Research Article |
Corresponding author: Rodrigo Barbosa Ferreira ( rodrigoecologia@yahoo.com.br ) Academic editor: Angelica Crottini
© 2019 Rodrigo Barbosa Ferreira, Alexander Tamanini Mônico, Emanuel Teixeira da Silva, Fernanda Cristina Ferreira Lirio, Cássio Zocca, Marcio Marques Mageski, João Filipe Riva Tonini, Karen H. Beard, Charles Duca, Thiago Silva-Soares.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ferreira RB, Mônico AT, da Silva ET, Lirio FCF, Zocca C, Mageski MM, Tonini JFR, Beard KH, Duca C, Silva-Soares T (2019) Amphibians of Santa Teresa, Brazil: the hotspot further evaluated. ZooKeys 857: 139-162. https://doi.org/10.3897/zookeys.857.30302
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A checklist of the amphibians of Santa Teresa municipality, in southeastern Brazil is presented based on fieldwork, examination of specimens in collections, and a literature review. This new amphibian list of Santa Teresa includes 108 species, of which 106 (~98%) belong to Anura and two (~2%) to Gymnophiona. Hylidae was the most represented family with 47 species (43%). Compared to the previous amphibian lists for Santa Teresa, 14 species were added, 17 previously reported species were removed, and 13 species were re-identified based on recent taxonomic rearrangements. Of the 14 species added, 11 (79%) were first recorded during our fieldwork and specimen examination. It is also the first list of caecilians for Santa Teresa. This list suggests that Santa Teresa has 0.16 species per km2 (i.e., 108 species/683 km2), one of the highest densities of amphibian species in the world at a regional scale. This richness represents 78% of the 136 anurans from Espírito Santo state and 10% of the 1,080 amphibians from Brazil. We highlight the need for long-term monitoring to understand population trends and develop effective conservation plans to safeguard this remarkable amphibian richness.
Anura, Atlantic Forest, Caecilians, Diversity, Espírito Santo, Inventory
Species checklists provide a scientific value to areas by identifying the richness that is threatened given anthropogenic actions. The Brazilian Amphibian Conservation Action plan recognizes that species lists are a scientific priority for many areas across Brazil (
The Atlantic Forest harbors 625 anuran species and 14 caecilians (
Santa Teresa is also a hotspot for several other taxa, such as plants (
The municipality of Santa Teresa has 683 km2 and is located in the mountainous region (altitude range: ~120–1099 m a.s.l.) of Espírito Santo state, southeastern Brazil (19°56'14"S, 40°35'52"W; Figure
The predominant vegetation types are montane and sub-montane rainforests (
The climate of Santa Teresa is classified as oceanic climate without dry season and with temperate summer (Cfb) according to Köppen classification (
The species list presented in this study has been compiled in part using field surveys conducted by the authors from 2006 to 2019, and also through the evaluation of specimens in zoological collections (see Appendix I) and a literature review.
During field surveys, we conducted intensive sampling across Santa Teresa using audio and visual searches inside bromeliads, in the leaf litter, and in water bodies (see
We also reviewed the literature and compiled records of amphibians for Santa Teresa. In addition, we examined specimens deposited in the following institutions: Coleção de Anfíbios Célio F. B. Haddad (CFBH), Universidade Estadual Paulista (
We recorded 108 amphibian species for Santa Teresa, of which 106 (98%) belong to Anura (16 families and 41 genera) and two (2%) to Gymnophiona (one family and one genus) (Table
Amphibians from Santa Teresa: A Allobates capixaba B Brachycephalus alipioi C Ischnocnema abdita D Ischnocnema colibri E Ischnocnema cf. nasuta F Ischnocnema aff. guentheri G Ischnocnema oea H Ischnocnema gr. parva sp. new 1 I Ischnocnema gr. parva sp. new 2 J Ischnocnema verrucosa K Dendrophryniscus carvalhoi L Rhinella crucifer M Rhinella granulosa N Rhinella diptycha O Vitreorana aff. eurygnatha. Photographs by JFR Tonini (A), CN Fraga (B), RB Ferreira (C, D, H, I, K), AT Mônico (E, G, J, K, L, M, N, O), T Silva-Soares (F).
Amphibians from Santa Teresa: A Vitreorana uranoscopa B Euparkerella tridactyla C Haddadus binotatus D Thoropa miliaris E Zachaenus carvalhoi F Adelophryne glandulata G Fritziana aff. fissilis H Fritziana tonimi I Gastrotheca megacephala J Aparasphenodon brunoi K Aplastodiscus cavicola L Aplastodiscus aff. eugenioi M Aplastodiscus weygoldti N Boana albomarginata O Boana albopunctata. Photographs by AT Mônico (A, C, D, G, H, K, L, O), RB Ferreira (B, E, F, I, N), C Zocca (J), T Silva-Soares (M).
Amphibians from Santa Teresa: A Boana crepitans B Boana faber C Boana pardalis D Boana polytaenia E Boana semilineata F Bokermannohyla caramaschii G Dendropsophus berthalutzae H Dendropsophus bipunctatus I Dendropsophus branneri J Dendropsophus bromeliaceus K Dendropsophus decipiens L Dendropsophus elegans M Dendropsophus giesleri N Dendropsophus haddadi O Dendropsophus microps. Photographs by AT Mônico (A, C, D, E, F, H, L, M, N, O), RB Ferreira (B, G, I, J), ET Silva (K).
Compared to previous anuran lists for Santa Teresa, we added 14 species, removed 17 previously reported species, and re-determined 14 species based on recent taxonomic rearrangements. Out of the 14 added species, 11 (79%) were first recorded during our fieldwork and specimen examination, two (14%) records were from the literature, and one (7%) new record was from pers. comm. (Gastrotheca ernestoi; MT Rodrigues, field number MTR 34695).
Fourteen species classified to morphotypes are new species, such as Aplastodiscus aff. eugenioi (M Mongin, pers. comm.), Brachycephalus aff. didactylus (TSS, in. prep.), Crossodactylus aff. gaudichaudii (R Montesinos, in. prep.), Fritziana aff. fissilis (RBF, pers. obs.), Ischnocnema aff. parva sp. 1 (CAG Cruz, in. prep.), Ischnocnema aff. parva sp. 2 (TSS, in. prep.), Leptodactylus aff. spixi (L Nascimento, in. prep.), Ololygon aff. heyeri (J Lacerda, pers. comm.), Phyllodytes aff. luteolus (ATM, in. prep.), Pipa aff. carvalhoi (PV Scherrer, in. prep.), Pithecopus aff. rohdei (D Baêta, pers. comm.), Scinax aff. perereca (TSS, pers. comm.), Thoropa aff. lutzi (CL Assis, pers. comm.), and Vitreorana aff. eurygnatha (R Pontes, in. prep.).
Amphibians from Santa Teresa: A Dendropsophus minutus B Dendropsophus ruschii C Dendropsophus seniculus D Itapotihyla langsdorffii E Ololygon arduous F Ololygon argyreornata G Ololygon heyeri H Ololygon kautskyi I Pithecopus aff. rohdei J Phasmahyla exilis K Phyllomedusa burmeisteri L Phyllodytes kautskyi M Phyllodytes luteolus N Phyllodytes aff. luteolus O Scinax alter. Photographs by RB Ferreira (A, D, J), AT Mônico (B, C, E, F, G, I, K, N, O), T Silva-Soares (H), CZ Zocca (L, M).
Amphibians from Santa Teresa: A Scinax cuspidatus B Scinax eurydice C Scinax fuscovarius D Scinax hayii E Scinax aff. perereca F Scinax cf. x-signatus G Trachycephalus mesophaeus H Trachycephalus nigromaculatus I Crossodactylus aff. gaudichaudii J Crossodactylus timbuhy K Hylodes lateristrigatus L Crossodactylodes bokermanni M Crossodactylodes izecksohni N Leptodactylus cupreus O Leptodactylus fuscus. Photographs by ET Silva (A, E, F), CZ Zocca (B, O), T Silva-Soares (C), AT Mônico (D, I, K, L), RB Ferreira (G, H, J, M), JFR Tonini (N).
Amphibians from Santa Teresa: A Leptodactylus aff. latrans B Leptodactylus aff. spixi C Physalaemus crombiei D Physalaemus cuvieri E Physalaemus maculiventris F Chiasmocleis capixaba G Chiasmocleis schubarti H Myersiella microps I Proceratophrys boiei J Proceratophrys laticeps K Proceratophrys paviotii L Proceratophrys schirchi M Pipa aff. carvalhoi N Siphonops annulatus O Siphonops hardyi. Photographs by T Silva-Soares (A, B, L, M, N), AT Mônico (C, D, E, G, H, J, K), RB Ferreira (F, I, O).
Amphibian species of Santa Teresa municipality, Espírito Santo state, Southeastern Brazil. An asterisk * indicates a taxonomic change.
Species by Family | Type locality | Our study |
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AROMOBATIDAE | ||||
Allobates capixaba (Lutz, 1925) | X | X | X* | |
BRACHYCEPHALIDAE | ||||
Brachycephalus alipioi Pombal & Gasparini, 2006 | X | X | – | |
Brachycephalus aff. didactylus | X | – | – | |
Ischnocnema abdita Canedo & Pimenta, 2010 | X | X | X | – |
Ischnocnema colibri Taucce, Canedo, Parreiras, Drummond, Nogueira-Costa & Haddad, 2018 | X | X | – | – |
Ischnocnema epipeda (Heyer, 1984) | X | X | X | X |
Ischnocnema aff. guentheri | X | X* | X* | |
Ischnocnema cf. nasuta (Lutz, 1925) | X | X* | X* | |
Ischnocnema oea (Heyer, 1984) | X | X | X | X |
Ischnocnema aff. parva sp. 1 | X | X* | X* | |
Ischnocnema aff. parva sp. 2 | X | – | – | |
Ischnocnema verrucosa Reinhardt & Lütken, 1862 | X | X | X | |
BUFONIDAE | ||||
Dendrophryniscus carvalhoi Izecksohn, 1994 | X | X | X | X |
Rhinella crucifer (Wied-Neuwied, 1821) | X | X | X | |
Rhinella granulosa (Spix, 1824) | X | X | X | |
Rhinella diptycha (Cope, 1862) | X | X | X | |
CENTROLENIDAE | ||||
Vitreorana aff. eurygnatha | X | X* | X* | |
Vitreorana uranoscopa (Müller, 1924) | X | X | X | |
CERATOPHRYIDAE | ||||
Ceratophrys aurita (Raddi, 1823) | X | X | X* | |
CRAUGASTORIDAE | ||||
Euparkerella tridactyla Izecksohn, 1988 | X | X | X | X |
Haddadus binotatus (Spix, 1824) | X | X | X | |
CYCLORAMPHIDAE | ||||
Cycloramphus fuliginosus Tschudi, 1838 | X | X | X | |
Thoropa aff. lutzi | X | X* | – | |
Thoropa miliaris (Spix, 1824) | X | X | X | |
Thoropa petropolitana (Wandolleck, 1907) | X | X | – | |
Zachaenus carvalhoi Izecksohn, 1983 | X | X | X | X |
ELEUTHERODACTYLIDAE | ||||
Adelophryne glandulata Lourenço-de-Moraes, Ferreira, Fouquet & Bastos, 2014 | X | X | X* | – |
HEMIPHRACTIDAE | ||||
Fritziana aff. fissilis | X | X* | X* | |
Fritziana tonimi Walker, Gasparini, Haddad, 2016 | X | X | X* | X* |
Gastrotheca albolineata (Lutz & Lutz, 1939) | X | X | – | |
Gastrotheca ernestoi Miranda-Ribeiro, 1920 | X | – | – | |
Gastrotheca megacephala Izecksohn, Carvalho-e-Silva & Peixoto, 2009 | X | – | – | |
HYLIDAE | ||||
Aparasphenodon brunoi Miranda-Ribeiro, 1920 | X | – | X | |
Aplastodiscus cavicola (Cruz & Peixoto, 1985) | X | X | X | X |
Aplastodiscus aff. eugenioi | X | – | – | |
Aplastodiscus weygoldti (Cruz & Peixoto, 1987) | X | X | X | X |
Boana albomarginata (Spix, 1824) | X | X | X | |
Boana albopunctata (Spix, 1824) | X | X | X | |
Boana crepitans (Wied-Neuwied, 1824) | X | X | X | |
Boana faber (Wied-Neuwied, 1821) | X | X | X | |
Boana pardalis (Spix, 1824) | X | X | X | |
Boana polytaenia (Cope, 1870) | X | X | – | |
Boana semilineata (Spix, 1824) | X | X | X | |
Bokermannohyla caramaschii (Napoli, 2005) | X | X | X | X |
Dendropsophus berthalutzae (Bokermann, 1962) | X | X | X | |
Dendropsophus bipunctatus (Spix, 1824) | X | X | X | |
Dendropsophus branneri (Cochran, 1948) | X | X | X | |
Dendropsophus bromeliaceus Ferreira, Faivovich, Beard & Pombal, 2015 | X | X | – | – |
Dendropsophus decipiens (Lutz, 1925) | X | X | X | |
Dendropsophus elegans (Wied-Neuwied, 1824) | X | X | X | |
Dendropsophus giesleri (Mertens, 1950) | X | X | X | |
Dendropsophus haddadi (Bastos & Pombal, 1996) | X | X | X | |
Dendropsophus microps (Peters, 1872) | X | X | X | |
Dendropsophus minutus (Peters, 1872) | X | X | X | |
Dendropsophus ruschii (Weygoldt & Peixoto, 1987) | X | X | X | |
Dendropsophus seniculus (Cope, 1868) | X | X | X | |
Itapotihyla langsdorffii (Duméril & Bibron, 1841) | X | X | X | |
Ololygon arduous (Peixoto, 2002) | X | X | X | X |
Ololygon argyreornata (Miranda-Ribeiro, 1926) | X | X | X | |
Ololygon cf. flavoguttata (Lutz & Lutz, 1939) | X | – | – | |
Ololygon aff. heyeri | X | – | – | |
Ololygon heyeri Peixoto & Weygoldt, 1986 | X | X | X | X |
Ololygon kautskyi Carvalho-e-Silva & Peixoto, 1991 | X | X | X | |
Phasmahyla exilis (Cruz, 1980) | X | X | X | X |
Phrynomedusa marginata (Izecksohn & Cruz, 1976) | X | X | X | X |
Phyllodytes kautskyi Peixoto & Cruz, 1988 | X | – | – | |
Phyllodytes luteolus (Wied-Neuwied, 1824) | X | X | X | |
Phyllodytes aff. luteolus | X | – | – | |
Phyllomedusa burmeisteri Boulenger, 1882 | X | X | X | |
Pithecopus aff. rohdei | X | X* | X* | |
Scinax alter (Lutz, 1973) | X | X | X | |
Scinax cuspidatus (Lutz, 1925) | X | X | X | |
Scinax eurydice (Bokermann, 1968) | X | X | X* | |
Scinax fuscovarius (Lutz, 1925) | X | X | X | |
Scinax hayii (Barbour, 1909) | X | X | X* | |
Scinax aff. perereca | X | – | – | |
Scinax cf. x-signatus (Spix, 1824) | X | X | X | |
Trachycephalus mesophaeus (Hensel, 1867) | X | X | X | |
Trachycephalus nigromaculatus Tschudi, 1838 | X | X | X | |
HYLODIDAE | ||||
Crossodactylus aff. gaudichaudii | X | X | X* | |
Crossodactylus timbuhy Pimenta, Cruz & Caramaschi, 2014 | X | X | X* | X* |
Hylodes cf. babax Heyer, 1982 | X | X* | X* | |
Hylodes lateristrigatus (Baumann, 1912) | X | X | X | |
Megaelosia apuana Pombal, Prado & Canedo, 2003 | X | X | X* | |
LEPTODACTYLIDAE | ||||
Crossodactylodes bokermanni Peixoto, 1983 | X | X | X | X |
Crossodactylodes izecksohni Peixoto, 1983 | X | X | X | X |
Leptodactylus cupreus Caramaschi, Feio & São Pedro, 2008 | X | X | – | |
Leptodactylus fuscus (Schneider, 1799) | X | X | X | |
Leptodactylus aff. latrans (Steffen, 1815) | X | X* | X* | |
Leptodactylus aff. spixi | X | X* | X* | |
Physalaemus crombiei Heyer & Wolf, 1989 | X | X | X | X |
Physalaemus cuvieri Fitzinger, 1826 | X | X | X | |
Physalaemus maculiventris (Lutz, 1925) | X | X | – | |
Physalaemus cf. olfersii (Lichtenstein & Martens, 1856) | X | X* | X* | |
MICROHYLIDAE | ||||
Chiasmocleis capixaba Cruz, Caramaschi & Izecksohn, 1997 | X | – | – | |
Chiasmocleis schubarti Bokermann, 1952 | X | – | X | |
Myersiella microps (Duméril & Bibron, 1841) | X | X | X | |
ODONTOPHRYNIDAE | ||||
Macrogenioglottus alipioi Carvalho, 1946 | X | X | X | |
Proceratophrys boiei (Wied-Neuwied, 1824) | X | X | X | |
Proceratophrys laticeps Izecksohn & Peixoto, 1981 | X | X | X | |
Proceratophrys moehringi Weygoldt & Peixoto, 1985 | X | X | X | X |
Proceratophrys paviotii Cruz, Prado & Izecksohn, 2005 | X | X | X | X |
Proceratophrys phyllostomus Izecksohn, Cruz & Peixoto, 1999 | X | X | X | |
Proceratophrys schirchi (Miranda-Ribeiro, 1937) | X | X | X | |
PIPIDAE | ||||
Pipa aff. carvalhoi | X | X* | X* | |
RANIDAE | ||||
Lithobates catesbeianus (Shaw, 1802) | X | – | – | |
SIPHONOPIDAE | ||||
Siphonops annulatus (Mikan, 1822) | X | – | – | |
Siphonops hardyi Boulenger, 1888 | X | – | – |
The current number of 106 anuran species for Santa Teresa is remarkable, and represents 78% of the 136 species listed for Espírito Santo state (
The two species of Gymnophiona (Siphonops annulatus and S. hardyi) were found during our fieldwork but have been reported previously for Santa Teresa (
Our fieldwork since 2005 in Santa Teresa has made notable contributions toward the knowledge of local amphibians. It has resulted in the description of three new species for the municipality (i.e., Adelophryne glandulata in Lourenço-de-Moraes, Ferreira, Fouquet, Bastos 2014, Dendropsophus bromeliaceus in Ferreira, Faivovich, Beard, Pombal 2015, and Ischnocnema colibri in Taucce, Canedo, Parreiras, Drummond, Nogueira-Costa, Haddad 2018). Furthermore, our fieldwork found individuals of 13 morphospecies that are currently under formal description (i.e., Aplastodiscus aff. eugenioi, Brachycephalus aff. didactylus, Crossodactylus aff. gaudichaudii, Fritziana aff. fissilis, Ischnocnema aff. parva sp. 1, Ischnocnema aff. parva sp. 2, Leptodactylus aff. spixi, Ololygon aff. heyeri, Phyllodytes aff. luteolus, Pipa aff. carvalhoi, Pithecopus aff. rohdei, Scinax aff. perereca, and Vitreorana aff. eurygnatha). The discovery of new species, morphospecies, and new records for Santa Teresa may be due to our sampling in remote forested areas and rocky outcrops through both visual bromeliad surveys and active leaf-litter searches (
Our species list resolved some differences between the previous species lists of Santa Teresa, which had disagreements on 11 species (e.g.,
The wide elevational range of Santa Teresa (~120–1099 m a.s.l.) partially explains the high richness of amphibian species. Species typical of both Atlantic Forest lowlands (e.g., Allobates capixaba, Chiasmocleis schubarti, C. capixaba, Dendropsophus bipunctatus, Ololygon argyreornata) and highlands (e.g., Aplastodiscus cavicola, Bokermannohyla caramaschii, Dendropsophus ruschii) occur in Santa Teresa, which suggest that the elevational gradient influences species composition. The high amphibian diversity also may be related to edaphic and topographic heterogeneity, which is known to cause speciation in many Atlantic Forest species occurring in mountainous areas (
Amphibians from Santa Teresa have faced several anthropogenic disturbances over the last couple of decades. The first report on amphibian declines for Santa Teresa was in 1989 (see
Over the decades, we have noted population disappearances of anurans in Santa Teresa. The construction of condominiums and vacation ranches has intensified over the last decade and consequently increased deforestation of primary forest. We have also observed the expansion of the non-native Eucalyptus spp. plantations near primary and secondary forests and the replacement of coffee plantations. Another unmeasured concern is the increasing record of morphological anuran deformities, which is likely a result of pesticides used on crops (e.g.,
The landscape configuration of Santa Teresa does not safeguard the maintenance of amphibian reproduction outside protected reserves because forests on private properties are mostly restricted to hilltops and non-natural matrix habitats occupy most valleys. Because water-body breeding species migrate toward reproductive habitats in the valleys, these species face severe threats, such as the risk of predation and desiccation (
Santa Teresa is an important hotspot for amphibian conservation due to its high richness and number of endemic species. The discovery of several new species further emphasizes the importance of this mountainous region for amphibian conservation. Even though Santa Teresa and its surrounding areas in southeastern Brazil are one of the most sampled regions in the Atlantic Forest, the region still harbors numerous remote areas that have not yet been sampled for frogs (e.g.,
We dedicated this manuscript to Rogério L Teixeira who was born and raised in Santa Teresa and dedicated decades sampling frogs and mentoring herpetologists. We thank Bromeligenous Project for field support; landowners for allowing access to their properties; Instituto Nacional da Mata Atlântica for logistic support. We are grateful to Cecilia Waichert, Francys Lacchine, Gustavo Milanezi, Jandyra Zocca Zandomenico, Juliano Saich, Lamara P Barbosa, Namany Lourpen, Paulo R Jesus, Randerson LB Ferreira for field sampling. We especially thank Carlos A Cruz, Clarissa Canedo, Clodoaldo L Assis, Délio Baeta, Gustavo Prado, João V Lacerda, Juliana Kirchmeyer, Juliana Peres, Leo Malagoli, Marcele Mongin, Marco A Peixoto, Miguel Trefault Rodrigues, Paulo V Scherrer, Pedro Taucce, Rafael Pontes, Raquel Montesinos, and Victor Dill for discussions on species identification. Sampling permits were issued by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio, permits 28607, 50402, and 63575) and Institutional Animal Care and Use Committee (IACUC-USU, permit 2002). RBF (0823/FCLF (001/1774502), and CZZ (001/1700071) thank Coordenação de Aperfeiçoamento Pessoal de Nível Superior - Brasil (CAPES) for scholarships. RBF, ATM, ETS and TSS thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq: 430195/2018, 304374/2016-4, 141569/2014-0, and 454789/2015-7) for scholarships. JFRT thanks CAPES/Science without Borders and David Rockefeller Center for Latin Studies/Harvard University for scholarships. This research was supported by the Utah Agricultural Experiment Station, Utah State University, and approved as journal paper number 9217 and by Harvard Open Access Equity Fund (HOPE).
Vouchers of examined specimens
Adelophryne glandulata (