Neotropical dancing frog: the rich repertoire of visual displays in a hylodine species
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.
KeywordsVisual displays Territoriality Courtship Limb lifting Foot flagging Arm waving Hylodes Anuran
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.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no potential conflict of interest.
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.
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
- 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) 43:37–123Google 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):1506–1516Google Scholar
- Forti LR, Castanho LM (2012) Behavioural repertoire and a new geographical record of the torrent frog Hylodes cardosoi (Anura: Hylodidae). Herpetol Bull 121:17–22Google 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
- 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:#X74QE0Google Scholar
- Haddad CFB, Giaretta AA (1999) Visual and acoustic communication in the Brazilian torrent frog, Hylodes asper (Anura: Leptodactylidae). Herpetologica 55(3):324–333Google 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 PauloGoogle 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):1675–1685Google Scholar
- Heyer WR, Rand AS, Cruz CAG, Peixoto OL, Nelson CE (1990) Frogs of Boracéia. Arq Zool S Paulo 31(4):231–410Google Scholar
- Hödl W, Amézquita A (2001) Visual signaling in anuran amphibians. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, DC, pp 121–141Google Scholar
- 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/TübingenGoogle 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, GoiâniaGoogle Scholar
- Mertens R (1927) Neue Froschlurch aus Rio Grande do Sul, Brasilien. Blätter für Aquarien-und Terrarien-Kunde 38:287–290Google Scholar
- Ryan MJ (2001) Anuran communication. Smithsonian Institution Press, Washington, DCGoogle Scholar
- Wells KD (2010) The ecology and behavior of amphibians. The University of Chicago Press, LondonGoogle Scholar