Abstract
The ability to respond to competition is critical for social behaviors involved in mating, territoriality and foraging. Physiological mechanisms of competitive social behaviors may determine not only baseline behavior, but possibly also the plasticity of the response to competition. We examined the effects of the neuropeptide arginine vasotocin (AVT), which is implicated in social behavior in non-mammalian vertebrates, on both spontaneous acoustic advertisement calling behavior and the plastic response to a simulated competitive challenge in Cope’s gray treefrogs, Hyla chrysoscelis. We injected males either with AVT or a saline control and then analyzed recordings of spontaneous calling prior to playback, playback of average advertisement calls, playback of highly competitive advertisement calls, and spontaneous calling after playback. We found a tendency for AVT-treated males to be more likely to resume calling, and AVT males had higher call rates than control males, although they did not differ in pulse number or call effort. There were no differences between the AVT and control treatments in the plasticity of calling behavior in response to simulated competitors. Our results generally align with other studies on how AVT affects anuran vocalizations, and suggest that its primary effect is on motivation to call, with less of an effect on plasticity in response to competition. Nevertheless, these effects on call motivation are significant, because mating success is often determined more by participation in the chorus than by the values of specific call characteristics.
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References
Akre KL, Farris HE, Lea AM et al (2011) Signal perception in frogs and bats and the evolution of mating signals. Science 333:751–752. https://doi.org/10.1126/science.1205623
Albers HE (2012) The regulation of social recognition, social communication and aggression: vasopressin in the social behavior neural network. Horm Behav 61:283–292. https://doi.org/10.1016/j.yhbeh.2011.10.007
Balment RJ, Lu W, Weybourne E, Warne JM (2006) Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol 147:9–16. https://doi.org/10.1016/j.ygcen.2005.12.022
Baran NM (2017) Sensitive periods, vasotocin-family peptides, and the evolution and development of social behavior. Front Endocrinol. https://doi.org/10.3389/fendo.2017.00189
Bates D, Maechler M, Bolker BM, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bell AM (2020) Individual variation and the challenge hypothesis. Horm Behav 123:104549. https://doi.org/10.1016/j.yhbeh.2019.06.013
Blumstein DT, Ebensperger LA, Hayes LD et al (2010) Toward an integrative understanding of social behavior: new models and new opportunities. Front Behav Neurosci 4:34. https://doi.org/10.3389/fnbeh.2010.00034
Booker WW, Gerhardt HC, Lemmon AR et al (2020) The complex history of genome duplication and hybridization in North American gray treefrogs. bioRxiv. https://doi.org/10.1101/2020.11.25.398461
Boyd SK (1994) Arginine vasotocin facilitation of advertisement calling and call phonotaxis in bullfrogs. Horm Behav 28:232–240
Boyd SK (2013) Vasotocin modulation of social behaviors in amphibians. In: Choleris E, Pfaff DW, Kavaliers M (eds) Oxytocin, vasopressin and related peptides in the regulation of behavior. Cambridge University Press, Cambridge, pp 97–109
Bretman A, Gage MJG, Chapman T (2011) Quick-change artists: male plastic behavioural responses to rivals. Trends Ecol Evol 26:467–473. https://doi.org/10.1016/j.tree.2011.05.002
Briffa M, Sneddon LU (2007) Physiological constraints on contest behaviour. Funct Ecol 21:627–637. https://doi.org/10.1111/j.1365-2435.2006.01188.x
Burmeister SS, Wilczynski W (2001) Social context influences androgenic effects on calling in the green treefrog (Hyla cinerea). Horm Behav 40:550–558
Burmeister S, Somes C, Wilczynski W (2001) Behavioral and hormonal effects of exogenous vasotocin and corticosterone in the green treefrog. Gen Comp Endocrinol 122:189–197. https://doi.org/10.1006/gcen.2001.7625
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 34:248–261
Delville Y, Mansour KM, Ferris CF (1996) Testosterone facilitates aggression by modulating vasopressin receptors in the hypothalamus. Physiol Behav 60:25–29. https://doi.org/10.1016/0031-9384(95)02246-5
Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900–904. https://doi.org/10.1126/science.1158668
Dunham LA, Wilczynski W (2014) Arginine vasotocin, steroid hormones and social behavior in the green anole lizard (Anolis carolinensis). J Exp Biol 217:3670–3676. https://doi.org/10.1242/jeb.107854
Gayou DC (1984) Effects of temperature on the mating call of Hyla versicolor. Copeia 1984:733–738. https://doi.org/10.2307/1445157
Gerhardt HC (1975) Sound pressure levels and radiation patterns of the vocalizations of some North American frogs and toads. J Comp Physiol A 102:1–12
Gerhardt HC (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615–635
Gerhardt HC (2005) Advertisement-call preferences in diploid-tetraploid treefrogs (Hyla chrysoscelis and Hyla versicolor): Implications for mate choice and the evolution of communication systems. Evolution 59:395–408
Gerhardt HC, Brooks R (2009) Experimental analysis of multivariate female choice in gray treefrogs (Hyla versicolor): evidence for directional and stabilizing selection. Evolution 63:2504–2512
Gerhardt HC, Daniel RE, Perrill SA, Schramm S (1987) Mating behaviour and male mating success in the green treefrog. Anim Behav 35:1490–1503
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 7:7–18. https://doi.org/10.1093/beheco/7.1.7
Given MF (2002) Interrelationships among calling effort, growth rate, and chorus tenure in Bufo fowleri. Copeia 2002:979–987
Goodson JL (1998) Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm Behav 34:67–77
Goodson JL, Adkins-Regan E (1999) Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J Neuroendocrinol 11:19–25. https://doi.org/10.1046/j.1365-2826.1999.00284.x
Goodson JL, Bass AH (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Rev 35:246–265
Hau M, Goymann W (2015) Endocrine mechanisms, behavioral phenotypes and plasticity: known relationships and open questions. Front Zool 12:S7. https://doi.org/10.1186/1742-9994-12-S1-S7
Heimovics SA, Ferris JK, Soma KK (2015) Non-invasive administration of 17β-estradiol rapidly increases aggressive behavior in non-breeding, but not breeding, male song sparrows. Horm Behav 69:31–38. https://doi.org/10.1016/j.yhbeh.2014.11.012
Insel TR, Young LJ (2000) Neuropeptides and the evolution of social behavior. Curr Opin Neurobiol 10:784–789. https://doi.org/10.1016/S0959-4388(00)00146-X
Kelly AM, Wilson LC (2020) Aggression: Perspectives from social and systems neuroscience. Horm Behav 123:104523. https://doi.org/10.1016/j.yhbeh.2019.04.010
Kelly AM, Vitousek MN, Kelly AM (2017) Dynamic modulation of sociality and aggression: an examination of plasticity within endocrine and neuroendocrine systems. Philos Trans R Soc B 372:20160243
Kime NM, Whitney TK, Davis ES, Marler CA (2007) Arginine vasotocin promotes calling behavior and call changes in male túngara frogs. Brain Behav Evol 69:254–265. https://doi.org/10.1159/000099613
Kime NM, Whitney TK, Ryan MJ et al (2010) Treatment with arginine vasotocin alters mating calls and decreases call attractiveness in male túngara frogs. Gen Comp Endocrinol 165:221–228. https://doi.org/10.1016/j.ygcen.2009.06.023
Klomberg KF, Marler CA (2000) The neuropeptide arginine vasotocin alters male call characteristics involved in social interactions in the grey treefrog, Hyla versicolor. Anim Behav 59:807–812
Klump GM, Gerhardt HC (1987) Use of non-arbitrary acoustic criteria in mate choice by female gray tree frogs. Nature 326:286–288. https://doi.org/10.1038/326286a0
Leary CJ (2009) Hormones and acoustic communication in anuran amphibians. Integr Comp Biol 49:452–470. https://doi.org/10.1093/icb/icp027
Leary CJ, Harris S (2013) Steroid hormone levels in calling males and males practicing alternative non-calling mating tactics in the green treefrog, Hyla cinerea. Horm Behav 63:20–24. https://doi.org/10.1016/j.yhbeh.2012.11.006
Lessells CM (2008) Neuroendocrine control of life histories: What do we need to know to understand the evolution of phenotypic plasticity? Philos Trans R Soc B Biol Sci 363:1589–1598. https://doi.org/10.1098/rstb.2007.0008
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 29:554–570
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
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 26:156–166. https://doi.org/10.1016/0018-506X(92)90039-X
Mougeot F, Dawson A, Redpath SM, Leckie F (2005) Testosterone and autumn territorial behavior in male red grouse Lagopus lagopus scoticus. Horm Behav 47:576–584. https://doi.org/10.1016/j.yhbeh.2004.11.021
Murphy CG (1994) Chorus tenure of male barking treefrogs, Hyla gratiosa. Anim Behav 48:763–777
Niemelä PT, Dingemanse NJ (2018) Meta-analysis reveals weak associations between intrinsic state and personality. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.2823
O’Bryant EL, Wilczynski W (2010) Changes in plasma testosterone levels and brain AVT cell number during the breeding season in the green treefrog. Brain Behav Evol 75:271–281
Oliveira RF (2004) Social modulation of androgens in vertebrates: mechanisms and function. Advances in the study of behavior. Academic Press, Cambridge, pp 165–239
Oliveira RF (2009) Social behavior in context: Hormonal modulation of behavioral plasticity and social competence. Integr Comp Biol 49:423–440. https://doi.org/10.1093/icb/icp055
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 170:73–82
R Development Core Team (2021) R: a language and environment for statistical computing
Reichert MS, Gerhardt HC (2012) Trade-offs and upper limits to signal performance during close-range vocal competition in gray tree frogs Hyla versicolor. Am Nat 180:425–437. https://doi.org/10.1086/667575
Reichert MS, Gerhardt HC (2014) Behavioral strategies and signaling in interspecific aggressive interactions in gray tree frogs. Behav Ecol 25:520–530. https://doi.org/10.1093/beheco/aru016
Remage-Healey L, Bass AH (2005) Rapid elevations in both steroid hormones and vocal signaling during playback challenge: a field experiment in Gulf toadfish. Horm Behav 47:297–305. https://doi.org/10.1016/j.yhbeh.2004.11.017
Ritke M, Semlitsch R (1991) Mating behavior and determinants of male mating success in the gray treefrog, Hyla chrysoscelis. Can J Zool 69:246–250. https://doi.org/10.1139/z91-037
Ritke ME, Babb JG, Ritke MK (1992) Temporal patterns of reproductive activity in the gray treefrog (Hyla chrysoscelis). J Herpetol 26:107–111
Ruuskanen S, Laaksonen T (2010) Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca). Horm Behav 57:119–127. https://doi.org/10.1016/j.yhbeh.2009.09.017
Santangelo N, Bass AH (2006) New insights into neuropeptide modulation of aggression: Field studies of arginine vasotocin in a territorial tropical damselfish. Proc R Soc B Biol Sci 273:3085–3092. https://doi.org/10.1098/rspb.2006.3683
Schwartz JJ (2001) Call monitoring and interactive playback systems in the study of acoustic interactions among male anurans. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, pp 183–204
Schwartz JJ, Bee MA (2013) Anuran acoustic signal production in noisy environments. In: Brumm H (ed) Animal communication and noise. Springer, Heidelberg, pp 91–132
Schwartz JJ, Buchanan BW, Gerhardt HC (2001) Female mate choice in the gray treefrog (Hyla versicolor) in three experimental environments. Behav Ecol Sociobiol 49:443–455. https://doi.org/10.1007/s002650100317
Schwartz JJ, Buchanan B, Gerhardt HC (2002) Acoustic interactions among male gray treefrogs, Hyla versicolor, in a chorus setting. Behav Ecol Sociobiol 53:9–19. https://doi.org/10.1007/s00265-002-0542-7
Semsar K, Klomberg KF, Marler CA (1998) Arginine vasotocin increases calling-site acquisition by nonresident male grey treefrogs. Anim Behav 56:983–987
Sih A, Mathot KJ, Moirón M et al (2015) Animal personality and state–behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50–60. https://doi.org/10.1016/j.tree.2014.11.004
Snell-Rood EC (2013) An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav 85:1004–1011. https://doi.org/10.1016/j.anbehav.2012.12.031
Sullivan BK, Hinshaw SH (1992) Female choice and selection on male calling behaviour in the grey treefrog Hyla versicolor. Anim Behav 44:733–744
Taff CC, Vitousek MN (2016) Endocrine flexibility: optimizing phenotypes in a dynamic world? Trends Ecol Evol 31:476–488. https://doi.org/10.1016/j.tree.2016.03.005
Tanner JC, Ward JL, Shaw RG, Bee MA (2017) Multivariate phenotypic selection on a complex sexual signal. Evolution 71:1742–1754. https://doi.org/10.1111/evo.13264
Ten Eyck GR (2005) Arginine vasotocin activates advertisement calling and movement in the territorial Puerto Rican frog, Eleutherodactylus coqui. Horm Behav 47:223–229
Tito MB, Hoover MA, Mingo AM, Boyd SK (1999) Vasotocin maintains multiple call types in the gray treefrog, Hyla versicolor. Horm Behav 36:166–175
Trainor B, Rouse K, Marler CA (2003) Arginine vasotocin interacts with the social environment to regulate advertisement calling in the gray treefrog (Hyla versicolor). Brain Behav Evol 61:165–171
Veenit V, Cordero MI, Tzanoulinou S, Sandi C (2013) Increased corticosterone in peripubertal rats leads to long-lasting alterations in social exploration and aggression. Front Behav Neurosci 7:26. https://doi.org/10.3389/fnbeh.2013.00026
Ward JL, Love EK, Vélez A et al (2013) Multitasking males and multiplicative females: dynamic signalling and receiver preferences in Cope’s grey treefrog. Anim Behav 86:231–243. https://doi.org/10.1016/j.anbehav.2013.05.016
Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693. https://doi.org/10.1016/0003-3472(77)90118-X
Wells KD, Schwartz JJ (2007) The behavioral ecology of anuran communication. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer-Verlag, New York, pp 44–86
Wells KD, Taigen TL (1986) The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor). Behav Ecol Sociobiol 19:9–18. https://doi.org/10.1007/BF00303837
Wilczynski W, Quispe M, Muñoz MI, Penna M (2017) Arginine vasotocin, the social neuropeptide of amphibians and reptiles. Front Endocrinol 8:186. https://doi.org/10.3389/fendo.2017.00186
Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The challenge hypothesis - theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846
Wingfield JC, Goymann W, Jalabert C, Soma KK (2019) Concepts derived from the challenge hypothesis. Horm Behav 115:104550. https://doi.org/10.1016/j.yhbeh.2019.06.014
Young LJ, Wang Z, Cooper TT, Albers HE (2000) Vasopressin (V1a) receptor binding, mRNA expression and transcriptional regulation by androgen in the Syrian hamster brain. J Neuroendocrinol 12:1179–1185. https://doi.org/10.1046/j.1365-2826.2000.00573.x
Acknowledgements
We thank James Erdmann, A.J. Hager and Cheyenne Smith for assistance capturing and measuring frogs. Two anonymous reviewers made helpful comments on a previous version of this manuscript.
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This work was supported by a grant from the Lew Wentz Foundation to N.C.
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All procedures were approved by the IACUC of Oklahoma State University (protocol number AS-19-4), and were conducted with the permission of the Oklahoma Department of Wildlife Conservation.
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Clapp, N., Reichert, M.S. Arginine vasotocin affects motivation to call, but not calling plasticity, in Cope’s gray treefrog Hyla chrysoscelis. J Comp Physiol B 192, 115–125 (2022). https://doi.org/10.1007/s00360-021-01399-1
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DOI: https://doi.org/10.1007/s00360-021-01399-1