Vol. 18 No. 1 (2023)
Articles

Patterns of acoustic phenology in an anuran assemblage of the Yungas Andean forests of Argentina

Martín Boullhesen
Instituto de Ecorregiones Andinas (INECOA), CONICET – UNJu. San Salvador de Jujuy
Marcos Vaira
Instituto de Ecorregiones Andinas (INECOA), CONICET – UNJu. San Salvador de Jujuy
Rubén Marcos Barquez
Instituto de Biodiversidad Argentina (PIDBA), Facultad de Ciencias Naturales e Instituto Miguel Lillo, Tucumán.
Mauricio Sebastián Akmentins
Instituto de Ecorregiones Andinas (INECOA), CONICET – UNJu. San Salvador de Jujuy

Published 2023-07-01

Keywords

  • advertisement calls,
  • anurans,
  • calling guilds,
  • Passive Acoustic Monitoring,
  • Acoustic breeding strategies,
  • acoustic phenology
  • ...More
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How to Cite

Boullhesen, M., Vaira, M., Barquez, R. M., & Akmentins, M. S. (2023). Patterns of acoustic phenology in an anuran assemblage of the Yungas Andean forests of Argentina. Acta Herpetologica, 18(1), 23–36. https://doi.org/10.36253/a_h-14050

Funding data

Abstract

Breeding seasons in anurans are usually noticed by their advertisement calls, which stand as the main signal emitted by males during their adult life. These calls are species-specific signals with multiple information and can be used to monitor anuran populations over extended time periods. Applying a Passive Acoustic Monitoring method (PAM), we described the acoustic breeding phenology of an anuran assemblage along an altitudinal elevation range in the Yungas Andean forests of Argentina. In addition, we propose a new classification scheme for their acoustic phenological strategies, based on the male’s calling records throughout an entire year. Also, we assessed the temporal and spectral niche overlap by the anuran species recorded. The assemblage was active throughout the entire year, with a higher concentration of calls recorded during the spring-summer season. We describe five distinct Acoustic Breeding Strategies based on the calling patterns of the recorded species. Temporal niche overlap was higher in the spring-summer season and in the lowest study site. The use of a PAM as a tool to monitor the advertisement calls in anurans communities could be a reliable technique to obtain different information about the species’ acoustic phenology and the temporal use of the acoustic communication channel.

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References

Akmentins, M.S. (2011): Vocal repertoire of two species of Oreobates Jiménez de la Espada, 1872 (Anura: Strabomantidae) of the Yungas Andean Forest, NW Argentina. J. Nat. Hist. 45: 1789-1799.
Akmentins, M.S., Boullhesen, M. (2020): The advertisement call of Gastrotheca chrysosticta Laurent, 1976 (Anura: Hemiphractidae). Zootaxa 4895: 297-300.
Rodrigues, M.T., Bertoluci, J. (2002): Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Boracéia, Southeastern Brazil. Amphib-reptil. 23:161-167.
Barrio, A. (1965): Las subespecies de Hyla pulchella Duméril y Bibron (Anura, Hylidae). Physis 25:115-128.
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.
Boullhesen, M., Salica, M.J., Pereyra, L., Akmentins, M. (2019): Actividad vocal diaria y su relación con claves ambientales en un ensamble de anuros en las Yungas de Jujuy, Argentina. Cuadernos de Herpetología 33: 59-70.
Bridges, A.S., Dorcas, M.E. (2000): Temporal variation in anuran calling behavior: implications for surveys and Monitoring Programs. Copeia 587-592.
Buckley, J., Beebee, T.J. (2004): Monitoring the conservation status of an endangered amphibian: the natterjack toad Bufo calamita in Britain. Animal Conservation 7: 221-228.
Burrowes, P.A. (2008): Climatic Change and Amphibian Declines. In: Amphibian Biology, (pp. 3268-3279). Heatwole, H., Wilkinson, J.W., (Eds.). Surrey Beatty & Sons.
Candolin, U. (2003): The use of multiple cues in mate choice. Biological reviews 78: 575-595.
Castro‐Arellano, I., Lacher Jr., T.E., Willig, M.R., Rangel, T.F. (2010): Assessment of assemblage‐wide temporal niche segregation using null models. Methods in ecology and evolution 1: 311-318.
Cei, J.M. (1980): Amphibians of Argentina volume 2. Universitá degli studi di Firenze.
Cook, R.P., Tupper, T.A., Paton, P.W., Timm, B.C. (2011): Effects of temperature and temporal factors on anuran detection probabilities at Cape Cod National Seashore, Massachusetts, USA: implications for long-term monitoring. Herpetological Conservation and Biology 6: 25-39.
De Solla, S.R., Fernie, K.J., Barrett, G.C., Bishop, C.A. (2006): Population trends and calling phenology of anuran populations surveyed in Ontario estimated using acoustic surveys. Biodiversity Conservation 15: 3481-3497.
De Oliveira, M., Aver, G.F., Moreira, L.F.B., Colombo, P., Tozetti, A.M. (2016): Daily movement and microhabitat use by the Blacksmith Treefrog Hypsiboas faber (Anura: Hylidae) during the breeding season in a subtemperate forest of Southern Brazil. South American Journal of Herpetology 11: 89-97.
Duarte, M.H., Caliari, E.P., Viana, Y.P., Nascimento, L.B. (2019): A natural orchestra: how are anuran choruses formed in artificial ponds in southeast Brazil? Amphib-reptil. 40: 373-382.
Duellman, W.E. (1970): The hylid frogs of Middle America. Monograph of the Museum of Natural History, The University of Kansas.
Dorcas, M.E., Price, S.J., Walls, S.C., Barichivich, W.J. (2009): Auditory monitoring of anuran populations. In: Amphibian Ecology and Conservation: A Hand Book of Techniques, p. 281–298. Dodd, C.K., (Ed.). Oxford University Press.
Donnelly, M.A., Guyer, C. (1994): Patterns of reproduction and habitat use in an assemblage of Neotropical hylid frogs. Oecologia, 98: 291-302.
Drewry, G.E., Rand, A.S. (1983): Characteristics of an acoustic community: Puerto Rican frogs of the genus Eleutherodactylus. Copeia 941-953.
Emmrich, M., Vences, M., Ernst, R., Köhler, J., Barej, M.F., Glaw, F., Jansen M., Rödel. M.O. (2020): A guild classification system proposed for anuran advertisement calls. Zoosystematics and Evolution 96: 515.
Emerson, S.B., Boyd, S.K. (1999): Mating vocalizations of female frogs: control and evolutionary mechanisms. Brain, Behavior and Evolution 53:187-197.
Feinsinger, P., Spears, E.E., Poole, R.W. (1981): A simple measure of niche breadth. Ecology 62: 27-32.
Gerhardt, H.C., Huber, F. (2002): Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press.
Gerhardt, H.C., Schwartz, J.J. (2001): Auditory tuning and frequency preferences. Anuran Communication. Smithsonian Institution Press, Washington.
Goodale, E., Beauchamp, G., Magrath, R.D. Nieh J.C., and G. D. Ruxton. (2010): Interspecific information transfer influences animal community structure. Trends in Ecology & Evolution 25: 354-361
Guerra, V., de Queiroz Costa, N., Llusia, D., Márquez, R., Bastos, R.P. (2020): Nightly patterns of calling activity in anuran assemblages of the Cerrado, Brazil. Community Ecology 21: 33-42.
Grau, A., Brown, A.D. (2000): Development threats to biodiversity and opportunities for conservation in the mountain ranges of the Upper Bermejo River Basin, NW Argentina and SW Bolivia. AMBIO: A Journal of the Human. Environment 29: 445-450.
Herrick, S.Z., Wells, K.D., Farkas, T.E., Schultz, E.T. (2018): Noisy neighbors: Acoustic interference and vocal interactions between two syntopic species of Ranid frogs, Rana clamitans and Rana catesbeiana. Journal of Herpetology 52: 176-184.
Hiert, C., Moura, M.O. (2010): Abiotic correlates of temporal variation of Hypsiboas leptolineatus (Amphibia: Hylidae). Zoologia 27: 703-708.
Huang, W.S., Lee, J.K., Ho, C.H. (2001): Breeding patterns of two sympatric rhacophorid frogs, Buergeria japonica and B. robusta, with comments on anuran breeding seasons in Taiwan. Zoological Science 18: 63-70.
Jammalamadaka, S. Rao, SenGupta, A. (2001): Topics in Circular Statistics. World Scientific Press, Singapore.
Klump, G.M., Gerhardt, H.C. (1992): Mechanisms and function of call-timing in male–male interactions in frogs. In: Playback and studies of animal communication, p.153-174. McGregor, P.K. Ed. Plenum, New York.
Köhler, J., Jansen, M., Rodriguez, A., Kok, P.J., Toledo, L.F., Emmrich, M., Glaw, F., Haddad, C.F.B., Rödel, M.O., Vences, M. (2017): The use of bioacoustics in anuran taxonomy: theory, terminology, methods, and recommendations for best practice. Zootaxa 4251: 1-124.
Krause, B.L. (1987): Bioacoustics, habitat ambience in ecological balance. Whole Earth Review 57: 14-18.
Krause, B.L. (1993): The niche hypothesis: a virtual symphony of animal sounds, the origins of musical expression and the health of habitats. The Soundscape Newsletter 6: 6-10.
Lannoo, M.J., Stiles, R.M. (2020): Uncovering shifting amphibian ecological relationships in a world of environmental change. Herpetologica 76: 144-152.
Lavilla, E.O. (2001): Amenazas, declinaciones poblacionales y extinciones en anfibios argentinos. Cuadernos de herpetología 15: 59-82
Lemckert, F., Mahony, M. (2008): Core calling periods of the frogs of temperate New South Wales, Australia. Herpetological Conservation and Biology 3:71-76.
Lima, M.S.C.S., Pederassi, J., Pineschi, R.B., Barbosa, D.B.S. (2019): Acoustic niche partitioning in an anuran community from the municipality of Floriano, Piauí, Brazil. Brazilian Journal of Biology 79: 566-576.
Llusia, D. (2013): Comunicación acústica en anuros ibéricos. Influencia del clima, hábitat y ambiente sonoro. Universidad Autónoma de Madrid. Madrid.
Márquez, R., Llusia, D., Beltrán, J.F. (2014): Aplicación de la bioacústica al seguimiento de anfibios. Boletín de la Asociación Herpetológica Española 25: 52-58.
Márquez, R., Verrell, P. (1991): The courtship and mating of the Iberian midwife toad Alytes cisternasii (Amphibia: Anura: Discoglossidae). Journal of Zoology 225: 125-139.
Mason, M. J. (2007): Pathways for sound transmission to the inner ear in amphibians. In: Hearing and sound communication in amphibians, p. 147-183. Narins, P. M., Feng, A.S., R.R. Fay, A.N. Popper, Eds. Springer, New York.
Measey, G., Stevenson, J.B.C., Scott, T., Altwegg, R., Borchers, D.L. (2017): Counting chirps: acoustic monitoring of cryptic frogs. Journal of Applied Ecology 54: 894-902.
Moreira, L.F.B., Machado, I.F., Lace, A.R.G.M., Maltchik, L. (2007): Calling period and breeding modes in an anuran community of a temporary pond in southern Brazil. South American Journal of Herpetology 2: 129-135.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B., Kent, J. (2000): Biodiversity hotspot for conservation priorities. Nature 403: 853-858.
Nelson, D.V., Garcia, T.S. (2017): Seasonal and diel vocal behavior of the northern red-legged frog, Rana aurora. Northwestern Naturalist 98: 33-38.
Oyarzabal, M., Clavijo, J. R., Oakley, L.J., Biganzoli, F., Tognetti, P.M., Barberis, I., Maturo, M.H., Aragón, R., Campanello, P.I., Prado, D., Oesterheld, M., León, R.J.C. (2018): Unidades de vegetación de la Argentina. Ecología Austral 28: 040-063.
Pereyra, L.C., Akmentins, M.S., Sanabria, E.A., Vaira, M. (2016): Diurnal? Calling activity patterns reveal nocturnal habits in the aposematic toad Melanophryniscus rubriventris. Canadian Journal of Zoology 94: 497-503.
Pereyra, L.C., Akmentins, M.S., Vaira, M., Moreno, C.E. (2018): Disentangling the multiple components of anuran diversity associated to different land‐uses in Yungas forests, Argentina. Animal Conservation 21: 396-404.
Pérez-Granados, C., Schuchmann, K. L., Ramoni-Perazzi, P. y Marques, M. I. (2020): Calling behaviour of Elachistocleis matogrosso (Anura, Microhylidae) is associated with habitat temperature and rainfall. Bioacoustics 29: 670-683.
Pewsey, A., Neuhäuser, M., Ruxton, G.D. (2013): Circular statistics in R. Oxford University Press.
Pieterson, E.C., Addison, L.M., Agobian, J.N., Brooks-Solveson, B., Cassani, J. y Everham, III. E.M. (2006): Five years of the Southwest Florida frog monitoring network: Changes in frog communities as an indicator of landscape change. Florida Scientist 69: 117-126.
Prado, C., Uetanabaro, M., Haddad, C. (2005): Breeding activity patterns, breeding modes, and habitat use by anurans (Amphibia) in a seasonal environment in the Pantanal, Brazil. Amphib-reptil. 26: 211-221.
Prestwich, K.N. (1994): The energetics of acoustic signalling in anurans and insects. American Zoologist 34: 625–643.
Ryan, M.J. (1988a): Energy, calling, and selection. American Zoologist 28: 885-898.
Ryan, M.J. (1988): Constraints and patterns in the evolution of anuran acoustic communication. In: The Evolution of the Amphibian Auditory System, pp. 637- 677. Fritzsch, B., Ryan, M.J., Wilczynski, W., Hetherington, T.E., Walkowiak, W. Eds. Wiley, New York.
Schwartz, J.J., Wells, K.D. (1983): An experimental study of acoustic interference between two species of Neotropical treefrogs. Animal Behaviour 31:181-190.
Shirose, L.J., Bishop, C.A., Green, D.M., MacDonald, C.J., Brooksm R.J., Helferty, N.J. (1997): Validation tests of an amphibian call count survey technique in Ontario, Canada. Herpetologica 53: 312-320.
Sinsch, U., Lümkemann, K., Rosar, K., Schwarz, C., Dehling, M. (2012): Acoustic niche partitioning in an anuran community inhabiting an Afromontane wetland (Butare, Rwanda). African Zoology 47: 60-73.
Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S., Fischman, D.L., Waller, R.W. (2004): Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783-1786.
Ulloa, J.S., Aubin, T., Llusia, D., Courtois, É. A., Fouquet, A., Gaucher, P., Pavoine, S. y Sueur, J. (2019): Explosive breeding in tropical anurans: environmental triggers, community composition and acoustic structure. BMC ecology 19: 1-17.
Vaira, M. (2002): Anurans of a subtropical montane forest in northwestern Argentina: ecological survey and a proposed list of species of conservation concern. Biodiversity & Conservation 11: 1047-1062.
Vaira, M., Pereyra, L.C., Akmentins, M.S., Bielby, J. (2017): Conservation status of amphibians of Argentina: An update and evaluation of national assessments. Amphibian & Reptile Conservation 11: 36–44
Villanueva-Rivera, L.J. (2014): Eleutherodactylus frogs show frequency but no temporal partitioning: implications for the acoustic niche hypothesis. PeerJ 2: e496.
Weir, L.A., Mossman, M.J. (2005): North American Amphibian Monitoring Program (NAAMP). In: Amphibian Declines: The Conservation Status of United States Species (p. 307-313). Lannoo, M.J. Ed. University of California Press, Berkeley, California, USA.
Wells, K.D. (1977): The social behaviour of anuran amphibians. Animal Behaviour 25: 666-693.
Wells, K.D. (2007): The ecology and behavior of amphibians. University of Chicago press.
Wells K.D., Schwartz J.J. (2007): The Behavioral Ecology of Anuran Communication. In: Hearing and Sound Communication in Amphibians (p. 44-86). Narins, P.M., Feng, A. S., Fay, R.R., Popper A.N. Eds., Springer Handbook of Auditory Research, vol. 28. Springer, New York, NY.
Wilkie, D. (1983): Rayleigh test for randomness of circular data. Applied statistics 32: 311-312
Willacy, R.J., Mahony, M., Newell, D.A. (2015): If a frog calls in the forest: Bioacoustic monitoring reveals the breeding phenology of the endangered Richmond Range Mountain frog (Philoria richmondensis). Austral Ecology 40: 625-633.
Williams, P.J., Engbrecht, N.J., Robb, J.R., Terrell, V.C., Lannoo, M.J. (2013): Surveying a threatened amphibian species through a narrow detection window. Copeia 3: 552-561.
Yoo, E. y Jang, Y. (2012): Abiotic effects on calling phenology of three frog species in Korea. Animal Cells and Systems 16: 260-267.
Zaracho, V.H., Lavilla, E.O. (2015): Diversidad, distribución espacio-temporal y turnos de vocalización de anuros (Amphibia, Anura) en un área ecotonal del nordeste de Argentina. Iheringia Série Zoologia 105: 199-208.