Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE (Open Access)

Unravelling male advertisement call variability in the brown tree frog (Litoria ewingii) complex by using citizen science

Jessica Elliott-Tate https://orcid.org/0000-0002-9043-9900 A B * and Jodi J. L. Rowley https://orcid.org/0000-0002-2011-9143 A B
+ Author Affiliations
- Author Affiliations

A Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia.

B Centre for Ecosystem Science; School of Biological, Earth and Environmental Sciences (BEES), University of New South Wales, Sydney, NSW 2052, Australia.

* Correspondence to: z5357092@zmail.unsw.edu.au

Handling Editor: Steven Cooper

Australian Journal of Zoology 72, ZO23026 https://doi.org/10.1071/ZO23026
Submitted: 8 July 2023  Accepted: 26 March 2024  Published: 7 May 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

In the face of global biodiversity declines, conservation measures are urgently needed. However, our lack of knowledge on species’ diversity, distributions and population trends presents a major obstacle, particularly for morphologically cryptic species. Field surveys to gather this information present a logistical challenge, but the rapid rise of citizen science presents a new opportunity, generating huge volumes of data rapidly across a species’ range. We use data from a national citizen-science project to document the distribution and advertisement call variability in a group of five morphologically conserved treefrogs. Using 542 male advertisement calls across the entire range of five species, we found considerable levels of acoustic variation both among and within species. Note shape, notes per call and positions of the longest and shortest notes were most useful to delineate species. Our research will assist in species delineation and identification in the field and form the basis for a more accurate understanding of species diversity and distributions in the brown tree frog complex. We also demonstrated the utility of citizen science in documenting species distributions and diversity.

Keywords: advertisement call, citizen science, geographic variation, Litoria calliscelis, Litoria ewingii, Litoria paraewingi, Litoria sibilus, Litoria verreauxii.

References

Amano T, Lamming JDL, Sutherland WJ (2016) Spatial gaps in global biodiversity information and the role of citizen science. Bioscience 66(5), 393-400.
| Crossref | Google Scholar |

Banks SC, Scheele BC, Macris A, Hunter D, Jack C, Fraser CI (2020) Chytrid fungus infection in alpine tree frogs is associated with individual heterozygosity and population isolation but not population-genetic diversity. Frontiers of Biogeography 12(1), e43875e.
| Crossref | Google Scholar |

Bee MA, Perrill SA (1996) Responses to conspecific advertisement calls in the green frog (Rana clamitans) and their role in male-male communication. Behaviour 133, 283-301.
| Crossref | Google Scholar |

Bee MA, Perrill SA, Owen PC (2000) Male green frogs lower the pitch of acoustic signals in defense of territories: a possible dishonest signal of size? Behavioral Ecology 11, 169-177.
| Crossref | Google Scholar |

Bela G, Peltola T, Young JC, Balázs B, Arpin I, Pataki G, Hauck J, Kelemen E, Kopperoinen L, Van Herzele A, Keune H, Hecker S, Suškevičs M, Roy HE, Itkonen P, Külvik M, László M, Basnou C, Pino J, Bonn A (2016) Learning and the transformative potential of citizen science. Conservation Biology 30(5), 990-999.
| Crossref | Google Scholar | PubMed |

Bivand R, Keitt T, Rowlingson B (2022) rgdal: bindings for the ‘geospatial’ data abstraction library. R package version 1.5-29. Available at https://CRAN.R-project.org/package=rgdal

Blaustein AR, Wake DB (1995) The puzzle of declining amphibian populations. Scientific American 272(4), 52-57.
| Crossref | Google Scholar |

Brattstrom BH (1963) A preliminary review of the thermal requirements of amphibians. Ecology 44(2), 238-255.
| Crossref | Google Scholar |

Brown GW, Scroggie MP, Smith MJ, Steane D (2007) An evaluation of methods for assessing the population status of the threatened alpine tree frog Litoria Verreauxii Alpina in Southeastern Australia. Copeia 2007(3), 765-770.
| Crossref | Google Scholar |

Bull JW, Milner-Gulland E-J, Müller J (2020) Choosing prevention or cure when mitigating biodiversity loss: trade-offs under ‘no net loss’ policies. Journal of Applied Ecology 57(2), 354-366.
| Crossref | Google Scholar |

Callaghan CT, Roberts JD, Poore AGB, Alford RA, Cogger H, Rowley JJL (2020) Citizen science data accurately predicts expert-derived species richness at a continental scale when sampling thresholds are met. Biodiversity and Conservation 29(4), 1323-1337.
| Crossref | Google Scholar |

Caughley G, Gunn G (1996) ‘Conservation biology in theory and practice.’ (Blackwell Science: Malden, MA, USA)

Cocroft RB, Ryan MJ (1995) Patterns of advertisement call evolution in toads and chorus frogs. Animal Behaviour 49, 283-303.
| Crossref | Google Scholar |

Cutajar TP, Portway CD, Gillard GL, Rowley JJL (2022) Australian Frog Atlas: species’ distribution maps informed by the FrogID dataset. Technical Reports of the Australian Museum (online) 36. pp. 1–48. (The Australian Museum) 10.3853/j.1835-4211.36.2022.1789

Darwell CT, Cook JM (2017) Cryptic diversity in a fig wasp community-morphologically differentiated species are sympatric but cryptic species are parapatric. Molecular Ecology 26(3), 937-950.
| Crossref | Google Scholar | PubMed |

Department of Agriculture, Water and the Environment (2014) Approved Conservation Advice for Litoria verreauxii alpina (alpine tree frog). Department of the Environment. Available at http://www.environment.gov.au/biodiversity/threatened/species/pubs/66669-conservation-advice.pdf

Dickinson JL, Zuckerberg B, Bonter DN (2010) Citizen science as an ecological research tool: challenges and benefits. Annual Review of Ecology, Evolution, and Systematics 41, 149-172.
| Crossref | Google Scholar |

Fang G, Jiang F, Yang P, Cui J, Brauth SE, Tang Y (2014) Male vocal competition is dynamic and strongly affected by social contexts in music frogs. Animal Cognition 17, 483-494.
| Crossref | Google Scholar | PubMed |

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.
| Crossref | Google Scholar |

Frost DR (2023) Amphibian species of the world: an online reference (version 6.1). Electronic Database. American Museum of Natural History, New York, NY, USA. Accessible at https://amphibiansoftheworld.amnh.org/index.php [Accessed 27 January 2023]

Gartside DF (1972) The Litoria ewingi complex (Anura : Hylidae) in south-eastern Australia III. Blood protein variation across a narrow hybrid zone between L. ewingi and L. paraewingi. Australian Journal of Zoology 20(4), 435-443.
| Crossref | Google Scholar |

Gartside DF (1982) The Litoria ewingi complex (Anura : Hylidae) in south-eastern Australia VI. Geographic variation in transferrins of four taxa. Australian Journal of Zoology 30(1), 103-113.
| Crossref | Google Scholar |

Gerhardt HC (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Animal Behaviour 42(4), 615-635.
| Crossref | Google Scholar |

Gerhardt HC, Davis MS (1988) Variation in the coding of species identity in the advertisement calls of Litoria verreauxii (Anura: Hylidae). Evolution 42(3), 556-565.
| Crossref | Google Scholar | PubMed |

Gerhardt HC, Huber F (2002) ‘Acoustic communication in insects and anurans: common problems and diverse solutions.’ (University Of Chicago Press: Chicago, IL, USA)

Gillard GL, Rowley JJL (2023) Assessment of the acoustic adaptation hypothesis in frogs using large-scale citizen science data. Journal of Zoology 320(4), 271-281.
| Crossref | Google Scholar |

Gillespie GR, Roberts JD, Hunter D, Hoskin CJ, Alford RA, Heard GW, Hines H, Lemckert F, Newell D, Scheele BC (2020) Status and priority conservation actions for Australian frog species. Biological Conservation 247, 108543.
| Crossref | Google Scholar |

Heard GW, Canessa S, Parris KM (2015) Interspecific variation in the phenology of advertisement calling in a temperate Australian frog community. Ecology and Evolution 5(18), 3927-3938.
| Crossref | Google Scholar | PubMed |

Hero J, Morrison C (2004) Frog declines in Australia: global implications. The Herpetological Journal 14, 175-186.
| Google Scholar |

Hijmans RJ (2022) raster: geographic data analysis and modeling. R package version 3.5-15. Available at https://CRAN.R-project.org/package=raster

Hopkins WA (2007) Amphibians as models for studying environmental change. ILAR Journal 48(3), 270-277.
| Crossref | Google Scholar | PubMed |

Howard RD, Young JR (1998) Individual variation in male vocal traits and female mating preferences in Bufo americanus. Animal Behaviour 55, 1165-1179.
| Crossref | Google Scholar | PubMed |

Hunter D, Waudby HP (2017) ‘Frogs of south-west NSW.’ (Office of Environment and Heritage: Sydney, NSW, Australia)

IUCN (2021) The IUCN Red List of Threatened Species. Version 2021-3. Available at https://www.iucnredlist.org [Accessed 28 March 2022]

K Lisa Yang Center for Conservation Bioacoustics (2022) Raven Pro: interactive sound analysis software (version 1.6.4) [Computer software]. (The Cornell lab of Ornithology: Ithaca, NY, USA) Available at https://ravensoundsoftware.com/

Kassambara A (2020) ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.4.0. Available at https://CRAN.R-project.org/package=ggpubr

Kim KC, Byrne LB (2006) Biodiversity loss and the taxonomic bottleneck: emerging biodiversity science. Ecological Research 21(6), 794-810.
| Crossref | Google Scholar |

Kime NM, Burmeister SS, Ryan MJ (2004) Female preferences for socially variable call characters in the cricket frog, Acris crepitans. Animal Behaviour 68(6), 1391-1399.
| Crossref | Google Scholar |

Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, Kuussaari M, Lindborg R, Öckinger E, Pärtel M, Pino J, Pöyry J, Raatikainen KM, Sang A, Stefanescu C, Teder T, Zobel M, Steffan-Dewenter I (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecology Letters 13(5), 597-605.
| Crossref | Google Scholar | PubMed |

Köhler J, Jansen M, Rodríguez A, Kok PJR, Toledo LF, Emmrich M, Glaw F, Haddad CFB, Rödel M-O, Vences M (2017) The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa 4251(1), 1-124.
| Crossref | Google Scholar | PubMed |

Lesbarreres D, Lodé T (2002) Variations in male calls and responses to an unfamiliar advertisement call in a territorial breeding anuran, Rana dalmatina: evidence for a “dear enemy” effect. Ethology Ecology & Evolution 14, 287-295.
| Crossref | Google Scholar |

Lillywhite HB (1970) Behavioral temperature regulation in the bullfrog, Rana catesbeiana. Copeia 1970, 158-168.
| Crossref | Google Scholar |

Littlejohn MJ (1965) Premating isolation in the Hyla ewingi complex (Anura: Hylidae). Evolution 19(2), 234-243.
| Crossref | Google Scholar |

Littlejohn MJ (1976) The Litoria ewingi complex (Anura : Hylidae) in south-eastern Australia IV. Variation in mating-call structure across a narrow hybrid zone between L. ewingi and L. paraewingi. Australian Journal of Zoology 24(2), 283-167.
| Crossref | Google Scholar |

Littlejohn MJ, Roberts JD (1975) Acoustic analysis of an intergrade zone between two call races of the Limnodynastes tasmaniensis complex (Anura: Leptodactylidae) in south-eastern Australia. Australian Journal of Zoology 23(1), 113-122.
| Crossref | Google Scholar |

Littlejohn MJ, Watson GF (1983) The Litoria ewingi complex (Anura: Hylidae) in south-eastern Australia VII. Mating-call structure and genetic compatibility across a narrow hybrid zone between L. ewingi and L. paraewingi. Australian Journal of Zoology 31(2), 193-204.
| Crossref | Google Scholar |

Luedeling E (2019) chillR: statistical methods for phenology analysis in temperate fruit trees. R package version 0.70.15. Available at https://CRAN.R-project.org/package=chillR

Lötters S, Schmitz A, Reichle S, Rödder D, Quennet V (2009) Another case of cryptic diversity in poison frogs (Dendrobatidae: Ameerega): description of a new species from Bolivia. Zootaxa 2028, 20-30.
| Crossref | Google Scholar |

Mahony M, Moses B, Mahony SV, Lemckert FL, Donnellan S (2020) A new species of frog in the Litoria ewingii species group (Anura: Pelodryadidae) from south-eastern Australia. Zootaxa 4858(2), 201-230.
| Crossref | Google Scholar |

Martínez-Rivera CC, Gerhardt HC (2008) Advertisement-call modification, male competition, and female preference in the bird-voiced treefrog Hyla avivoca. Behavioral Ecology and Sociobiology 63(2), 195-208.
| Crossref | Google Scholar |

Mitchell BA, Callaghan CT, Rowley JJL (2020) Continental-scale citizen science data reveal no changes in acoustic responses of a widespread tree frog to an urbanisation gradient. Journal of Urban Ecology 6(1), juaa002.
| Crossref | Google Scholar |

Morais AR, Batista VG, Gambale PG, Signorelli L, Bastos RP (2012) Acoustic communication in a neotropical frog (Dendropsophus minutus): vocal repertoire, variability and individual discrimination. Herpetological Journal 22(4), 249-257.
| Google Scholar |

Narins PM, Meenderink SWF (2014) Climate change and frog calls: long-term correlations along a tropical altitudinal gradient. Proceedings of the Royal Society B: Biological Sciences 281(1783), 20140401.
| Crossref | Google Scholar |

Ooms J (2023) av: working with audio and visual in R. R package version 0.9.0. Available at https://CRAN.R-project.org/package=av

Osborne W, Hunter D, Hollis G (1999) Population declines and rang contraction in Australian alpine frogs. In ‘Declines and disappearances of Australian frogs’. (Ed. A Campbell) pp. 145–157. (Environment Australia)

Oseen KL, Wassersug RJ (2002) Environmental factors influencing calling in sympatric anurans. Oecologia 133(4), 616-625.
| Crossref | Google Scholar | PubMed |

O’Connor NE, Crowe TP (2005) Biodiversity loss and ecosystem functioning: distinguishing between number and identity of species. Ecology 86(7), 1783-1796.
| Crossref | Google Scholar |

Parkin T, Rowley JJL, Elliott-Tate J, Mahony MJ, Sumner J, Melville J, Donnellan SC (2024) Systematic assessment of the brown tree frog (Anura: Pelodryadidae: Litoria ewingii) reveals two endemic species in South Australia. Zootaxa 5406(1), 1-36.
| Crossref | Google Scholar | PubMed |

Pebesma E (2018) Simple features for R: standardized support for spatial vector data. The R Journal 10(1), 439-446.
| Crossref | Google Scholar |

Perpinan Lamigueiro O, Hijmans R (2022) rasterVis. R package version 0.51.2. Available at https://CRAN.R-project.org/package=rasterVis

R Core Team (2021) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing, Vienna, Austria) Available at https://www.R-project.org/

Renan S, Gafny S, Perl RGB, Roll U, Malka Y, Vences M, Geffen E (2017) Living quarters of a living fossil-uncovering the current distribution pattern of the rediscovered Hula painted frog (Latonia nigriventer) using environmental DNA. Molecular Ecology 26(24), 6801-6812.
| Crossref | Google Scholar | PubMed |

Roberts JD (1993) Hybridization between the western and northern call races of the Limnodynastes–Tasmaniensis complex (Anura, Myobatrachidae) on the Murray River in South Australia. Australian Journal of Zoology 41(2), 101-122.
| Crossref | Google Scholar |

Rocha CFD, Van Sluys M, Hatano FH, Boquimpani-Freitas L, Marra RV, Marques RV (2004) Relative efficiency of anuran sampling methods in a restinga habitat (Jurubatiba, Rio de Janeiro, Brazil). Brazilian Journal of Biology 64(4), 879-884.
| Crossref | Google Scholar |

Rowley JJL, Alford RA (2013) Hot bodies protect amphibians against chytrid infection in nature. Scientific Reports 3, 1515.
| Crossref | Google Scholar | PubMed |

Rowley JJL, Callaghan CT (2020) The FrogID dataset: expert-validated occurrence records of Australia’s frogs collected by citizen scientists. ZooKeys 912, 139-151.
| Crossref | Google Scholar | PubMed |

Rowley JJL, Callaghan CT, Cutajar T, Portway C, Potter K, Mahony S, Trembath D, Flemons P, Woods A (2019) FrogID: citizen scientists provide validated biodiversity data on frogs of Australia. Herpetological Conservation and Biology 14(1), 155-170.
| Crossref | Google Scholar |

Ryan MJ, Cocroft RB, Wilczynski W (1990) The role of environmental selection in intraspecific divergence of mate recognition signals in the cricket frog, Acris crepitans. Evolution: International Journal of Organic Evolution 44(7), 1869-1872.
| Crossref | Google Scholar | PubMed |

Sanders M (2021) ‘Photographic field guide to Australian frogs.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Scheele BC, Legge S, Armstrong DP, Copley P, Robinson N, Southwell D, Westgate MJ, Lindenmayer DB (2018) How to improve threatened species management: an Australian perspective. Journal of Environmental Management 223, 668-675.
| Crossref | Google Scholar | PubMed |

Smith MJ, Osborne W, Hunter D (2003) Geographic variation in the advertisement call structure of Litoria verreauxii (Anura: Hylidae). Copeia 2003(4), 750-758.
| Crossref | Google Scholar |

Smith KL, Hale JM, Kearney MR, Austin JJ, Melville J (2013a) Molecular patterns of introgression in a classic hybrid zone between the Australian tree frogs, L. ewingii and L. paraewingi: evidence of a tension zone. Molecular Ecology 22(7), 1869-1883.
| Crossref | Google Scholar | PubMed |

Smith KL, Hale JM, Gay L, Kearney M, Austin JJ, Parris KM, Melville J (2013b) Spatio-temporal changes in the structure of an Australian frog hybrid zone: a 40-year perspective. Evolution 67(12), 3442-3454.
| Crossref | Google Scholar | PubMed |

South A (2017a) rnaturalearth: world map data from natural earth. R package version 0.1.0. Available at https://CRAN.R-project.org/package=rnaturalearth

South A (2017b) rnaturalearthdata: world vector map data from natural earth used in ‘rnaturalearth’. R package version 0.1.0. Available at https://CRAN.R-project.org/package=rnaturalearthdata

Souza DM, Teixeira RFM, Ostermann OP (2015) Assessing biodiversity loss due to land use with Life Cycle Assessment: are we there yet? Global Change Biology 21(1), 32-47.
| Crossref | Google Scholar | PubMed |

Sparks AH, Padgham M, Parsonage H, Pembleton K, Balamuta J, Anderson B (2019) bomrang: Australian Government Bureau of Meteorology (BOM) data from R. R package version 0.5.0. Available at https://CRAN.R-project.org/package=bomrang

Sullivan BK, Hinshaw SH (1990) Variation in advertisement calls and male calling behavior in the spring peeper (Pseudacris crucifer). Copeia 1990(4), 1146-1150.
| Crossref | Google Scholar |

Sumner M (2021) ozmaps: Australia Maps. R package version 0.4.5. Available at https://CRAN.R-project.org/package=ozmaps

Tessarolo G, Maciel NM, de Morais AR, Bastos RP (2016) Geographic variation in advertisement calls among populations of Dendropsophus cruzi (Anura: Hylidae). Herpetological Journal 26, 219-224.
| Google Scholar |

Theodoridis S, Nogués-Bravo D, Conti E (2019) The role of cryptic diversity and its environmental correlates in global conservation status assessments: insights from the threatened bird’s-eye primrose (Primula farinosa L.). Diversity and Distributions 25(9), 1457-1471.
| Crossref | Google Scholar |

Toledo LF, Martins IA, Bruschi DP, Passos MA, Alexandre C, Haddad CFB (2014) The anuran calling repertoire in the light of social context. Acta Ethologica 18(2), 87-99.
| Crossref | Google Scholar |

Van Sluys M, Marra RV, Boquimpani-Freitas L, Rocha CFD (2012) Environmental factors affecting calling behavior of sympatric frog species at an Atlantic Rain Forest Area, Southeastern Brazil. Journal of Herpetology 46(1), 41-46.
| Crossref | Google Scholar |

Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences of the USA 105, 11466-11473.
| Google Scholar | PubMed |

Watson GF (1972) The Litoria ewingi complex (Anura : Hylida) in south-eastern Australia II. Genetic incompatibility and delimitation of a narrow hybrid zone between L. ewingi and L. paraewingi. Australian Journal of Zoology 20(4), 423-433.
| Crossref | Google Scholar |

Watson GF, Littlejohn MJ (1978) The Litoria ewingi complex (Anura: Hylidae) in south-eastern Australia V. Interactions between northern L. ewingi and adjacent taxa. Australian Journal of Zoology 26(1), 175-195.
| Crossref | Google Scholar |

Watson GF, Loftus-Hills JJ, Littlejohn MJ (1971) The Litoria ewingi complex (Anura : Hylidae) in south-eastern Australia I: a new species from Victoria. Australian Journal of Zoology 19(4), 401-416.
| Crossref | Google Scholar |

Watson GF, Littlejohn MJ, Gartside DF, Loftus-Hills JJ (1985) The Litoria ewingi complex (Anura : Hylidae) in South-Eastern Australia VIII. Hybridization between L. ewingi and L. verreauxii alpina in the Mount Baw Baw Area, south central Victoria. Australian Journal of Zoology 33(2), 143-152.
| Crossref | Google Scholar |

Weaver SJ, Callaghan CT, Rowley JJL (2020) Anuran accents: continental-scale citizen science data reveal spatial and temporal patterns of call variability. Ecology and Evolution 10(21), 12115-12128.
| Crossref | Google Scholar | PubMed |

Wells KD (2007) ‘The ecology and behavior of amphibians.’ (University Of Chicago Press: Chicago, IL, USA)

Wells KD, Schwartz JJ (1984) Vocal communication in a Neotropical treefrog, Hyla ebraccata: advertisement calls. Animal Behaviour 32, 405-420.
| Crossref | Google Scholar |

Wells KD, Taigen TL (1986) The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor). Behavioral Ecology and Sociobiology 19, 9-18.
| Crossref | Google Scholar |

Whiles MR, Hall RO, Jr, Dodds WK, Verburg P, Huryn AD, Pringle CM, Lips KR, Kilham SS, Colón-Gaud C, Rugenski AT, Peterson S, Connelly S (2013) Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16(1), 146-157.
| Crossref | Google Scholar |

Wickham H (2016) ‘ggplot2: elegant graphics for data analysis.’ (Springer-Verlag: New York, NY, USA)

Wickham H, Girlich M (2022) tidyr: Tidy Messy Data. R package version 1.2.0. Available at https://CRAN.R-project.org/package=tidyr

Wickham H, Seidel D (2020) scales: scale functions for visualization. R package version 1.1.1. Available at https://CRAN.R-project.org/package=scales

Wickham H, François R, Henry L, Müller K (2022a) dplyr: a grammar of data manipulation. R package version 1.0.8. Available at https://CRAN.R-project.org/package=dplyr

Wickham H, Hester J, Bryan J (2022b) readr: read rectangular text data. R package version 2.1.2. Available at https://CRAN.R-project.org/package=readr

Woodford JE, Meyer MW (2003) Impact of lakeshore development on green frog abundance. Biological Conservation 110(2), 277-284.
| Crossref | Google Scholar |