Calling behavior of males and females of a Bornean frog with male parental care and possible sex-role reversal

  • Johana Goyes Vallejos
  • T. Ulmar Grafe
  • Hanyrol H. Ahmad Sah
  • Kentwood D. Wells
Featured Student Research Paper

Abstract

In many species that use acoustic signals for mate attraction, males are usually the most vocal sex. In frogs, females typically remain silent, while males produce advertisement calls to attract mates. In some species, females vocalize, but usually as a response to an initial male advertisement call. The smooth guardian frog (Limnonectes palavanensis), found on Borneo, has exclusive paternal care while the females mate and desert after laying the clutch. Males provide care to the eggs until hatching and then they transport the tadpoles to small bodies of water. The vocal repertoire of this species has never been described. Males have a distinctive advertisement call to attract females, but produce the call very infrequently. We found that females of L. palavanensis not only respond to male advertisement calls but also vocalize spontaneously, forming lek-like aggregations around a single male. Males may or may not respond to a particular female with a short courtship call, which is elicited only by the female call and not the male advertisement call. The calling rate of females is consistently higher throughout the night compared with the calling rate of males. These observations suggest that this species exhibits a reversal in calling behavior and possibly a sex-role-reversed mating system.

Significance statement

Exceptional cases of species with a sex-role reversed mating system have been observed in fishes and birds, but not in frogs. For sex-role reversal to occur, there must be intense parental care by the males and a surplus of females. Additionally, females should exhibit characteristics that are usually observed in males in species with conventional sex roles. We found that in L. palavanensis, females are highly vocal, exhibiting higher calling rates compared with the calling rates of the males. This behavior, where females out-signal males has not been observed in anurans. This female calling behavior coupled with observations of several females approaching a male provides evidence of a female-biased operational sex ratio, a characteristic of a sex-role-reversed mating system. Thus, this study provides quantitative evidence that L. palavanensis exhibits various aspects consistent with a sex-role reversed mating system.

Keywords

Female calling Frogs Sex-role reversal Vocal behavior Calling rate Limnonectes palavanensis 

Supplementary material

265_2017_2323_MOESM1_ESM.mp4 (39.9 mb)
ESM 1(MP4 40905 kb)

References

  1. Andersson M (1995) Evolution of reversed sex roles, sexual size dimorphism, and mating system in coucals (Centropodidae, Aves). Biol J Linn Soc 54:173–181CrossRefGoogle Scholar
  2. Bee MA, Suyesh R, Biju SD (2013) Vocal behavior of the Ponmudi bush frog (Raorchestes graminirupes): repertoire and individual variation. Herpetologica 69:22–35CrossRefGoogle Scholar
  3. Berglund A (1995) Many mates make male pipefish choosy. Behaviour 132:213–218CrossRefGoogle Scholar
  4. Berglund A, Rosenqvist G (1993) Selective males and ardent females in pipefishes. Behav Ecol Sociobiol 32:331–336Google Scholar
  5. Boistel R, Sueur J (1997) Comportement sonore de la femelle de Platymantis vitiensis (Amphibia, Anura) en l’absence du mâle. CR Acad Sci Sci III-Vie 320:933–941Google Scholar
  6. Boistel R, Sueur J (2002) XVIIth symposium of the international bioacoustic council—abstracts. Bioacoustics 13:77–102CrossRefGoogle Scholar
  7. Bosch J (2001) Female reciprocal calling in the Iberian midwife toad (Alytes cisternasii) varies with male call rate and dominant frequency: implications for sexual selection. Naturwissenschaften 88:434–438CrossRefGoogle Scholar
  8. Bush SL (1996) Why is double clutching rare in the Majorcan midwife toad? Anim Behav 52:913–922CrossRefGoogle Scholar
  9. Bush SL (1997) Vocal behavior of males and females in the Majorcan midwife toad. J Herpetol 31:251–257CrossRefGoogle Scholar
  10. Bush SL, Bell DJ (1997) Courtship and female competition in the Majorcan midwife toad, Alytes muletensis. Ethology 103:292–303CrossRefGoogle Scholar
  11. Bush SL, Dyson ML, Halliday TR (1996) Selective phonotaxis by males in the Majorcan midwife toad. Proc R Soc Lond B 263:913–917CrossRefGoogle Scholar
  12. Cooley JR, Marshall DC (2001) Sexual signaling in periodical cicadas, Magicicada spp. (Hemiptera: Cicadidae). Behaviour 138:827–855CrossRefGoogle Scholar
  13. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
  14. Ekstrom JMM, Burke T, Randrianaina L, Birkhead TR (2007) Unusual sex roles in a highly promiscuous parrot: the greater vasa parrot Caracopsis vasa. Ibis 149:313–320CrossRefGoogle Scholar
  15. Emerson SB (1992) Courtship and nest-building behavior of a Bornean frog, Rana blythii. Copeia 1992:1123–1127CrossRefGoogle Scholar
  16. Emerson SB, Inger RF, Iskandar DT (2000) Molecular systematics and biogeography of the fanged frogs of Southeast Asia. Mol Phylogenet Evol 16:131–142CrossRefPubMedGoogle Scholar
  17. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefPubMedGoogle Scholar
  18. Emlen ST, Wrege PH, Webster MS (1998) Cuckoldry as a cost of polyandry in the sex-role reversed jacana, Jacana jacana. Proc R Soc Lond B 265:2359–2364CrossRefGoogle Scholar
  19. Geberzahn N, Goymann W, Muck C, ten Cate C (2009) Females alter their song when challenged in a sex-role reversed bird species. Behav Ecol Sociobiol 64:193–204CrossRefPubMedPubMedCentralGoogle Scholar
  20. Geberzahn N, Goymann W, ten Cate C (2010) Threat signaling in female song—evidence from playbacks in a sex-role reversed bird species. Behav Ecol 21:1147–1155CrossRefGoogle Scholar
  21. Gerhardt HC (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615–635CrossRefGoogle Scholar
  22. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. The University of Chicago Press, ChicagoGoogle Scholar
  23. Given MF (1993) Male response to female vocalization in the carpenter frog, Rana virgatipes. Herpetologica 44:304–317Google Scholar
  24. Goyes Vallejos J (2016) Parental care and acoustic communication of the smooth guardian frog Limnonectes palavanensis, a Bornean frog with possible sex-role reversal. PhD Dissertation, University of ConnecticutGoogle Scholar
  25. Goymann W, Wittenzellner A, Wingfield J (2004) Competing females and caring males. Sex-role reversal in African black coucals, Centropus grillii. Anim Behav 68:733–740CrossRefGoogle Scholar
  26. Grafe TU, Bitz JH (2004) Functions of duetting in the tropical boubou, Laniarius aethiopicus: territorial defence and mutual mate guarding. Anim Behav 68:193–201CrossRefGoogle Scholar
  27. Hauselberger KF, Alford RA (2005) Effects of season and weather on calling in the Australian microhylid frog Austrochaperina robusta. Herpetologica 61:349–363CrossRefGoogle Scholar
  28. Illes AE, Yunes-Jimenez L (2009) A female songbird out-sings male conspecifics during simulated territorial intrusions. Proc R Soc Lond B 276:981–986CrossRefGoogle Scholar
  29. Inger RF, Voris HK (1988) Taxonomic status and reproductive biology of Bornean tadpole-carrying frogs. Copeia 1988:1060–1061CrossRefGoogle Scholar
  30. Inger RF, Voris HK, Walker P (1986) Larval transport in a Bornean ranid frog. Copeia 1986:523–525CrossRefGoogle Scholar
  31. Judge KA, Swanson SJ, Brooks RJ (2000) Rana catesbeiana (Bullfrog): female vocalization. Herpetol Rev 31:236–237Google Scholar
  32. Kaefer IL, Montanarin A, da Costa RS, Lima AP (2012) Temporal patterns of reproductive activity and site attachment of the brilliant-thighed frog Allobates femoralis from Central Amazonia. J Herpetol 46:549–554CrossRefGoogle Scholar
  33. Kokko H, Jennions MD (2008) Parental investment, sexual selection, and sex ratios. J Evol Biol 21:919–948CrossRefPubMedGoogle Scholar
  34. Krishna S, Krishna S (2005) Female courtship calls of the litter frog (Rana curtipes) in the tropical forests of Western Ghats, South India. Amphibia-Reptilia 26:431–435CrossRefGoogle Scholar
  35. Marquez R, Verrell PA (1991) The courtship and mating of the Iberian midwife toad Alytes cisternasii (Amphibia: Anura: Discoglossidae). J Zool 225:125–139CrossRefGoogle Scholar
  36. Matsui M (1995) Calls produced by a “voiceless” frog, Rana blythi Boulenger 1920, from Peninsular Malaysia (Amphibia, Anura). Trop Zool 8:325–331CrossRefGoogle Scholar
  37. Monteiro N, Carneiro D, Antunes A, Queiroz N, Vieira M, Jones A (2017) The lek mating system of the worm pipefish (Nerophis lumbriciformis): a molecular maternity analysis and test of the phenotype-linked fertility hypothesis. Mol Ecol 26:1371–1385CrossRefPubMedGoogle Scholar
  38. Orlov NL (1997) Breeding behavior and nest construction in a Vietnam frog related to Rana blythi. Copeia 1997:464–465CrossRefGoogle Scholar
  39. Pettitt BA, Bourne GR, Bee MA (2013) Advertisement call variation in the golden rocket frog (Anomaloglossus beebei): evidence for individual distinctiveness. Ethology 119:244–256CrossRefGoogle Scholar
  40. Price JJ, Yunes-Jimenez L, Osorio-Beristain M (2008) Sex-role reversal in song? Females sing more frequently than males in the streak-backed oriole. Condor 110:387–392CrossRefGoogle Scholar
  41. Price JJ, Lanyon SM, Omland KE (2009) Losses of female song with changes from tropical to temperate breeding in the New World blackbirds. Proc R Soc Lond B 276:1971–1980CrossRefGoogle Scholar
  42. Rebar D, Bailey NW, Zuk M (2009) Courtship song’s role during female mate choice in the field cricket Teleogryllus oceanicus. Behav Ecol 20:1307–1314CrossRefGoogle Scholar
  43. Rodríguez RL, Sullivan LE, Cocroft RB (2004) Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evolution 58:571–578CrossRefPubMedGoogle Scholar
  44. Roithmair ME (1994) Male territoriality and female mate selection in the dart-poison frog Epipedobates trivittatus (Dendrobatidae, Anura). Copeia 1994:107–115CrossRefGoogle Scholar
  45. Rowley JJL, Le DTT, Hoang HD, Altig R (2014) The breeding behaviour, advertisement call and tadpole of Limnonectes dabanus (Anura: Dicroglossidae). Zootaxa 3881:195–200CrossRefPubMedGoogle Scholar
  46. Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton, NJGoogle Scholar
  47. Shen JX, Feng AS, Xu ZM, Yu ZL, Arch VS, Yu XJ, Narins PM (2008) Ultrasonic frogs show hyperacute phonotaxis to female courtship calls. Nature 453:914–916CrossRefPubMedGoogle Scholar
  48. Slater PJB, Mann NI (2004) Why do the females of many bird species sing in the tropics? J Avian Biol 35:289–294CrossRefGoogle Scholar
  49. Smith RL (1979) Paternity assurance and altered roles in the mating behaviour of a giant water bug, Abedus herberti (Heteroptera: Belostomatidae). Anim Behav 27:716–725CrossRefGoogle Scholar
  50. Summers K (1989) Sexual selection and intra-female competition in the green poison-dart frog, Dendrobates auratus. Anim Behav 37:797–805CrossRefGoogle Scholar
  51. Suthers RA, Narins PM, Lin WY, Schnitzler HU, Denzinger A, Xu CH, Feng AS (2006) Voices of the dead: complex nonlinear vocal signals from the larynx of an ultrasonic frog. J Exp Biol 209:4984–4993CrossRefPubMedGoogle Scholar
  52. Tobias ML, Viswanathan SS, Kelley DB (1998) Rapping in the African clawed frog Xenopus laevis. P Natl Acad Sci USA 95:1870–1875CrossRefGoogle Scholar
  53. Toledo LF, Martins IA, Bruschi DP, Passos MA, Alexandre C, Haddad CFB (2014) The anuran calling repertoire in the light of social context. Acta Ethol 18:87–99CrossRefGoogle Scholar
  54. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine-Atherton, Chicago, pp 136–179Google Scholar
  55. Ursprung E, Ringler M, Jehle R, Hödl W (2011) Strong male/male competition allows for nonchoosy females: high levels of polygynandry in a territorial frog with paternal care. Mol Ecol 20:1759–1771CrossRefPubMedGoogle Scholar
  56. Vincent ACJ (1992) Prospects for sex role reversal in teleost fishes. Neth J Zool 42:392–399CrossRefGoogle Scholar
  57. Wagner WE Jr, Reiser MG (2000) The importance of calling song and courtship song in female mate choice in the variable cricket. Anim Behav 59:1219–1226CrossRefPubMedGoogle Scholar
  58. Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693CrossRefGoogle Scholar
  59. Wells KD (1978) Courtship and parental behavior in a Panamanian poison-arrow frog, Dendrobates auratus. Herpetologica 34:148–155Google Scholar
  60. Wells KD (1980) Social behavior and communication of a dendrobatid frog (Colostethus trinitatis). Herpetologica 36:189–199Google Scholar
  61. Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  62. Wells MM, Henry CS (1992) The role of courtship songs in reproductive isolation among populations of green lacewings of the genus Chrysoperla (Neuroptera: Chrysopidae). Evolution 46:31–42CrossRefPubMedGoogle Scholar
  63. Wells KD, Taigen TL (1986) The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor). Behav Ecol Sociobiol 19:9–18CrossRefGoogle Scholar
  64. Zimmerman BL, Bogart JP (1984) Vocalizations of primary forest frog species in the Central Amazon. Acta Amaz 14:473–519CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA
  2. 2.Department of Biology, Faculty of ScienceUniversiti Brunei DarussalamGadongBrunei Darussalam

Personalised recommendations