Skip to main content
Log in

Neotropical dancing frog: the rich repertoire of visual displays in a hylodine species

  • Article
  • Published:
Journal of Ethology Aims and scope Submit manuscript

Abstract

During reproductive season, males usually must defend their territory against competitor males and attract females for reproduction. Acoustic signals evolved as an alternative to physical attacks, thus reducing injuries to both opponents during a territorial dispute, but they are also the primarily trait used by female frogs to select males. However, there is some recent evidence that visual signalling also can be important during social interactions in frogs. Here, for the first time, we describe the sophisticated visual behaviour of Hylodes meridionalis, a diurnal species that is endemic to the southern Atlantic Forest, where it inhabits fast streams. We submitted resident males to mirror self-image presentations to simulate the presence of an intruder male in their territories. Furthermore, we collected observations from close-range interactions between individuals of this very shy species. We observed seven types of visual displays: toe flagging (slow up-and-down movements of one or more toes), arm lifting (rapid up-and-down movements of one arm), leg lifting (rapid up-and-down movements of one leg), arm waving (lifting an arm and waving it in an arc), both legs kicking (rapidly stretching both hind limbs towards the back), foot flagging (slowly raising one hind limb in a semi-arch movement) and throat display (pulsation of one or both paired lateral vocal sacs without sound production). Only the kicking of both legs was displayed exclusively by females; toe flagging and foot flagging were displayed by males only during agonistic interactions. The frequency of visual displays (7 types, 117 events) was much greater than that of acoustic signals (3 types, 66 events). Our data demonstrate that the visual repertoire of the genus Hylodes is richer than previously noted and that visual display behaviour in anurans could be more common than previously believed. Therefore, this characterisation study aids our understanding of the function of the rich repertoire of visual displays in frog species and highlights that ethologists should be directing more of their attention towards this poorly explored anuran behaviour.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amézquita A, Hödl W (2004) How, when, and where to perform visual displays: the case of the Amazonian frog Hyla parviceps. Herpetologica 60:420–429

    Article  Google Scholar 

  • Backes A, Prates FL, Viola MG (2005) Produção de serapilheira em Floresta Ombrófila Mista, em São Francisco de Paula, Rio Grande do Sul, Brasil. Acta Bot Bras 19(1):155–160

    Article  Google Scholar 

  • Biju SD, Garg S, Gururaja KV, Shouche Y, Walujkar SA (2014) DNA barcoding reveals unprecedented diversity in dancing frogs of India (Micrixalidae, Micrixalus): a taxonomic revision with description of 14 new species. Ceylon J Sci (Biol Sci) 43:37–123

    Article  Google Scholar 

  • Caldart VM, Iop S, Cechin SZ (2014) Social interactions in a neotropical stream frog reveal a complex repertoire of visual signals and the use of multimodal communication. Behaviour 151:719–739

    Article  Google Scholar 

  • de Sá FP, Zina J, Haddad CFB (2016) Sophisticated communication in the Brazilian torrent frog Hylodes japi. PLoS One 11(1):e0145444

    Article  Google Scholar 

  • Elias-Costa AJ, Montesinos R, Grant T, Faivovich J (2017) The vocal sac of Hylodidae (Amphibia, Anura): phylogenetic and functional implications of a unique morphology. J Morphol 278(11):1506–1516

    Article  Google Scholar 

  • Ferreira PMA, Eggers L (2008) Espécies de Cyperaceae do Centro de Pesquisa e Conservação da Natureza Pró-Mata, Município de São Francisco de Paula, RS, Brasil. Acta Bot Bras 22:173–185

    Article  Google Scholar 

  • Fite KV (1973) The visual fields of the frog and toad: a comparative study. Behav Biol 9:707–718

    Article  CAS  Google Scholar 

  • Forti LR, Castanho LM (2012) Behavioural repertoire and a new geographical record of the torrent frog Hylodes cardosoi (Anura: Hylodidae). Herpetol Bull 121:17–22

    Google Scholar 

  • Frost DR (2019) Amphibian species of the world 6.0: an online reference. American Museum of Natural History, New York. http://research.amnh.org/vz/herpetology/amphibia. Accessed 20 Feb 2019

  • Furtado R, Nomura F (2014) Visual signals or displacement activities? The function of visual displays in agonistic interactions in nocturnal tree frogs. Acta Ethol 17:9–14

    Article  Google Scholar 

  • Furtado R, Márquez R, Hartz SM (2017) In front of a mirror: visual displays may not be aggressive signals in nocturnal tree frogs. J Nat Hist 51(7–8):443–454

    Article  Google Scholar 

  • Grafe TU, Tony JA (2017) Temporal variation in acoustic and visual signalling as a function of stream background noise in the Bornean foot-flagging frog, Staurois parvus. J Ecoacoust 1:#X74QE0

    Article  Google Scholar 

  • Haddad CFB, Giaretta AA (1999) Visual and acoustic communication in the Brazilian torrent frog, Hylodes asper (Anura: Leptodactylidae). Herpetologica 55(3):324–333

    Google Scholar 

  • Haddad CFB, Toledo LF, Prado CPA (2008) Anfíbios da Mata Atlântica: guia dos anfíbios anuros da Mata Atlântica/Guide for the Atlantic Forest anurans. Editora Neotropica, São Paulo

    Google Scholar 

  • Hartmann MT, Giasson LOM, Hartmann PA, Haddad CFB (2005) Visual communication in Brazilian species of anurans from the Atlantic Forest. J Nat Hist 39(19):1675–1685

    Article  Google Scholar 

  • Heyer WR, Rand AS, Cruz CAG, Peixoto OL, Nelson CE (1990) Frogs of Boracéia. Arq Zool S Paulo 31(4):231–410

    Google Scholar 

  • Hödl W, Amézquita A (2001) Visual signaling in anuran amphibians. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, DC, pp 121–141

  • Kwet A, Lingnau R, Di-Bernardo M (2010) Pró-Mata: Anfíbios da Serra Gaúcha, sul do Brasil/Amphibien der Serra Gaúcha, Südbrasilien/Amphibians of the Serra Gaúcha, South of Brazil. EDIPUCRS/Brasilien-Zentrum der Universität Tübingen, Porto Alegre/Tübingen

  • Lindquist ED, Hetherington TE (1996) Field studies on visual and acoustic signaling in the “earless” Panamanian golden frog, Atelopus zeteki. J Herpetol 30(3):347–354

    Article  Google Scholar 

  • Lindquist ED, Hetherington TE (1998) Semaphoring in an earless frog: the origin of a novel visual signals. Anim Cogn 1:83–87

    Article  CAS  Google Scholar 

  • Lingnau R (2003) Comunicação acústica e visual, territorialidade e comportamento reprodutivo de Hylodes heyeri (Anura: Leptodactylidae) no Município de Morretes, Estado do Paraná, Brasil (dissertation). Universidade Federal de Goiás, Goiânia

  • Lingnau R, Canedo C, Pombal JP (2008) A new species of Hylodes (Anura: Hylodidae) from the Brazilian Atlantic Forest. Copeia 3:595–602

    Article  Google Scholar 

  • Lingnau R, Zank C, Colombo P, Kwet A (2013) Vocalization of Hylodes meridionalis (Mertens, 1927) (Anura, Hylodidae) in Rio Grande do Sul, Brazil, with comments on nocturnal calling in the family Hylodidae. Stud Neotrop Fauna E 48(1):76–80

    Article  Google Scholar 

  • Maestripieri D, Schino G, Aureli F, Troisi A (1992) A modest proposal: displacement activities as an indicator of emotions in primates. Anim Behav 44(5):967–979

    Article  Google Scholar 

  • Mertens R (1927) Neue Froschlurch aus Rio Grande do Sul, Brasilien. Blätter für Aquarien-und Terrarien-Kunde 38:287–290

    Google Scholar 

  • Narins PM, Hödl W, Grabul DS (2003) Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis. Proc Natl Acad Sci 100(2):577–580

    Article  CAS  Google Scholar 

  • Narvaes P, Rodrigues MT (2005) Visual communication, reproductive behavior, and home range of Hylodes dactylocinus (Anura, Leptodactylidae). Phyllomedusa 4(2):147–158

    Article  Google Scholar 

  • Narvaes IS, Brena DA, Longhi SJ (2005) Estrutura da regeneração natural em Floresta Ombrófila Mista na Floresta Nacional de São Francisco de Paula, RS. Ciênc Flor 15(4):331–342

    Article  Google Scholar 

  • Nosil P (2012) Ecological speciation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Pombal JP, Sazima I, Haddad CFB (1994) Breeding behavior of the Pumpkin Toadlet, Brachycephalus ephippium (Brachycephalidae). J Herpetol 28(4):516–519

    Article  Google Scholar 

  • Preininger D, Boeckle M, Freudmann A, Starnberger I, Sztatecsny M, Hödl W (2013) Multimodal signaling in the small torrent frog (Micrixalus saxicola) in a complex acoustic environment. Behav Ecol Sociobiol 67(9):1449–1456

    Article  Google Scholar 

  • Reichert MS, Höbel G (2015) Modality interactions alter the shape of acoustic mate preference functions in gray treefrogs. Evolution 69(9):2384–2398

    Article  Google Scholar 

  • Rendall D, Owren MJ, Ryan MJ (2009) What do animal signals mean? Anim Behav 78(2009):233–240

    Article  Google Scholar 

  • Ryan MJ (2001) Anuran communication. Smithsonian Institution Press, Washington, DC

  • Silva HR, Benmaman P (2008) Uma nova espécie de Hylodes Fitzinger da Serra da Mantiqueira, Minas Gerais, Brasil (Anura: Hylodidae). Rev Bras Zool 25(1):89–99

    Article  Google Scholar 

  • Stangel J, Preininger D, Sztatecsny M, Hödl W (2015) Ontogenetic change of signal brightness in the foot-flagging frog species Staurois parvus and Staurois guttatus. Herpetologica 71(1):1–7

    Article  Google Scholar 

  • Tinbergen N (1952) “Derived” activities; their causation, biological significance, origin, and emancipation during evolution. Q Rev Biol 27:1–32

    Article  CAS  Google Scholar 

  • Toledo LF, Martins IA, Bruschi DP, Passos MA, Alexandre C, Haddad CFB (2015) The anuran calling repertoire in the light of social context. Acta Ethol 18(2):87–99

    Article  Google Scholar 

  • Wells KD (2010) The ecology and behavior of amphibians. The University of Chicago Press, London

    Google Scholar 

  • Weygoldt P, Silva SPC (1992) Mating and oviposition in the hylodine frog Crossodactylus gaudichaudii (Anura: Leptodactylidae). Amphibia-Reptilia 13(1):35–45

    Article  Google Scholar 

  • Wogel H, Abrunhosa PA, Weber LN (2004) The tadpole, vocalizations and visual displays of Hylodes nasus (Anura: Leptodactylidae). Amphibia-Reptilia 25:219–227

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the Graduate Program in Ecology of the Universidade Federal do Rio Grande do Sul (UFRGS). RF received a scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). LNL received a scholarship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). RM was funded by the Ministerio de Ciencia e Innovación, Spain (project TATANKA CGL2011-25062). SMH received a fellowship from the Brazilian Research Council (CNPq; grant 304820/2014-8). Juliana Heck and André Luza provided assistance during field work and map construction, respectively. We thank Michael Bottesch and two anonymous reviewers for critically reading the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raíssa Furtado.

Ethics declarations

Conflict of interest

The authors declare that they have no potential conflict of interest.

Ethical approval

This study was carried out in accordance with the guidelines of the Ethics Committee on the Use of Animals of the Instituto Chico Mendes de Conservação da Biodiversidade—ICMBio, Brazil. ICMBio permitted the fieldwork with anuran species in the National Forest of São Franscisco de Paula (no. 51201-2). No animals were sacrificed during the study, and all of the animals used for the study were released back into nature.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MP4 33688 kb) Video S1. Resident male Hylodes meridionalis performing toe flagging and foot flagging displays for a conspecific intruder male. The intruder male performed arm lifting at the beginning of the recording. Recorded on January 4, 2016 at 17:37 h, air temperature of 20.9 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10296MOV1

Supplementary material 2 (MP4 52443 kb) Video S2. Male Hylodes meridionalis performing leg and arm lifting movements as response to mirror self-image presentation. Recorded on January 6, 2016 at 15:25 h, air temperature of 23.3 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10297MOV1

Supplementary material 3 (MP4 83396 kb) Video S3. Male Hylodes meridionalis performing arm waving displays as response to mirror self-image presentation. Recorded on November 13, 2016 at 17:04 h, air temperature of 19.6 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10298MOV1

Supplementary material 4 (MP4 25163 kb) Video S4. Female Hylodes meridionalis performing a both legs kicking display in front of a conspecific male. Recorded on November 13, 2016 at 18:00 h, air temperature of 19.6 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10299MOV1

Supplementary material 5 (MP4 48773 kb) Video S5. Interaction between two calling males of Hylodes meridionalis. The resident male (bottom right corner of the video) performed foot flagging displays with alternation of feet. Recorded on January 4, 2016 at 17:37 h, air temperature of 20.9 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10300MOV1

Supplementary material 6 (MP4 48450 kb) Video S6. Male Hylodes meridionalis performing throat displays during an agonistic interaction with another male. Recorded on February 24, 2017 at 14:00 h, air temperature of 24 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10302MOV1

Supplementary material 7 (MP4 58687 kb) Video S7. Male Hylodes meridionalis producing an advertisement call and, immediately after that, jumping towards the mirror that was positioned in front of the focal animal to simulate an intruder male. Recorded on January 4, 2016 at 15:58 h, air temperature of 23.6 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10303MOV1

Supplementary material 8 (MP4 45825 kb) Video S8. Male Hylodes meridionalis alternating territorial calls and throat displays during an agonistic interaction with another male. Recorded on February 24, 2017 at 15:00 h, air temperature of 24 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10304MOV1

Supplementary material 9 (MP4 54616 kb) Video S9. Male (bottom) of Hylodes meridionalis performing leg lifting and throat displays and, in sequence, producing courtship calls to a female (top) close to him. Recorded on November 13, 2016 at 18:00 h, air temperature of 19.6 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10306MOV1

Supplementary material 10 (MP4 182369 kb) Video S10. Agonistic interaction with physical attack between two males of Hylodes meridionalis. Recorded on January 4, 2016 at 17:37 h, air temperature of 20.9 °C, in São Francisco de Paula National Forest, southern Brazil. Fonoteca Zoológica Code: 10305MOV1

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Furtado, R., Lermen, L.N., Márquez, R. et al. Neotropical dancing frog: the rich repertoire of visual displays in a hylodine species. J Ethol 37, 291–300 (2019). https://doi.org/10.1007/s10164-019-00600-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10164-019-00600-x

Keywords

Navigation