Social interactions in a neotropical stream frog reveal a complex repertoire of visual signals and the use of multimodal communication

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?


Visual communication has evolved independently in several families of frogs and is complex in diurnal stream frogs. In addition to isolated visual and acoustic signals, some species may emit multimodal displays characterized by the association of these signals. Through the analysis of focal recordings obtained in situ in southern Brazil, we investigated the visual and multimodal communication in the diurnal stream frog Crossodactylus schmidti. We found a complex visual repertoire of nine signals used in intraspecific communication, of which the signal Both legs kicking was described for the first time. Males, females and juveniles emitted visual signals, but males had a larger repertoire and used most signals in agonistic interactions. The four most common visual signals, Toe flagging, Limb lifting, Body jerking and Running-jumping, were emitted predominantly upon rocks in the stream bed. The emission of isolated visual and acoustic signals, as well as audiovisual displays with simultaneous or temporally coupled components, demonstrates that the communication in C. schmidti is complex and that the multimodal displays may have different functions. We discuss the historical, behavioural, ecological factors which may have influenced the evolution of the visual repertoire of C. schmidti, and how the ritualization of derived activities similar to visual signals may have led to the evolution of part of the repertoire. This study provides novel results on visual and multimodal communication for the genus Crossodactylus and demonstrates that C. schmidti represents an appropriate model for studies of complex displays.



AmézquitaA.HödlW. (2004). How, when and where to perform visual displays: the case of the amazonian frog Hyla parviceps. — Herpetologica 6: 420-429.

AyresM.AyresM.Jr.AyresD.L.SantosA.S. (2007). BioEstat 5.0. Aplicações estatísticas nas áreas das ciências biológicas e médicas. Sociedade Civil de Mamirauá, Belém.

BernalX.E.RandA.S.RyanM.J. (2006). Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to túngara frog calls. — Behav. Ecol. 17: 709-715.

BorkentA. (2008). The frog-biting midges of the world (Corethrellidae: Diptera). — Zootaxa 1804: 1-456.

BorkentA.GrafeT.U. (2012). The frog-biting midges of Borneo — From two to eleven species (Corethrellidae: Diptera). — Zootaxa 3279: 1-45.

CaldartV.M.IopS.SantosT.G.CechinS.Z. (2010). Extension of the geographical distribution of two anuran species for Rio Grande do Sul State, Brazil, with comments on natural history. — Biota Neotrop. 10: 143-147.

CaldartV.M.IopS.CechinS.Z. (2011). Vocalizations of Crossodactylus schmidti Gallardo, 1961 (Anura, Hylodidae): advertisement call and aggressive call. — North-West. J. Zool. 7: 118-124.

CaldartV.M.IopS.BertasoT.R.N.CechinS.Z. (2012). Feeding ecology of Crossodactylus schmidti (Anura, Hylodidae) in southern Brazil. — Zool. Stud. 51: 484-493.

DoucetS.M.MennillD.J. (2010). Dynamic sexual dichromatism in an explosively breeding neotropical toad. — Biol. Letters 6: 63-66.

EliasD.O.SivalinghemS.MasonA.C.AndradeM.C.B.KasumovicM.M. (2010). Vibratory communication in the jumping spider Phidippus clarus: substrate-borne courtship signals are important for male mating success. — Ethology 116: 990-998.

EndlerJ.A. (1992). Signals, signals conditions, and the direction of evolution. — Am. Nat. 139: S125-S153.

EndlerJ.A. (1993). Some general comments on the evolution and design of animal communication systems. — Philos. Trans. Roy. Soc. Lond. B 340: 215-225.

EnquistM.HurdP.L.GhirlandaS. (2010). Signaling. — In: Evolutionary behavioural ecology ( WestneatD.F.FoxC.W., eds). Oxford University Press, Oxford, p.  266-284.

FergusonL.V.SmithT.G. (2012). Reciprocal trophic interactions and transmission of blood parasites between mosquitoes and frogs. — Insects 3: 410-423.

FortiL.R.CastanhoL.M. (2012). Behavioural repertoire and a new geographical record of the torrent frog Hylodes cardosoi (Anura: Hylodidae). — Herpetol. Bull. 121: 17-22.

FrostD.R. (2013). Amphibian species of the world: an online reference. Version 5.6 (9 January 2013). American Museum of Natural History, New York, NY, available online at (accessed 5 August 2013).

GerhardtH.C. (1994). The evolution of vocalization in frogs and toads. — Annu. Rev. Ecol. Syst. 25: 293-324.

GerhardtH.C.HuberF. (2002). Acoustic communication in insects and anurans: common problems and diverse solutions. — University of Chicago Press, Chicago, IL.

GiassonL.O.M.HaddadC.F.B. (2006). Social interactions in Hypsiboas albomarginatus (Anura: Hylidae) and the significance of acoustic and visual signals. — J. Herpetol. 40: 171-180.

GotelliN.J.EllisonA.M. (2011). Princípios de estatística em ecologia. — Artmed, Porto Alegre.

GrafeT.U.WangerT.C. (2007). Multimodal signaling in male and female foot-flagging frogs Staurois guttatus (Ranidae): an alerting function of calling. — Ethology 113: 772-781.

GrafeT.U.PreiningerD.SztatecsnyM.KasahR.DhelingM.ProkschS.HödlW. (2012). Multimodal communication in a noisy environment: a case study of the bornean rock frog Staurois parvus. — Plos One 7: e37965, DOI:10.1371/journal.pone.0037965.

HaddadC.F.B.GiarettaA.A. (1999). Visual and acoustic communication in the Brazilian torrent frog, Hylodes asper (Anura: Leptodactylidae). — Herpetologica 55: 324-333.

HartmannM.T.GiassonL.O.M.HartmannP.A.HaddadC.F.B. (2005a). Visual communication in Brazilian species of anurans from the Atlantic forest. — J. Nat. Hist. 39: 1675-1685.

HartmannM.T.HartmannP.A.HaddadC.F.B. (2005b). Repertório vocal de Hylodes phyllodes (Amphibia, Anura, Hylodidae). — Pap. Avul. Zool. 46: 203-209.

HebetsE.A.PapajD.R. (2005). Complex signal function: developing a framework of testable hypotheses. — Behav. Ecol. Sociobiol. 57: 197-214.

HebetsE.A.RundusA.S. (2011). Chemical communication in a multimodal context. — In: Chemical communication in crustaceans ( BreithauptT.ThielM., eds). Springer, New York, NY, p.  335-354.

HighamJ.P.HebetsE.A. (2013). An introduction to animal communication. — Behav. Ecol. Sociobiol. 67: 1381-1388.

HödlW.AmézquitaA. (2001). Visual signaling in anuran amphibians. — In: Anuran communication ( RyanM.J., ed.). Smithsonian Institution Press, Washington, DC, p.  121-141.

HuxleyJ.S. (1966). A discussion on ritualization of behaviour in animals and man — Introduction. — Philos. Trans. Roy. Soc. Lond. B 251: 249-271.

JohnsonR.N.YoungD.G.ButlerJ.F. (1993). Trypanosome transmission by Corethrella wirthi (Diptera: Chaoboridae) to the green frog, Hyla cinerea, (Anura: Hylidae). — J. Med. Entomol. 30: 918-921.

KrishnaS.N.KrishnaS.B. (2006). Visual and acoustic communication in an endemic stream frog, Micrixalus saxicolus in the Western Ghats, India. — Amphibia-Reptilia 27: 143-147.

LehnerP.N. (1996). Handbook of ethological methods. — Cambridge University Press, Cambridge.

LindquistE.D.HetheringtonT.E. (1998). Semaphoring in an earless frog: the origin of a novel visual signal. — Anim. Cogn. 1: 83-87.

LingnauR.CanedoC.PombalJ.P.Jr. (2008). A new species of Hylodes (Anura: Hylodidae) from the Brazilian Atlantic Forest. — Copeia: 595-602.

LorenzK.Z. (1966). Evolution of ritualization in the biological and cultural spheres. — Philos. Trans. Roy. Soc. Lond. B 251: 273-284.

MalufJ.R.T. (2000). Nova classificação climática do Estado do Rio Grande do Sul. — Ver. Bras. Agrometeor. 8: 141-150.

McKeeverS. (1977). Observations of Corethrella feeding on tree frogs (Hyla). — Mosquito News 37: 522-523.

MuramatsuD. (2011). For whom the male waves: four types of claw-waving display and their audiences in the fiddler crab, Uca lactea. — J. Ethol. 29: 3-8.

NarvaesP.RodriguesM.T. (2005). Visual communication, reproductive behavior, and home range of Hylodes dactylocinus (Anura, Leptodactylidae). — Phyllomedusa 4: 147-158.

Oliveira-FilhoA.T.JarenkowJ.A.RodalM.J.N. (2006). Floristic relationships of seasonally dry forests of eastern South America based on tree species distribution patterns. — In: Neotropical savannas and seasonally dry forests: plant diversity, biogeography, and conservation ( PenningtonR.T.LewisG.P.RatterJ., eds). Taylor & Francis/CRC Press, Boca Raton, FL, p.  159-192.

PreiningerD.BoeckleM.HödlW. (2009). Communication in noisy environments II: visual signaling behavior of male foot-flagging frogs Staurois latopalmatus. — Herpetologica 65: 166-173.

PreiningerD.BoeckleM.SztatecsnyM.HödlW. (2013). Divergent receiver responses to components of multimodal signals in two foot-flagging frog species. — Plos One 8: e55367, DOI:10.1371/journal.pone.0055367.

R Development Core Team (2011). R: a language and environment for statistical computing, version 2.12.2. — R Foundation for Statistical Computing, Vienna, available online at

RadcliffeC.W.ChiszarD.EstepK.MurphyJ.B.SmithH.M. (1986). Observations on pedal luring and pedal movements in Leptodactylid frogs. — J. Herpetol. 20: 300-306.

RosenthalG.G.RyanM.J. (2000). Visual and acoustic communication in non-human animals: a comparison. — J. Biosci. 25: 285-290.

RosenthalG.G.RandA.S.RyanM.J. (2004). The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback. — Anim. Behav. 68: 55-58.

RyanM.J. (1980). Female mate choice in a neotropical frog. — Science 209: 523-525.

ScottJ.L.KawaharaA.Y.SkevingtonJ.H.YenS.-H.SamiA.SmithM.L.YackJ.E. (2010). The evolutionary origins of ritualized acoustic signals in caterpillars. — Nature Commun. 1: DOI:10.1038/ncomms1002.

Scott-PhillipsT.C. (2008). Defining biological communication. — J. Evol. Biol. 21: 387-395.

Scott-PhillipsT.C.BlytheR.A.GardnerA.WestS.A. (2012). How do communication systems emerge?Proc. Roy. Soc. Lond. B: Biol. Sci. 279: 1943-1949.

SEMA Secretaria Estadual do Meio Ambiente (2005). Plano de Manejo do Parque Estadual do Turvo. Estado do Rio Grande do Sul: [s.n.], 348 p.

TakatsuH.MinamiM.TainakaK.YoshimuraJ. (2012). Spontaneous flash communication of females in an Asian firefly. — J. Ethol. 30: 355-360.

TinbergenN. (1952). ‘Derived’ activities, their causation, biological significance, origin, and emancipation during evolution. — Q. Rev. Biol. 27: 1-23.

TuttleM.D.RyanM.J. (1981). Bat predation and the evolution of frog vocalizations in the neotropics. — Science 214: 677-678.

WellsK.D. (1977). The social behaviour of anuran amphibians. — Anim. Behav. 25: 666-693.

WeygoldtP.Carvalho-e-SilvaS.P. (1992). Mating and oviposition in the Hylodine frog Crossodactylus gaudichaudii (Anura: Leptodactylidae). — Amphibia-Reptilia 13: 35-45.

WilgersD.J.HebetsE.A. (2012). Seismic signaling is crucial for female mate choice in a multimodal signaling wolf spider. — Ethology 118: 387-397.

WogelH.AbrunhosaP.A.WeberL.N. (2004). The tadpole, vocalizations and visual displays of Hylodes nasus (Anura, Leptodactylidae). — Amphibia-Reptilia 25: 219-227.


  • Mosaic distribution of the most frequent visual signals of Crossodactylus schmidti (674 signalizations from 54 individuals) according to the sites used for signal emission, based on 22 h of observations in Parque Estadual do Turvo, northwest of Rio Grande do Sul, Brazil. Each column represents the total frequency of emission of a visual signal and the numbered lines represent the emission sites used to signalize a visual signal; the relative frequency of signal emission is proportionally distributed within rectangles, and dashes represent the absence of a visual signal for the respective site. Abbreviations: TF, Toe flagging; LL, Limb lifting; BJ, Body jerking; RJ, Running-jumping; 1, on rock, above the water level; 2, on rock, at the water level; 3, on rock, below the water level; 4, on vegetation, at the water level; 5, on marginal vegetation. This figure is published in colour in the online edition of this journal, which can be accessed via

    View in gallery
  • Percentage of unimodal (visual) and multimodal (visual + acoustic) displays emitted by males of Crossodactylus schmidti (227 signalizations) considering the most frequent visual signals, based on 6 h of representative focal recordings of advertising males (N=2), agonistic interactions between males (N=22) and courtship interactions (N=12), selected from the total time of recordings obtained in Parque Estadual do Turvo, northwest of Rio Grande do Sul, Brazil. Abbreviations: TF, Toe flagging; LL, Limb lifting; BJ, Body jerking; RJ, Running-jumping.

    View in gallery


Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 12 12 7
Full Text Views 5 5 5
PDF Downloads 2 2 2
EPUB Downloads 0 0 0