Factors influencing fine-scale occupancy and detectability of an insular Atlantic Forest frog
Caroline Norén Flynn A * , Átilla Colombo Ferreguetti B , Luciana Ardenghi Fusinatto B , Marlon Almeida-Santos B , Fernanda Dias-Silva C D , Helena Godoy Bergallo B and Carlos Frederico D. Rocha BA The Graduate Center, City University of New York, 365 Fifth Avenue, New York, NY 10016, USA.
B Department of Ecology, Universidade do Estado do Rio de Janeiro, Pavilhão Haroldo Lisboa da Cunha, Rua São Francisco Xavier, n° 524, Maracanã, Rio de Janeiro, RJ 20550-013, Brazil.
C Herpetology Sector, Department of Vertebrates, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão, Rio de Janeiro, RJ 20940-040, Brazil.
D Bioscience Institute, Universidade Federal do Estado do Rio de Janeiro, Av. Pasteur, Urca, Rio de Janeiro, RJ 22290-240, Brazil.
Abstract
Species of the tropical frog Family Hylodidae tend to be restricted to streams and, hence, have a small occupancy area. Hylodes fredi (Canedo and Pombal 2007), a diurnal stream-dwelling species endemic to the Atlantic Forest in Ilha Grande, south-eastern Brazil, is one such species. Because of scarce population studies, it is also categorised as Data Deficient (DD) in the IUCN Red List. Previous studies on the habitat use by this species did not account for imperfect detection, which could have led to biased results.
We aimed to systematically describe the microhabitats occupied by H. fredi, by generating a fine-scale occupancy model while accounting for imperfect detection.
We sampled six streams where the species is known to occur. Perpendicular transects were established in each stream and further subdivided into 10 sampling plots. Single-species and single-season occupancy models were created with the UNMARKED R package, and model selection was performed on the basis of the Akaike information criterion.
We observed the species in 70 of the 275 sampled sites, which resulted in a naïve occupancy of 0.28 and detectability of 0.25. The best models suggest that H. fredi occupancy increases positively with rock cover and inversely with leaf-litter cover. Detectability reduced with an increase in leaf litter cover and varied with the air temperature.
We conclude that H. fredi occupancy is affected by the presence of rock and leaf-litter cover. The data indicated that the species is restricted to the stream channel and does not seem to occupy forested areas that are distanced from the stream margins.
Considering that H. fredi and many other congeneric species are listed as ‘Data Deficient’ in the IUCN Red List, it is important to define a threat category so as to conserve them. Many stream-associated species tend to have their occupancy overestimated, leading to an underestimation of their threat risk. This study systematically demonstrated that H. fredi has a strict and reduced occupancy, mostly limited to the stream margins, that should be considered when determining conservation efforts for this and ecologically similar species.
Keywords: Atlantic Forest, biodiversity conservation, detection probability, Hylodes, microhabitat, occupancy modeling, population ecology, stream-dwelling.
References
Alho CJR, Schneider M, Vasconcellos LA (2002) Degree of threat to the biological diversity in the Ilha Grande State Park (RJ) and guidelines for conservation. Brazilian Journal of Biology 62, 375-385.
| Crossref | Google Scholar |
Almeida-Gomes M, Rocha CFD (2014) Landscape connectivity may explain anuran species distribution in an Atlantic forest fragmented area. Landscape Ecology 29, 29-40.
| Crossref | Google Scholar |
Almeida-Gomes M, Hatano FH, Van Sluys M, Rocha CFD (2007) Diet and microhabitat use by two Hylodinae species (Anura, Cycloramphidae) living in sympatry and syntopy in a Brazilian Atlantic Rainforest area. Iheringia. Série Zoologia 97, 27-30.
| Crossref | Google Scholar |
Almeida-Gomes M, Lorini ML, Rocha CFD, Vieira MV (2014) Underestimation of extinction threat to stream-dwelling amphibians due to lack of consideration of narrow area of occupancy. Conservation Biology 28, 616-619.
| Crossref | Google Scholar |
Almeida-Gomes M, Rocha CFD, Vieira MV (2015) Anuran community composition along two large rivers in a tropical disturbed landscape. Zoologia (Curitiba) 32, 9-13.
| Crossref | Google Scholar |
Bridges AS, Dorcas ME (2000) Temporal variation in anuran calling behavior: implications for surveys and monitoring programs. Copeia 2000, 587-592.
| Crossref | Google Scholar |
Canedo C, Pombal JP (2007) Two new species of torrent frog of the genus Hylodes (Anura, Hylodidae) with nuptial thumb tubercles. Herpetologica 63, 224-235.
| Crossref | Google Scholar |
de Oliveira Machado A, Winck G, Dorigo TA, Rocha CFD (2016) Diet, diel activity pattern, habitat use, and reproductive effort of Hylodes nasus (Anura: Hylodidae) in one of the world’s largest urban parks (Tijuca National Park), southeastern Brazil. South American Journal of Herpetology 11(2), 127-135.
| Crossref | Google Scholar |
de Sá FP, Canedo C, Lyra ML, Haddad CFB (2015) A new species of Hylodes (Anura, Hylodidae) and its secretive underwater breeding behavior. Herpetologica 71, 58.
| Crossref | Google Scholar |
Dormann CF, McPherson JM, Araújo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, Kühn I, Ohlemüller R, Peres-Neto PR, Reineking B, Schröder B, Schurr FM, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30(5), 609-628.
| Crossref | Google Scholar |
Fatorelli P, Nogueira-Costa P, Rocha CFD (2018) Characterization of tadpoles of the southward portion (oceanic face) of Ilha Grande, Rio de Janeiro, Brazil, with a proposal for identification key. North-Western Journal of Zoology 14, 171-184.
| Google Scholar |
Fiske I, Chandler R (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. Journal of Statistical Software 43, 1-23.
| Crossref | Google Scholar |
Frost DR (2023) Amphibian Species of the World: an Online Reference. Version 6.1 (1 June 2023). Electronic Database accessible at https://amphibiansoftheworld.amnh.org/index.php. American Museum of Natural History, New York, USA. doi:10.5531/db.vz.0001
Hatano FH, Rocha CFD, Van Sluys M (2002) Environmental factors affecting calling activity of a tropical diurnal frog (Hylodes phyllodes: Leptodactylidae). Journal of Herpetology 36, 314-318.
| Crossref | Google Scholar |
Heyer WR, Rand AS, Cruz CAG, Peixoto OL, Nelson CE (1990) Frogs of Boracéia. Arquivos de Zoologia 31, 231-410.
| Google Scholar |
INEA (2011) Plano de Manejo do Parque Estadual da Ilha Grande. Available at http://www.inea.rj.gov.br/ [Accessed 20 March 2022]
INPA (2012) Roteiro para Levantamentos e Monitoramento de Peixes em grades e módulos RAPELD do PPBio. Available at https://ppbio.inpa.gov.br/manuais/ [Accessed 15 November 2020]
IUCN (2022) The IUCN red list of threatened species. Version 2021-3. Available at https://www.iucnredlist.org/ [Accessed 20 March 2022]
Laia RC, Fatorelli P, Hatano FH, Duarte Rocha CF, Rocha CFD (2010) Tadpole of Hylodes fredi (Anura; Hylodidae), a frog endemic to an Atlantic Forest island (Ilha Grande, Rio de Janeiro state), Brazil. Zootaxa 2640, 62-64.
| Crossref | Google Scholar |
Lima NGS, Oliveira U, Souza RCC, Eterovick PC (2019) Dynamic and diverse amphibian assemblages: can we differentiate natural processes from human induced changes? PLoS ONE 14 e0214316.
| Crossref | Google Scholar |
McGrath T, Guillera-Arroita G, Lahoz-Monfort JJ, Osborne W, Hunter D, Sarre SD (2015) Accounting for detectability when surveying for rare or declining reptiles: turning rocks to find the Grassland Earless Dragon in Australia. Biological Conservation 182, 53-62.
| Crossref | Google Scholar |
Motta-Tavares T, de Godoy Bergallo H, Nogueira CCR, Rocha CFD (2019) Geographic and altitudinal distribution of the insular endemic frog Hylodes fredi (Anura: Hylodidae) of the Atlantic coast of southeastern Brazil. Journal of Coastal Conservation 23, 615-621.
| Crossref | Google Scholar |
Navas CA, Gomes FR, Carvalho JE (2008) Thermal relationships and exercise physiology in anuran amphibians: integration and evolutionary implications. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 151(3), 344-362.
| Crossref | Google Scholar |
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/
Rocha CFD, Van Sluys M, Hatano FH (1997) Hylodes phyllodes (Leaf frog). Geographic distribution. Herpetological Review 28, 208.
| Google Scholar |
Rocha CFD, Van Sluys M, Alves MAS, Bergallo HG, Vrcibradic D (2000) Activity of leaf-litter frogs : when should frogs be sampled ? Journal of Herpetology 34, 285-287.
| Crossref | Google Scholar |
Rocha CFD, Van Sluys M, Alves MAS, Bergallo HG, Vrcibradic D (2001) Estimates of forest floor litter frog communities: a comparison of two methods. Austral Ecology 26, 14-21.
| Crossref | Google Scholar |
Rowley JJL, Alford RA (2007) Movement patterns and habitat use of rainforest stream frogs in northern Queensland, Australia: implications for extinction vulnerability. Wildlife Research 34(5), 371-378.
| Crossref | Google Scholar |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675 Available at https://imagej.nih.gov/ij/index.html.
| Crossref | Google Scholar |
Segalla MV, Caramaschi U, Cruz CAG, Garcia PCA, Grant T, Haddad CFB, Santana DJ, Toledo LF, Langone JA (2019) Brazilian amphibians: list of species. Herpetologia Brasileira 1, 65-96.
| Google Scholar |
Shoemaker VH, Hillman SS, Hillyard SD, Jackson DC, Mcclanahan LL, Withers P, Wygoda M (1992) Exchange of water, ions and respiratory gases in terrestrial amphibians. In ‘Environmental physiology of the amphibians’. (Eds M Feder, W Burggren) pp. 125–150. (The University of Chicago Press: Chicago, IL, USA)
Silva HRd, Benmaman P (2008) Uma nova espécie de Hylodes Fitzinger da Serra da Mantiqueira, Minas Gerais, Brasil (Anura: Hylodidae). Revista Brasileira de Zoologia 25, 89-99.
| Crossref | Google Scholar |
Van Sluys M, Vrcibradic D, Alves MAS, Bergallo HG, Rocha CFD (2007) Ecological parameters of the leaf-litter frog community of an Atlantic Rainforest area at Ilha Grande, Rio de Janeiro state, Brazil. Austral Ecology 32, 254-260.
| Crossref | Google Scholar |