Skip to main content
SpringerLink
Log in

Geographic variation in acoustic and visual cues and their potential to signal body condition in the Brazilian treefrog, Boana albomarginata

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Anuran communication is largely based on acoustic signals, but different sensory modes are also widespread, including visual communication using body color traits as a way of signaling. The Brazilian treefrog, Boana albomarginata, has a complex behavioral repertoire presenting several call types and performing gestures as visual signals. This species has a greenish body color with orange patches on the flanks and thighs. These patches become visible when males are in a calling posture or performing visual signals such as leg kicking and limb lifting, suggesting that they might use the patches as visual cues. We sampled seven populations, using call recordings and photographs to access males call and color traits. We demonstrate that there is variation in color and call properties across populations. Additionally, we observe variation in the relationship between color traits and call properties in different populations, revealing that only two populations exhibit a significant correlation between color and call traits. Further, while call properties and color traits were not related with individual body size, they were associated with body condition. The results indicate a universal pattern across populations for call properties, wherein males in better condition consistently displayed lower-pitched calls, longer calls, and shorter intervals between calls. Regarding color traits, males in better condition in four out of the seven evaluated populations exhibited larger orange patch sizes, lower orange hue values, and higher hue contrasts. Although we observed some level of relation among color, call, and body traits, there is not a universal pattern across all populations.

Significance statement

Animal social interactions are mediated by signals transmitted through different sensory modes (i.e., acoustic, chemical, tactile, and visual), and more than one of these modalities can compose the behavioral repertoire of one species. Using photographs and acoustic recordings of Boana albomarginata males in natural environments, we documented geographic variation in both signals, call and color, and investigated their potential to convey individual body size and condition. Our findings reveal that both signals were correlated with individual body condition. In addition, color traits were associated with call properties in some populations.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Toes clippings were deposited in the TLFT tissue collection at Universidade Estadual de Campinas (Unicamp; TLFT 4501–609; 4611–8; 4620–4; 4626–73). Audio files were deposited at Fonoteca Neotropical Jacques Vielliard (FNJV), Museu de Diversidade Biológica (MDBio), Unicamp (FNJV 43831–939; 43,941–53; 43,955–83; 43,985–4003), following previous recommendations (Dena et al. 2020). The datasets generated and analyzed during the current study are available as supplementary material.

References

  • Amezquita A, Lima AP, Jehle R, Castellanos L, Ramos O, Crawford AJ, Gasser H, Hoedl W (2009) Calls, colours, shape, and genes: a multi-trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. Biol J Linn Soc 98:826–838

    Article  Google Scholar 

  • Arch VS, Narins PM (2009) Sexual hearing: the influence of sex hormones on acoustic communication in frogs. Hearing Res 252:15–20

    Article  CAS  Google Scholar 

  • Augusto-Alves G, Toledo LF (2022) Communication across multiple sensory modes: quantifying the rich behavioural repertoire of a Neotropical torrent frog. Behaviour 159:351–375

    Article  Google Scholar 

  • Augusto-Alves G, Dena SA, Toledo LF (2018) Visual communication and aggressive behaviour in a giant mute torrent-frog, Megaelosia apuana (Anura; Hylodidae). Amphibia-Reptilia 39:260–264

    Article  Google Scholar 

  • Augusto-Alves G, Ruggeri J, Martins AGS, Domingos AHR, Santos I, Toledo LF (2020) Leptodactylus flavopictus: temporal calling activity and tadpole redescription. Salamandra 56:123–134

    Google Scholar 

  • Augusto-Alves G, Dena S, Toledo LF (2021) Acoustic allometry, background stream noise and its relationship with large-bodied and voiceless rheophilic frogs. Zool Anz 295:156–162

    Article  Google Scholar 

  • Bee MA, Micheyl C (2008) The cocktail party problem: what is it? How can it be solved? And why should animal behaviorists study it? J Comp Psychol 122:235–251

    Article  PubMed  PubMed Central  Google Scholar 

  • Bittencourt-Silva G, Silva H (2013) Insular anurans (Amphibia: Anura) of the coast of Rio de Janeiro, southeast, Brazil. Check List 9:225–234

    Article  Google Scholar 

  • Boeckle M, Preininger D, Hödl W (2009) Communication in noisy environments I: acoustic signals of Staurois latopalmatus Boulenger 1887. Herpetologica 65:154–165

    Article  Google Scholar 

  • Brenes-Soto A, Dierenfeld ES (2014) Effect of dietary carotenoids on vitamin A status and skin pigmentation in false tomato frogs (Dyscophus guineti). Zoo Biol 33:544–552

    Article  CAS  PubMed  Google Scholar 

  • Brenes-Soto A, Dierenfeld ES, Janssens GP (2017) Colouration in amphibians as a reflection of nutritional status: the case of tree frogs in Costa Rica. PLoS One 12:e0182020

    Article  PubMed  PubMed Central  Google Scholar 

  • Caldwell MS, Johnston GR, McDaniel JG, Warkentin KM (2010) Vibrational signaling in the agonistic interactions of red-eyed treefrogs. Curr Biol 20:1012–1017

    Article  CAS  PubMed  Google Scholar 

  • Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595

    Article  PubMed  Google Scholar 

  • Cannizzaro JS, Höbel G (2023) Hidden black and yellow thigh color acts as an aposematic signal in the Eastern Gray Treefrog (Hyla versicolor). Ethology 129:679–685

    Article  Google Scholar 

  • Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323:785–789

    Article  CAS  PubMed  Google Scholar 

  • Center for Conservation Bioacoustics (2019) Raven Pro: Interactive Sound Analysis Software, version 1.6.1. The Cornell Lab of Ornithology, Ithaca, NY. http://www.birds.cornell.edu/raven

  • Chen Z, Wiens JJ (2020) The origins of acoustic communication in vertebrates. Nat Commun 11:369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Rosa MV, Ferrão M, Pequeno PACL, Lima AP (2023) How do tree density and body size influence acoustic signals in Amazonian nurse frogs? Bioacoustics 32:491–505

    Article  Google Scholar 

  • de Souza AO, Oliveira SR, Bastos RP, Morais AR (2021) Intraspecific advertisement call variation of Scinax fuscomarginatus (Lutz, 1925) from Central Brazil. Stud Neotrop Fauna E 58:476–484

    Article  Google Scholar 

  • Feltl L, Pacakova V, Stulik K, Volka K (2005) Reliability of carotenoid analyses: a review. Curr Anal Chem 1:93–102

    Article  Google Scholar 

  • Fernandes IY, Moraes LJCL, Menin M, Farias IP, Lima AP, Kaefer IL (2021) Unlinking the speciation steps: geographical factors drive changes in sexual signals of an Amazonian nurse-frog through body size variation. Evol Biol 48:81–93

    Article  Google Scholar 

  • Ferrer ES, Uribe F, Sanz JJ, Senar JC (2021) Are plumage colour and song redundant ornaments in great tits (Parus major)? it depends on the colour. Biol J Linn Soc 133:1077–1083

    Article  Google Scholar 

  • Fleishman LJ (1992) The influence of the sensory system and the environment on motion patterns in the visual displays of anoline lizards and other vertebrates. Am Nat 139:S36–S61

    Article  Google Scholar 

  • Fleishman L, Persons M (2001) The influence of stimulus and background colour on signal visibility in the lizard Anolis cristatellus. J Exp Biol 204:1559–1575

    Article  CAS  PubMed  Google Scholar 

  • Fletcher NH (2004) A simple frequency-scaling rule for animal communication. J Acoust Soc Am 115:2334–2338

    Article  PubMed  Google Scholar 

  • Forrest T (1994) From sender to receiver: propagation and environmental effects on acoustic signals. Am Zool 34:644–654

    Article  Google Scholar 

  • Forti LR, Costa WP, Martins LB, Nunes-de-Almeida CHL, Toledo LF (2016) Advertisement call and genetic structure conservatism: good news for an endangered Neotropical frog. PeerJ 4:e2014

    Article  PubMed  PubMed Central  Google Scholar 

  • Freitas MO, Toledo LF (2021) Treefrogs with distinct advertisement calls produce similar territorial signals. Bioacoustics 30:389–401

    Article  Google Scholar 

  • Frost DR (2023) Amphibian Species of the World: an Online Reference, version 6.2. American Museum of Natural History, New York, USA. https://amphibiansoftheworld.amnh.org/index.php

  • 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 

  • Gerhardt HC, Klump GM (1988) Masking of acoustic signals by the chorus background noise in the green tree frog: a limitation on mate choice. Anim Behav 1988:1247–1249

    Article  Google Scholar 

  • Giasson LO, Haddad CFB (2006) Social interactions in Hypsiboas albomarginatus (Anura: Hylidae) and the significance of acoustic and visual signals. J Herpetol 40:171–180

    Article  Google Scholar 

  • Giasson LO, Haddad CFB (2007) Mate choice and reproductive biology of Hypsiboas albomarginatus (Anura: Hylidae) in the Atlantic Forest, southeastern Brazil. S Am J Herpetol 2:157–164

    Article  Google Scholar 

  • Gingras B, Boeckle M, Herbst C, Fitch W (2013) Call acoustics reflect body size across four clades of anurans. J Zool 289:143–150

    Article  Google Scholar 

  • Gomez D, Richardson C, Lengagne T, Plenet S, Joly P, Léna JP, Théry M (2009) The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). Proc R Soc Lond B 276:2351–2358

    Google Scholar 

  • Gomez D, Richardson C, Lengagne T, Derex M, Plenet S, Joly P, Léna JP, Théry M (2010) Support for a role of colour vision in mate choice in the nocturnal European treefrog (Hyla arborea). Behaviour 147:1753–1768

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214

    Article  Google Scholar 

  • Heyer WR, Barrio-Amorós CL (2009) The advertisement calls of two sympatric frogs, Leptodactylus lithonaetes (Amphibia: Anura: Leptodactylidae) and Pristimantis vilarsi (Amphibia: Anura: Strabomantidae). P Biol Soc Wash 122:282–291

    Article  Google Scholar 

  • Höbel G, Gerhardt HC (2003) Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution 57:894–904

    PubMed  Google Scholar 

  • Jacobs LE, Vega A, Dudgeon S, Kaiser K, Robertson JM (2017) Local not vocal: assortative female choice in divergent populations of red-eyed treefrogs, Agalychnis callidryas (Hylidae: Phyllomedusinae). Biol J Linn Soc 120:171–178

    Google Scholar 

  • Jang Y, Hahm EH, Lee HJ, Park S, Won YJ, Choe JC (2011) Geographic variation in advertisement calls in a tree frog species: gene flow and selection hypotheses. PLoS One 6:e23297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelber A, Yovanovich C, Olsson P (2017) Thresholds and noise limitations of colour vision in dim light. Phil Trans R Soc B 372:20160065

    Article  PubMed  PubMed Central  Google Scholar 

  • Köhler J, Jansen M, Rodriguez A, Kok PJ, Toledo LF, Emmrich M, Glaw F, Haddad CFB, Roedel M-O, Vences M (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251:1–124

    Article  PubMed  Google Scholar 

  • Le Guyader S, Maier J, Jesuthasan S (2005) Esrom, an ortholog of PAM (protein associated with c-myc), regulates pteridine synthesis in the zebrafish. Dev Biol 277:378–386

    Article  PubMed  Google Scholar 

  • Lee KH, Shaner PJL, Lin YP, Lin SM (2016) Geographic variation in advertisement calls of a Microhylid frog–testing the role of drift and ecology. Ecol Evol 6:3289–3298

    Article  PubMed  PubMed Central  Google Scholar 

  • Lengagne T, Slater PJ (2002) The effects of rain on acoustic communication: tawny owls have good reason for calling less in wet weather. Proc R Soc Lond B 269:2121–2125

    Article  Google Scholar 

  • Loeffler-Henry K, Kang C, Sherratt TN (2023) Evolutionary transitions from camouflage to aposematism: hidden signals play a pivotal role. Science 379:1136–1140

    Article  CAS  PubMed  Google Scholar 

  • Luther D, Gentry K (2013) Sources of background noise and their influence on vertebrate acoustic communication. Behaviour 150:1045–1068

    Article  Google Scholar 

  • Merkling T, Chandrasoma D, Rankin KJ, Whiting MJ (2018) Seeing red: pteridine-based colour and male quality in a dragon lizard. Biol J Linn Soc 124:677–689

    Article  Google Scholar 

  • Mills MG, Patterson LB (2009) Not just black and white: pigment pattern development and evolution in vertebrates. Sem Cell Dev Biol 20:72–81

    Article  CAS  Google Scholar 

  • Ord TJ, Stamps JA (2008) Alert signals enhance animal communication in “noisy” environments. P Natl Acad Sci USA 105:18830–18835

    Article  CAS  Google Scholar 

  • Ord TJ, Peters RA, Clucas B, Stamps JA (2007) Lizards speed up visual displays in noisy motion habitats. Proc R Soc Lond B 274:1057–1062

    Google Scholar 

  • Parris KM, Velik-Lord M, North JM (2009) Frogs call at a higher pitch in traffic noise. Ecol Soc 14:25

    Article  Google Scholar 

  • Partan SR, Marler P (2005) Issues in the classification of multimodal communication signals. Am Nat 166:231–245

    Article  PubMed  Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Poth D, Wollenberg KC, Vences M, Schulz S (2012) Volatile amphibian pheromones: macrolides from mantellid frogs from Madagascar. Angew Chem Int Edit 51:2187–2190

    Article  Google Scholar 

  • Pröhl H, Hagemann S, Karsch J, Höbel G (2007) Geographic variation in male sexual signals in strawberry poison frogs (Dendrobates pumilio). Ethology 113:825–837

    Article  Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing, version 3.6.3. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rebouças R, Augusto-Alves G, Toledo LF (2020) Evolution of treefrogs’ calls in tropical islands might be under directional selection. J Zool 312:43–52

    Article  Google Scholar 

  • Robertson JM, Greene HW (2017) Bright colour patterns as social signals in nocturnal frogs. Biol J Linn Soc 121:849–857

    Article  Google Scholar 

  • Robertson JM, Duryea MC, Zamudio KR (2009) Discordant patterns of evolutionary differentiation in two Neotropical treefrogs. Mol Ecol 18:1375–1395

    Article  PubMed  Google Scholar 

  • Robertson JM, Bell RC, Loew ER (2022) Vision in dim light and the evolution of color pattern in a crepuscular/nocturnal frog. Evol Ecol 36:355–371

    Article  Google Scholar 

  • Rodríguez RL, Araya-Salas M, Gray DA, Reichert MS, Symes LB, Wilkins MR, Safran RJ, Höbel G (2015) How acoustic signals scale with body size: common trends across diverse taxa. Behav Ecol 26:168–177

    Article  Google Scholar 

  • Röhr DL, Camurugi F, Martinez PA, Sousa-Lima RS, Juncá FA, Garda AA (2020) Habitat-dependent advertisement call variation in the monkey frog Phyllomedusa nordestina. Ethology 126:651–659

    Article  Google Scholar 

  • Rudh A, Rogell B, Höglund J (2007) Non-gradual variation in colour morphs of the strawberry poison frog Dendrobates pumilio: genetic and geographical isolation suggest a role for selection in maintaining polymorphism. Mol Ecol 16:4284–4294

    Article  CAS  PubMed  Google Scholar 

  • Ryan MJ (1988) Energy, calling, and selection. Amer Zool 28:885–898

    Article  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz J, Bee MA (2013) Anuran acoustic signal production in noisy environments. In: Brumm H (ed) Animal communication and noise. Springer, Berlin, pp 91–132

    Chapter  Google Scholar 

  • Serrano JM, Penna M, Soto-Azat C (2020) Individual and population variation of linear and non-linear components of the advertisement call of Darwin’s frog (Rhinoderma darwinii). Bioacoustics 29:572–589

    Article  Google Scholar 

  • Smith MJ, Hunter D (2005) Temporal and geographic variation in the advertisement call of the booroolong frog (Litoria booroolongensis: Anura: Hylidae). Ethology 111:1103–1115

    Article  Google Scholar 

  • Starnberger I, Preininger D, Hödl W (2014) The anuran vocal sac: a tool for multimodal signalling. Anim Behav 97:281–288

    Article  PubMed  PubMed Central  Google Scholar 

  • Suga T, Munesada K (1988) The pigments in the dorsal skin of frogs. J Nat Prod 51:713–718

    Article  CAS  PubMed  Google Scholar 

  • Summers K, Cronin TW, Kennedy T (2003) Variation in spectral reflectance among populations of Dendrobates pumilio, the strawberry poison frog, in the Bocas del Toro Archipelago, Panama. J Biogeogr 30:35–53

    Article  Google Scholar 

  • Tessarolo G, Maciel NM, Morais AR, Bastos RP (2016) Geographic variation in advertisement calls among populations of Dendropsophus cruzi (Anura: Hylidae). Herpetol J 26:219–227

    Google Scholar 

  • Toledo LF, Haddad CFB (2009) Defensive vocalizations of Neotropical anurans. S Am J Herpetol 4:25–42

    Article  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 18:87–99

    Article  Google Scholar 

  • Tonini JFR, Provete D, Maciel N, Morais AR, Goutte S, Toledo LF, Pyron RA (2020) Allometric escape from acoustic constraints is rare for frog calls. Ecol Evol 10:3686–3695

    Article  PubMed  PubMed Central  Google Scholar 

  • Troscianko J, Stevens M (2015) Image calibration and analysis toolbox–a free software suite for objectively measuring reflectance, colour and pattern. Methods Ecol Evol 6:1320–1331

    Article  PubMed  PubMed Central  Google Scholar 

  • Umbers KD, Silla AJ, Bailey JA, Shaw AK, Byrne PG (2016) Dietary carotenoids change the colour of Southern corroboree frogs. Biol J Linn Soc 119:436–444

    Article  Google Scholar 

  • Vásquez T, Pfennig KS (2007) Looking on the bright side: females prefer coloration indicative of male size and condition in the sexually dichromatic spadefoot toad, Scaphiopus couchii. Behav Ecol Sociobiol 62:127–1350

    Article  Google Scholar 

  • Velásquez NA, Moreno-Gómez FN, Brunetti E, Penna M (2018) The acoustic adaptation hypothesis in a widely distributed South American frog: southernmost signals propagate better. Sci Rep 8:6990

    Article  PubMed  PubMed Central  Google Scholar 

  • Vignal C, Kelley D (2007) Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis. Proc R Soc Lond B 274:479–488

    Google Scholar 

  • Weiss SL, Foerster K, Hudon J (2012) Pteridine, not carotenoid, pigments underlie the female-specific orange ornament of striped plateau lizards (Sceloporus virgatus). Comp Biochem Phys B 161:117–123

    Article  CAS  Google Scholar 

  • Williams CR, Brodie ED Jr, Tyler MJ, Walker SJ (2000) Antipredator mechanisms of Australian frogs. J Herpetol 34:431–443

    Article  Google Scholar 

  • Yovanovich CA, Koskela SM, Nevala N, Kondrashev SL, Kelber A, Donner K (2017) The dual rod system of amphibians supports colour discrimination at the absolute visual threshold. Proc R Soc B 372:20160066

    Google Scholar 

  • Ziegler I (2003) The pteridine pathway in zebrafish: regulation and specification during the determination of neural crest cell-fate. Pigm Cell Res 16:172–182

    Article  CAS  Google Scholar 

  • Zornosa-Torres C, Toledo LF (2019) Courtship behavior and advertisement call geographic variation of Bokermannohyla luctuosa (Pombal Jr. and Haddad, 1993) (Hylidae, Cophomantini). S Am J Herpetol 14:71–79

    Article  Google Scholar 

Download references

Acknowledgements

We thank Joice Ruggeri, Leandro Tacioli, and Mariana Retuci Pontes for helping in the fieldwork; Simone Dena for storing all media produced in this work at Museu de Diversidade Biológica (MDBio); Jolyon Troscianko for helping during MicaToolbox software installation; Luís O. M. Giasson for making the raw data of his manuscript available to us (Giasson and Haddad 2007); We thank the anonymous reviewers and the editors for providing their thoughtful contributions to this manuscript; and Serra do Mar State Park for support during fieldwork.

Funding

GA-A thanks Idea Wild for equipment donation; Grants and fellowships were provided by the São Paulo Research Foundation (FAPESP #2016/25358–3; #2019/03170–0; #2019/25109–1) and the National Council for Scientific and Technological Development (CNPq #302834/2020–6).

Author information

Authors and Affiliations

  1. Laboratório de História Natural de Anfíbios Brasileiros (LaHNAB), Departamento de Biologia Animal, Instituto de Biologia, Unicamp, Campinas, São Paulo, 13083-862, Brazil

    Guilherme Augusto-Alves & Luís Felipe Toledo

  2. Programa de Pós-Graduação em Ecologia, Instituto de Biologia, Unicamp, Campinas, São Paulo, 13083-862, Brazil

    Guilherme Augusto-Alves & Luís Felipe Toledo

  3. Department of Biological Sciences, Behavioral and Molecular Ecology Group, University of Wisconsin-Milwaukee, Lapham Hall, 3209 N. Maryland Ave., Milwaukee, WI, 53201-0413, USA

    Guilherme Augusto-Alves & Gerlinde Höbel

Authors
  1. Guilherme Augusto-Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gerlinde Höbel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luís Felipe Toledo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GA-A and LFT conceptualized the study and experimental design. GA-A collected the data, and analyzed the photographs and recordings. GA-A and GH conducted the statistical analyses. GA-A prepared the manuscript drafts, and GH and LFT critically reviewed and edited subsequent versions. All authors have read and approved the final manuscript and submission for publication.

Corresponding author

Correspondence to Guilherme Augusto-Alves.

Ethics declarations

Ethical approval

The use of animals in this study adheres to the set forth by the Animal Behavior Society/Association for the Study of Animal Behaviour. This study was approved by the Instituto Chico Mendes de Conservação da Biodiversidade (SISBio #63697–2), Comissão Técnico-Científica, Instituto Florestal (COTEC #483/2018), ethics committee of Unicamp (Comissão de Ética no Uso de Animais, CEUA #4983–1/2018), and was registered at the Sistema Nacional de Gestão do Patrimônio Genético e do Conhecimento Tradicional Associado (SISGen #AE9A0E0).

Conflict of interest

The authors declare no competing interests.

Additional information

Communicated by E. Ringler

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 710 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Augusto-Alves, G., Höbel, G. & Toledo, L.F. Geographic variation in acoustic and visual cues and their potential to signal body condition in the Brazilian treefrog, Boana albomarginata. Behav Ecol Sociobiol 78, 48 (2024). https://doi.org/10.1007/s00265-024-03462-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-024-03462-7

Keywords

Search

Navigation