forebrain structures in acoustically guided behavior in anurans. Eur J Morphol 37:177–181Google Scholar
  102. Wells KD (1977) The social behavior of anuran amphibians. Anim Behav 25:666–693Google Scholar
  103. Wells KD (2007) The ecology & behavior of amphibians. University of Chicago Press, ChicagoGoogle Scholar
  104. Wilczynski W, Burmeister SS (2016) Effects of steroid hormones on hearing and communication in frogs. In: Bass A, Sisneros JA, Popper AN, Fay R (eds) Hearing and hormones. Springer International Publishing, Switzerland, pp 53–75Google Scholar
  105. Wilczynski W, Capranica RR (1984) The auditory system of anuran amphibians. Prog Neurobiol 22:1–38.  https://doi.org/10.1016/0301-0082(84)90016-9 Google Scholar
  106. Wilczynski W, Endepols H (2006) Central auditory pathways in anuran amphibians: the anatomical basis of hearing and sound communication. In: Narins PM, Feng A, Fay R, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 221–249Google Scholar
  107. Wilczynski W, Lynch KS (2011) Female sexual arousal in amphibians. Horm Behav 59:630–636.  https://doi.org/10.1016/j.yhbeh.2010.08.015 Google Scholar
  108. Wilczynski W, Ryan MJ (2010) The behavioral neuroscience of anuran social signal processing. Curr Opin Neurobiol 20:754–763.  https://doi.org/10.1016/j.conb.2010.08.021 Google Scholar
  109. Wilczynski W, Rand AS, Ryan MJ (1999) Female preferences for temporal order of call components in the tungara frog: a Bayesian analysis. Anim Behav 58:841–851Google Scholar
  110. Wilczynski W, Lynch KS, O’Bryant EL (2005) Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology. Horm Behav 48:440–450Google Scholar
  111. Wilczynski W, Quispe M, Muñoz MI, Penna M (2017) Arginine vasotocin, the social neuropeptide of amphibians and reptiles. Front Endocrinol 8:1–17.  https://doi.org/10.3389/fendo.2017.00186 Google Scholar
  112. Witte K, Chen KC, Wilczynski W, Ryan MJ (2000) Influence of amplexus on phonotaxis in the cricket frog Acris crepitans blanchardi. Copeia 2000:257–261Google Scholar
  113. Witte K, Ryan MJ, Wilczynski W (2001) Changes in the frequency structure of a mating call decrease its attractiveness to females in the cricket frog Acris crepitans blanchardi. Ethology 107:685–699Google Scholar
  114. Zimmitti SJ (1999) Individual variation in morphological, physiological, and biochemical features associated with calling in spring peepers (Pseudacris crucifer). Physiol Biochem Zool 72:666–676Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA

Personalised recommendations