Skip to main content

Advertisement

SpringerLink
Log in

Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.

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
Fig. 7

Similar content being viewed by others

References

  • Anderson MJ (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639

    Article  Google Scholar 

  • Bee MA, Swanson EM (2007) Auditory masking of anuran advertisement calls by road traffic noise. Anim Behav 74:1765–1776

    Article  Google Scholar 

  • Bioacoustics Research Program (2014) Raven Pro: interactive sound analysis software (Version 1.5) [Computer software]. Ithaca, NY: The Cornell Lab of Ornithology. Available from http://www.birds.cornell.edu/raven

  • Bleach IT, Beckmann C, Both C, Brown GP, Shine R (2015) Noisy neighbours at the frog pond: effects of invasive cane toads on the calling behaviour of native Australian frogs. Behav Ecol Sociobiol 69:675–683

    Article  Google Scholar 

  • Boonman A, Kurniati H (2011) Evolution of high-frequency communication in frogs. Evolut Ecol Res 13:197–207

    Google Scholar 

  • Both C, Grant T (2012) Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs. Biol Lett 8:714–716

    Article  PubMed  PubMed Central  Google Scholar 

  • Both C, Solé M, Dos Santos TG, Cechin SZ (2009) The role of spatial and temporal descriptors for neotropical tadpole communities in southern Brazil. Hydrobiologia 624:125–138

    Article  Google Scholar 

  • Both C, Lingnau R, Santos-Jr AP, Lima LP, Madalozzo B, Grant T (2011) Widespread occurrence of the American Bullfrog, Lithobates catesbeianus (Shaw, 1802) (Anura: Ranidae), in Brazil. South Am J Herpetol 6:127–134

    Article  Google Scholar 

  • Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland

    Google Scholar 

  • Brumm H, Voss K, Köllmer I, Todt D (2004) Acoustic communication in noise: regulation of call characteristics in a New World monkey. J Exp Biol 207:443–448

    Article  PubMed  Google Scholar 

  • Capranica RR (1968) The vocal repertoire of the bullfrog (Rana catesbeiana). Behaviour 31:302–324

    Article  Google Scholar 

  • Cardoso AJ, Haddad CFB (1984) Variabilidade acústica em diferentes populações e interações agressivas de Hyla minuta (Amphibia: Anura). Cien Cult 36:1393–1399

    Google Scholar 

  • Cruz CAG, Caramaschi U (1998) Definição, composição e distribuição geográfica do grupo de Hyla polytaenia Cope, 1870 (Amphibia, Anura, Hylidae). Bol do Museu Nacional Zool (NS) 392:1–19

    Google Scholar 

  • Cunnington GM, Fahrig L (2010) Plasticity in the vocalizations of anurans in response to traffic noise. Acta Oecol 36:463–470

    Article  Google Scholar 

  • Dubois A, Martens J (1984) A case of possible vocal convergence between frogs and a bird in Himalayan torrents. J Ornithol 125:455–463

    Article  Google Scholar 

  • Edge WD, Marcum CL (1985) Movements of elk in relation to logging disturbances. J Wildl Manag 49:741–744

    Article  Google Scholar 

  • Farina A, Pieretti N, Morganti N (2013) Acoustic patterns of an invasive species: the Red-billed Leiothrix (Leiothrix lutea Scopoli 1786) in a Mediterranean shrubland. Bioacoustics. doi:10.1080/09524622.2012.761571

    Google Scholar 

  • Feng AS, Narins PM, Xu C-H, Lin W-Y, Yu Z-L, Qiu Q, Xu ZM, Shen JX (2006) Ultrasonic communication in frogs. Nature 440:333–336

    Article  CAS  PubMed  Google Scholar 

  • Fisher RA (1935) The logic of inductive inference. J R Stat Soc Ser A 98:39–54

    Article  Google Scholar 

  • Forsman A, Hagman M (2006) Calling is an honest indicator of paternal genetic quality in poison frogs. Evolution 60:2148–2157

    Article  PubMed  Google Scholar 

  • Frost DR (2015) Amphibian species of the World: an Online Reference. Version 6.0. Electronic database accessible at http://research.amnh.org/herpetology/amphibia/index.html. American Museum of Natural History, New York. Accessed 26 Apr 2015

  • Gehara M, Crawford AJ, Orrico VGD, Rodríguez A, Lötters S et al (2014) High levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the neotropical tree frog Dendropsophus minutus. PLoS ONE 9(9):e103958. doi:10.1371/journal.pone.0103958

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerhardt H (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615–635

    Article  Google Scholar 

  • Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. The University of Chicago Press, Chicago

    Google Scholar 

  • Goutte S, Dubois A, Legendre F (2013) The importance of ambient sound level to characterise anuran habitat. PLoS ONE 8(10):e78020. doi:10.1371/journal.pone.0078020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halfwerk W, Holleman LJM, Lessells CM, Slabbekoorn H (2011) Negative impact of traffic noise on avian reproductive success. J Appl Ecol 48:210–219

    Article  Google Scholar 

  • Hiert C, Moura MO (2007) Anfíbios do Parque Municipal das Araucárias, Guarapuava- Paraná. Editora Unicentro, Guarapuava

    Google Scholar 

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

    Google Scholar 

  • Hollen LI, Radford AN (2009) The development of alarm call behavior in mammals and birds. Anim Behav 78:791–800

    Article  Google Scholar 

  • Jaquiéry J, Broquet T, Aguilar C, Evanno G, Perrin N (2010) Good genes drive female choice for mating partners in the lek-breeding european treefrog. Evolution 64:108–115

    Article  PubMed  Google Scholar 

  • Kaiser K, Hammers JL (2009) The effect of anthropogenic noise on male advertisement call rate in the neotropical treefrog, Dendropsophus triangulum. Behaviour 146:1053–1069

    Article  Google Scholar 

  • Kaiser K, Scofield DG, Alloush M, Jones RM, Marczak S, Martineau K, Oliva MA (2011) When sounds collide: the effect of anthropogenic noise on a breeding assemblage of frogs in Belize, Central America. Behaviour 148:215–232

    Article  Google Scholar 

  • Kaiser K et al (2015) Effects of anthropogenic noise on endocrine and reproductive function in White’s treefrog, Litoria caerulea. Conserv Physiol 3(1):cou061

    Article  PubMed  PubMed Central  Google Scholar 

  • Krausman PR, Leopold BD, Scarbrough DL (1986) Desert mule deer response to aircraft. Wildl Soc Bull 14:68–70

    Google Scholar 

  • Kruger DJD, Preez LHD (2016) The effect of airplane noise on frogs: a case study on the critically endangered Pickersgill’s reed frog (Hyperolius pickersgilli). Ecol Res 31:393–405

    Article  Google Scholar 

  • Kwet A (2001) Frösche im brasilianischen Araukarienwald. Anurengemeinschaft des Araukarienwaldes von Rio Grande do Sul: Diversität, Reproduktion und Ressource-naufteilung. Münster. Natur und Tier-Verlag, 192

  • Kwet A, Di-Bernardo M (1999) Anfibios—Amphibien—Amphibians. EDIPUCRS, Porto Alegre

    Google Scholar 

  • Lane H, Tranel B (1971) The Lombard sign and the role of hearing in speech. J Speech Lang Hear Res 14:677–709

    Article  Google Scholar 

  • Lengagne T (2008) Traffic noise affects communication behaviour in a breeding anuran, Hyla arborea. Biol Conserv 141(8):2023–2031

    Article  Google Scholar 

  • Lever C (2003) Naturalized amphibians and reptiles of the world. Oxford University Press, New York

    Google Scholar 

  • Llusia D, Gómez M, Penna M, Márquez R (2013) Call Transmission efficiency in native and invasive anurans: competing hypotheses of divergence in acoustic signals. PLoS ONE 8(10):e77312. doi:10.1371/journal.pone.0077312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout MN, Bazzazz F (2000) Biotic invasions: causes, epidemiology, global consequences and control. Issues Ecol 5:1–20

    Google Scholar 

  • Magrini L, Giaretta AA (2001) Calls of two Brazilian species of Scinax of the S. ruber clade (Anura: Hylidae). Herpetol Notes 3:121–126

    Google Scholar 

  • Marcelino VR, Haddad CFB, Alexandrino J (2009) Geographic Distribution and Morphological Variation of Striped and Nonstriped Populations of the Brazilian Atlantic forest Treefrog Hypsiboas bischoffi (Anura: Hylidae). J Herpetol 43:351–361

    Article  Google Scholar 

  • Marten K, Marler P (1977) Sound transmission and its significance for animal vocalization. I. Temperate habitats. Behav Ecol Sociobiol 2:271–290

    Article  Google Scholar 

  • Marten K, Quine D, Marler P (1977) Sound transmission and its significance for animal vocalization. II. Tropical forest habitats. Behav Ecol Sociobiol 2:291–302

    Article  Google Scholar 

  • Martof BS, Thompson EF (1958) Reproductive behavior of the chorus frog (Pseudacris nigrita). Behaviour 13:243–258

    Article  Google Scholar 

  • McGregor PK, Dabelsteen T, Shepherd M, Pedersen SB (1992) The signal value of matched singing in Great Tits: evidence from in- teractive playback experiments. Anim Behav 43:987–998

    Article  Google Scholar 

  • Medeiros C, Both C, Kaefer I, Cechin SZ (2016) Reproductive phenology of the American Bullfrog in subtropical Brazil: photoperiod as a main determinant of seasonal activity. An Acad Bras Ciênc [Internet]. doi:10.1590/0001-3765201620150694

  • Narins PM (1995) Frog communication. Sci Am 273:78–83

    Article  Google Scholar 

  • Nogueira SSC, Pedroza JP, Nogueira-Filho SLG, Tokumaru RS (2012) The Function of Click Call Emission in Capybaras (Hydrochoerus Hydrochaeris). Ethology 118:1001–1009

    Article  Google Scholar 

  • Parris KM, Velik-Lord M, North JMA (2009) Frogs call at a higher pitch in traffic noise. Ecol Soc 14(1):25 (online)

    Article  Google Scholar 

  • Pillar VD (2006) MULTIV: multivariate exploratory analysis, randomization testing and bootstrap resampling. Universidade Federal do Rio Grande do Sul. See http://ecoqua.ecologia.ufrgs.br/ecoqua/MULTIV.html

  • Pillar VD, Orlóci L (1996) On randomization testing in vegetation science: multifactor comparisons of relevé groups. J Veg Sci 7:585–592

    Article  Google Scholar 

  • Planque R, Slabbekoorn H (2008) Spectral overlap in songs and temporal avoidance in a peruvian bird assemblage. Ethology 114:262–271

    Article  Google Scholar 

  • Pombal JP Jr (2010) O espaço acústico em uma taxocenose de anuros (Amphibia) do sudeste do brasil. Arquivos do Museu Nacional 68(1–2):135–144

    Google Scholar 

  • Pombal JP Jr, Bastos RP, Haddad CFB (1995) Vocalizações de algumas espécies do gênero Scinax (Anura, idae) do Sudeste do Brasil e comentários taxonômicos. Naturalia 20:213–225

    Google Scholar 

  • Primack BP, Rodrigues E (2001) Biologia da Conservação. Editora Planta, Londrina

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rabin LA, Mccowan B, Hooper SL, Owings DH (2003) Anthropogenic noise and its effect on animal communication: an interface between comparative psychology and conservation biology. Int J Comp Psychol 16:172–192

    Google Scholar 

  • Reby D, Cargnelutti B, Joachim E, Aulagnier S (1999) Spectral acoustic structure of barking in roe deer (Capreolus capreolus). Sex-, age- and individual-related variations. Comptes Rendus Acad Sci Ser III Sci Vie 322:271–279

    CAS  Google Scholar 

  • Rheindt FE (2003) The impact of roads on birds: does song frequency play a role in determining susceptibility to noise pollution? J Ornithol 144:295–306

    Article  Google Scholar 

  • Roca IT, Desrochers L, Giacomazzo M, Bertolo A, Bolduc P, Deschesnes R et al (2016) Shifting song frequencies in response to anthropogenic noise: a meta-analysis on birds and anurans. Behav Ecol 27:1269–1274

    Article  Google Scholar 

  • Ryan MJ (1988) Constraints and patterns in the evolution of anuran acoustic communication. In: Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 637–677

    Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • Silvano D, Scott N, Aquino L, Kwet A, Baldo D (2010) Rhinella icterica. In: IUCN. Red list of threatened species. Version 2010.4. http://www.iucnredlist.org. Accessed 24 June 2015

  • Sinsch U, Lümkemann K, Rosar K, Schwarz C, Dehling JM (2012) Acoustic niche partitioning in an anuran community inhabiting an Afromontane wetland (Butare, Rwanda). Afr Zool 47(1):60–73

    Article  Google Scholar 

  • Sueur J (2002) Cicada acoustic communication: potential sound partitioning in a multispecies community from Mexico (Hemiptera: Cicadomorpha: Cicadidae). Biol J Linn Soc 75:379–394

    Article  Google Scholar 

  • Sueur J, Aubin T, Simonis C (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics 18:213–226

    Article  Google Scholar 

  • Tennessen JB, Parks SE, Langkilde T (2014) Traffic noise causes physiological stress and impairs breeding migration behaviour in frogs. Conserv Physiol. doi:10.1093/conphys/cou032

    PubMed  PubMed Central  Google Scholar 

  • Tennessen JB, Parks SE, Tennessen TP, Langkilde T (2016) Raising a racket: invasive species compete acoustically with native treefrogs. Anim Behav 114:53–61

    Article  Google Scholar 

  • Vargas-Salinas F, Cunnington GM, Amézquita A, Fahrig L (2014) Does traffic noise alter calling time in frogs and toads? A case study of anurans in Eastern Ontario, Canada. Urban Ecosyst 17:945–953

    Article  Google Scholar 

  • Welch AM, Semlitsch RD, Gerhardt HC (1998) Call duration as an indicator of genetic quality in male gray tree frogs. Science 280(5371):1928–1930

    Article  CAS  PubMed  Google Scholar 

  • Wells KD (1977) The courtship of frogs. In: Taylor DH, Guttman SI (eds) The reproductive biology of amphibians. Plenum Press, New York, pp 233–262

    Chapter  Google Scholar 

  • Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Zelick R, Narins PM (1985) Characterization of the advertisement call oscillator in the frog Elutherodactylus coqui. J Comp Physiol A 156:223–229

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Abner Pontelli Perez, Rafael Henrique, Dilson Peixoto, Patrícia Barcarolo, Friedrich Keppeler, Rógger Antunes, André Luza, Mariane Bosholn and Pedro Aurélio Lima for their help in field and/or laboratory activities. We also thank the INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA BIODIVERSIDADE (ICMBio) for authorization to conduct this research (No. 42411-1), the COORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIOR (CAPES) for the award of a scholarship to CIM, the CONSELHO NACIONAL DE DESENVOLVIMENTO CIENTÍFICO E TECNOLÓGICO (CNPq) for the research fellowships of SMH (process 304820/2014-8), TG (305234/2014-5) and CB (401076/2014-8), and finally the UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL (UFRGS) Postgraduate program in Ecology and the FUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO (FAPESP) (2012/10000-5) for financial support of the equipment and field activities.

Author information

Authors and Affiliations

  1. Departamento de Ecologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, 91501-970, Brazil

    Camila Ineu Medeiros & Sandra Maria Hartz

  2. Departamento de Ecologia e Evolução, Universidade Federal de Santa Maria, Av. Roraima s/no, Santa Maria, Rio Grande do Sul, CEP 97105-900, Brazil

    Camila Ineu Medeiros & Camila Both

  3. Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, 05508-090, Brazil

    Taran Grant

Authors
  1. Camila Ineu Medeiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camila Both
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taran Grant
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sandra Maria Hartz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Camila Ineu Medeiros.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Medeiros, C.I., Both, C., Grant, T. et al. Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls. Biol Invasions 19, 675–690 (2017). https://doi.org/10.1007/s10530-016-1327-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1327-7

Keywords

Search

Navigation