Herpetology Notes, volume 13: 997-1002 (2020) (published online on 01 December 2020)

New records of anuran from the Pedra Talhada Biological Reserve, a Seasonal Semideciduous fragment in northeastern

Marcos Jorge Matias Dubeux1,2,3,*, Ubiratan Gonçalves2,3, Matheus Eduardo Bastos Ramos2,3, Aline Henrique de Melo2,3, Anita da Silva4, and Tamí Mott2,3

Despite centuries of destruction, the Atlantic Forest al., 2006; Ribeiro et al., 2009). Nevertheless, 77 species ecoregion of South America is considered a global of anuran amphibians have been catalogued in this area biodiversity hotspot (Myers et al., 2000). The remaining (Dubeux et al., 2020), 14 of which are endemic, and forest is still remarkably diverse and among the eight seven classified as endangered (ICMBio, 2018; IUCN, recognised sub-regions, there is considerable variation 2020). in human impact, conservation efforts and biological The Pedra Talhada Biological Reserve (PTBR) was knowledge (Silva and Casteleti, 2003; Tabarelli et created in 1989 and is one of the few areas in the BSR al., 2006; Ribeiro et al., 2009). The Pernambuco Pernambuco to be the subject of long-term studies of Biogeographical Sub-Region (BSR Pernambuco; sensu several taxa (Studer et al., 2015). This conservation Ribeiro et al., 2009) located north of the São Francisco unit covers 45 km2 of mainly semideciduous seasonal River (covering the latitudinal range of 5.2500ºS– forests with an altitudinal range from 459 to 883 meters 10.5000ºS) suffers from high anthropogenic impacts, (Tscharner et al., 2015). It is located on the border of low knowledge and few conservation initiatives. This the states of Pernambuco and Alagoas and covers sub-region contains just a few isolated fragments (<100 the municipalities of Quebrangulo and Chã Preta in km2, Ribeiro et al., 2009) and contains only 120 of 1,437 Alagoas and Lagoa do Ouro in Pernambuco (9.1830ºS Atlantic Forest Conservation Units (UCs) (CNUC/ to 9.2660ºS, and 36.3660ºW to 36.4660ºW). The area MMA, 2020) - less than 1% of its current coverage is stands out for its rich hydrography - it contains more protected (Ribeiro et al., 2009). than 168 springs, and numerous reservoirs, streams and This BSR Pernambuco has historically received less dams (Tscharner et al., 2015). The climate is classified attention from naturalists and researchers in comparison as tropical with dry summers; annual temperature range with other sub-regions and, consequently, is the least is 22–24 °C and annual rainfall of 1,000–1,300 mm known of the remaining forest remnants (Tabarelli et (Alvarez et al., 2013). Carvalho-e-Silva et al. (2015) recorded 42 species of 10 families of anuran amphibians for PTBR. This remarkably rich anuran assemblage represents one of the highest diversity communities north of the São Francisco River. Nevertheless, six of the 42 1 Universidade Federal de Pernambuco, Departamento de registered taxa have not been identified at the species Zoologia, Programa de Pós-Graduação em Biologia , level, either because they were registered only through CEP 50670-901 Recife, Pernambuco, Brazil. tadpoles or song characteristics, or because the taxon 2 Universidade Federal de Alagoas, Instituto de Ciências had nomenclatural problems. In this article we document Biológicas e da Saúde, Campus A.C. Simão, CEP 57072-900 nine new anuran species for the PTBR, and provide Maceió, Alagoas, Brazil. additional comments and clarifications on the 3 Universidade Federal de Alagoas, Museu de História Natural, and diversity of amphibians in the area. CEP 57010-020 Maceió, Alagoas, Brazil. 4 Instituto Chico Mendes de Conservação da Biodiversidade Expeditions to the PTBR were made in December (ICMBio), REBIO de Pedra Talhada, CEP 57750-000 2018; January, March, April, June and December Quebrangulo, Alagoas, Brazil. 2019; and February 2020. Each field visit lasted two * Corresponding author. E-mail: [email protected] days, during which a different water body was visited 998 Marcos Jorge Matias Dubeux et al.

Figure 1. New records of anuran amphibians from the Pedra Talhada Biological Reserve, Quebrangulo municipality, Alagoas, Brazil. A= Pristimantis aff. rammagi (not collected); B= Corythomantis greeningi (MUFAL 16110); C= Sphaenorhynchus cammaeus (MUFAL 16118); D= Adenomera aff. hylaedactyla (not collected); E= Leptodactylus macrosternum (MUFAL 16111); F= albifrons (MUFAL 16117); G= Pseudopaludicola mystacalis (not collected); H= Chiasmocleis alagoana (not collected); I= carvalhoi (MUFAL 16114); J= Sphaenorhynchus prasinus (MUFAL 16115). All specimens were photographed in the study area. Photo: G (R. Oliveira). New records of anuran amphibians from the Pedra Talhada Biological Reserve 999 within the conservation unit. These trips were part of The photo of Sphaenorhynchus prasinus in the a larger project that aims to investigate the presence aforementioned work (see Carvalho-e-Silva et al. of the fungus Batrachochytrium dendrobatidis (Bd) in [2015] figure 6.8.30, page 347) is misleading because it the local anurofauna. During the fieldwork campaign, represents an individual of S. cammaeus, described later individuals of new species for the area or those with from this locality by Roberto et al. (2017). However, taxonomic uncertainties were collected (ICMBio/ the occurrence of S. prasinus in the area was confirmed SISBio 66127). Morphological identification was after the collection of two individuals at the Nordesta performed using the available literature or by contacting lagoon (MUFAL 16115-16; Fig. 1J). Although both specialists in the groups. The taxonomic nomenclature species occur in the PTBR, they are not syntopic, follows Frost (2020) and all collected specimens were occupying distinct regions of the conservation unit. deposited in the Coleção Herpetológica do Museu de Sphaenorhynchus prasinus has been found in the weirs História Natural da Universidade Federal de Alagoas and wetlands only in the lowland section of the reserve. (MUFAL). During the 14 days of fieldwork we registered In contrast, S. cammaeus only occurs in the weirs of 28 of the 36 specific taxa registered by Carvalho-e-Silva high-altitude areas, ca. 890 m elevation. et al. (2015) (see Appendix 1 for complete list) and nine Leptodactylus latrans and L. macrosternum are the taxa never before registered in the PTBR (Table 1). only nominal species in the L. latrans species group Carvalho-e-Silva et al. (2015) registered six taxa at registered in Alagoas and Pernambuco states (Moura generic level: Boana sp., Chiasmocleis sp. (recorded et al., 2011; Almeida et al., 2016). Sympatric zones only by the tadpole), Physalaemus sp. (call registration of these species had already been reported (Cei, 1962; only), Pseudopaludicola sp., and two morphotypes Gallardo, 1964). Carvalho-e-Silva et al. (2015) named of Pristimantis designated as Pristimantis sp.1 and figures 6.8.39 and 6.8.40 as L. latrans. Their first photo Pristimantis sp.2. The last five taxa can be represented and the individuals collected here are undeniably L. by Chiasmocleis alagoana, Physalaemus albifrons, macrosternum because they have more than eight dorsal Pseudopaludicola mystacalis and Pristimantis and dorsolateral folds (up to eight folds in L. latrans) aff. ramagii, here identified with adult specimens, and their inguinal region are greenish colour (bluish or respectively. However, because we did not access their gray in L. latrans). voucher material due to the closure of Museums and Additionally, we report three anuran genera never Universities during COVID-19 pandemic, it was not registered for the area. Odontophrynus carvahoi was possible to determine whether these specimens represent recorded by a single individual found in an open area the same nominal taxa. in the access road to ICMBio research accommodation,

Table 1. New records of anuran amphibians from the Pedra Talhada Biological Reserve, Quebrangulo municipality, Alagoas, Brazil.Table 1. New records of anuran amphibians from the Pedra Talhada Biological Reserve, Quebrangulo municipality, Alagoas, Brazil.

Species Voucher Locality Coordinates Source Figure Pristimantis aff. ramagii (Boulenger, 1888) not near the 9.2591ºS Present study Fig. 1A collected Sede dam 36.4303ºW Corythomantis greeningi Boulenger, 1896 MUFAL stream of 9.2586ºS Present study Fig. 1B 16110 Sede dam 36.4303ºW Sphaenorhynchus cammaeus Roberto, Araujo-Vieira, MUFAL Junco lake 9.2395ºS Roberto et al. (2017) Fig. 1C Carvalho-e-Silva & Ávila, 2017 16118 36.4287ºW Present study Adenomera aff. hylaedactyla (Cope, 1868) not stream of 9.2418ºS Present study Fig. 1D collected Timbó 36.4427ºW Leptodactylus macrosternum Miranda-Ribeiro, 1926 MUFAL Carangueja 9.2584ºS Present study Fig. 1E 16111 lagoon 36.4375ºW Physalaemus albifrons (Spix, 1824) MUFAL Carangueja 9.2585ºS Present study Fig. 1F 16117 lagoon 36.4376ºW Pseudopaludicola mystacalis (Cope, 1887) not near Casa de 9.2576ºS Present study Fig. 1G collected Farinha lagoon 36.4407ºW Chiasmocleis alagoana Cruz, Caramaschi & Freire, 1999 not near Cafuringa 9.2511ºS Present study Fig. 1H collected stream 36.4279ºW Odontophrynus carvalhoi Savage & Cei, 1965 MUFAL access road to 9.2612ºS Present study Fig. 1I 16114 ICMBio 36.4283ºW

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1000 Marcos Jorge Matias Dubeux et al. southern portion of the PTBR. Corythomantis greeningi, CNUC/MMA (2020): Cadastro Nacional de Unidades de on the other hand, was collected in a rocky stream in Conservação. Tabela consolidada das Unidades de Conservação, the Sede Dam (adults and tadpoles), and was also MMA, 2016. http://www.mma.gov.br/cadastro_uc. Accessed on 18 April 2020. observed in the Nordesta Dam and close to the ICMBio Dubeux, M.J.M., Nascimento, F.A.C., Lima, L.R., Magalhães, research accommodation. Adenomera aff. hylaedactyla F.M., Silva, I.R.S., Gonçalves, U., et al. (2020): Morphological was photographed in a forest edge area, on the western characterization and taxonomic key of tadpoles (Amphibia: portion of the reserve. Anura) from the northern region of the Atlantic Forest. Biota The Pedra Talhada Biological Reserve hosts an Neotropica 20(2): 1–24. exceptionally diverse and unique assemblage of Frost, D.R. (2020): Amphibian Species of the World: Online anurofauna for the northern Atlantic Forest. Adding Reference. Version 6.0. http://research.amnh.org/herpetology/ amphibia/index.php. Accessed on 18 April 2020. our data to that of Carvalho-e-Silva et al. (2015), and Gallardo, J.M. (1964): Consideraciones sobre Leptodactylus considering only taxa identified at the species level, ocellatus (L.)(Amphibia, Anura) y especies aliadas. Physis there are at least 44 nominal anuran taxa, and others 24(68): 373–384. may be added, since taxonomic uncertainties still ICMBio (2018): Fauna brasileira ameaçada de extinção. In Fauna persist (e.g. Boana sp., Pristimantis sp.2; see Appendix brasileira ameaçada de extinçao. Fundação Biodiversitas para 1 for complete list). The presence of an endemic anuran a Conservação da Diversidade Biológica. Brasília, Distriro species in the area (Sphaenorhynchus cammaeus) and Federal, 492 pp. IUCN (2020): The IUCN Red List of Threatened Species: Online two endangered species (Chiasmocleis alagoana and Reference. Version 2020-1. http://www.iucnredlist.org. Hylomantis granulosa), highlights the importance of Accessed on 18 April 2020. developing conservation strategies to safeguard this Moura, G.J.B., Santos, E.M., Oliveira, M.A.B., Cabral, M.C.C. unique amphibian community in one the most threatened (2011): Herpetofauna no estado de Pernambuco. Instituto parts of the Atlantic Forest. Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Brasília, Distriro Federal, 441 pp. Acknowledgements. The authors thank the Museu de História Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, Natural da Universidade Federal de Alagoas for allowing us to G.A., Kent, J. (2000): Biodiversity hotspots for conservation access the material; researchers I. Martins, G. Silva, H. Vilela, priorities. Nature 403(6772): 853–858. A. Loz, L. Queiroz, R. Oliveira and B. Carnib for the support Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, in the field trips; Instituto Chico Mendes de Conservação da M.M. (2009): The Brazilian Atlantic Forest: How much is left, Biodiversidade – REBIO de Pedra Talhada for logistical support; and how is the remaining forest distributed? Implications for Projeto “Conservação e Valoração da Biodiversidade da ReBio conservation. Biologia e Conservação 142(6): 1141–1153. de Pedra Talhada: uma visão sobre anfíbios e aves” (CNPq- Roberto, I.J., Araujo-Vieira, K., Carvalho-e-Silva, S.P., Ávila, R.W. ICMBio 421305/2017-7) and its research coordinator M. Efe (2017): A new species of Sphaenorhynchus (Anura: ) for support in research development. MJMD thanks Fundação from northeastern Brazil. Herpetologica 73(2): 148–161. de Amparo a Ciência e Tecnologia do Estado de Pernambuco Silva, J.M.C., Casteleti, C.H.M. (2003): Status of the biodiversity - FACEPE (IBPG-1117-2.04/19) and TM thanks Conselho of the Atlantic Forest of Brazil. In: The Atlantic Forest of South Nacional de Desenvolvimento Científico e Tecnológico - CNPq America: Biodiversity Status, Threats, and Outlook, p. 43–59. (309904/2015-3 and 312291/2018-3) for financial support; R. Galindo-Leal, C., Câmara, I.G. TCABS and Island Press, Ladle for English editing; S. Potsch de Carvalho-e-Silva (UFRJ) Washington. and F. Magalhães (UFRN) for the valuable suggestions that Studer, A., Nusbaumer, L., Spichiger, R. (2015): Biodiversidade contributed to the improvement of this work. da Reserva Biológica de Pedra Talhada Alagoas, Pernambuco, Brasil. Boissiera: mémoires des Conservatoire et Jardin botaniques de la Ville de Genève, Pregny-Chambésy, 818 pp. References Tabarelli, M., Siqueira-Filho, J.A., Santos, A.M.M. (2006): Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., Conservação da Floresta Atlântica ao Norte do Rio São Sparovek, G. (2013): Köppen’s climate classification map for Francisco. In: Biodiversidade Biológica e Conservação da Brazil. Meteorologische Zeitschrift 22(6): 711–728. Floresta Atlântica ao Norte do Rio São Francisco, p. 41–48. Carvalho-e-Silva, S.P., Carvalho-e-Silva, A.M.P.T., Luna-Dias, C. Pôrto, K.C., Almeida-Cortez, J.S., Tabarelli M. Ministério do (2015): Anfíbios (Lissamphibia). In: Biodiversidade da Reserva Meio Ambiente, Brasília. Biológica de Pedra Talhada Alagoas, Pernambuco, Brasil, p. Tscharner, T., Duda, G.P., Oliveira, Silva, C.M.S., Nusbaumer, L., 333–356. Studer, A., Nusbaumer, L., Spichiger, R. Boissiera: Filho, A.F.S. (2015): Parâmetros abióticos da Reserva Biológica mémoires des Conservatoire et Jardin botaniques de la Ville de de Pedra Talhada. In: Biodiversidade da Reserva Biológica Genève, Pregny-Chambésy. de Pedra Talhada Alagoas, Pernambuco, Brasil, p. 39–58. Cei, J.M. (1962): Mapa preliminar de la distribución continental de Studer, A., Nusbaumer, L., Spichiger, R. Boissiera: mémoires las “sibling species” del grupo ocellatus (género Leptodactylus). des Conservatoire et Jardin botaniques de la Ville de Genève, Revista de la Sociedad Argentina de Biología 38: 258–265. Pregny-Chambésy. New records of anuran amphibians from the Pedra Talhada Biological Reserve 1001 Appendix 1. Anuran amphibians from the Pedra Talhada Biological Reserve, municipality of AppendixQuebrangulo, 1. Anuran amphibians Alagoas, from Brazil. the Pedra Conservation Talhada Biological status: NAReserve,= Not municipality Available; of VU Quebrangulo,= Vulnerable; Alagoas, Brazil. ConservationLC = status: Least NA Concern;= Not Available;DD= Data VU Deficient;= Vulnerable; EN =LC Endangered.= Least Concern; References: DD= Data 2015 Deficient;= Carvalho-e- EN= Endangered. References:Silva 2015 et= al. Carvalho-e-Silva (2015); 2020 =et Presental. (2015); study. 2020 *=Species Present endemicstudy. *Species this Conservation endemic this Conservation Unit. C= name Unit. C= name corrected.corrected. New records New in bold. records in bold.

SPECIES Conservation status Reference IUCN ICMBio 2015 2020 BUFONIDAE Rhinella crucifer (Wied-Neuwied, 1821) LC LC X X Rhinella granulosa (Spix, 1824) LC LC X X Rhinella jimi (Stevaux, 2002) LC LC X X CRAUGASTORIDAE Haddadus binotatus (Spix, 1824) LC LC X - Pristimantis aff. ramagii (Boulenger, 1888) LC LC - X HYLIDAE Boana albomarginata (Spix, 1824) LC LC X X Boana crepitans (Wied-Neuwied, 1824) LC LC X X Boana exastis (Caramaschi and Rodrigues, 2003) DD LC X X Boana faber (Wild-Neuwied, 1821) LC LC X X Boana raniceps Cope, 1862 LC LC X X Boana semilineata (Spix, 1824) LC LC X X Dendropsophus branneri (Cochran, 1948) LC LC X X Dendropsophus decipiens (Lutz, 1925) LC LC X - Dendropsophus dutrai (Gomes and Peixoto, 1996) DD DD X - Dendropsophus elegans (Wied-Neuwied, 1824) LC LC X X Dendropsophus haddadi (Bastos and Pombal, 1996) LC LC X X Dendropsophus minutus (Peters, 1872) LC LC X X Dendropsophus oliveirai (Bokermann, 1963) LC LC X X Dendropsphus studerae (Carvalho-e-Silva et al. 2003) DD DD X X auratus (Wied-Neuwied, 1821) LC LC X X Scinax eurydice (Bokermann, 1968) LC LC X X Scinax nebulosus (Spix, 1824) LC LC X X Scinax pachycrus (Miranda-Ribeiro, 1937) LC LC X X Scinax x-signatus (Spix, 1824) LC LC X X *Sphaenorhynchus cammaeus Roberto et al. 2017 NA NA C X Sphaenorhynchus prasinus Bokermann, 1973 LC LC -X Trachycephalus mesophaeus (Hensel, 1867) LC LC X - Adenomera aff. hylaedactyla (Cope, 1868) LC LC - X Leptodactylus fuscus (Schneider, 1799) LC LC X X Leptodactylus latrans (Steffen, 1815) LC LC X - Leptodactylus macrosternum Miranda-Ribeiro, 1926 LC LC C X 1 Leptodactylus mystacinus (Burmeister, 1861) LC LC X - Leptodactylus natalensis A. Lutz, 1930 LC LC X X Leptodactylus troglodytes A. Lutz, 1926 LC LC X X Leptodactylus vastus A. Lutz, 1930 LC LC X X Physalaemus albifrons (Spix, 1824) LC LC - X Physalaemus cuvieri Fitzinger, 1826 LC LC X X Pseudopaludicola mystacalis (Cope, 1887) LC LC - X MICROHYLIDAE Chiasmocleis alagoana Cruz, Caramaschi, Freire, 1999 DD EN - X Dermatonotus muelleri (Boettger, 1885) LC LC X - Odontophrynus carvalhoi Savage and Cei, 1965 LC LC - X Proceratophrys renalis (Miranda-Ribeiro, 1920) NA LC X X PHYLLOMEDUSIDAE Hylomantis granulosa Cruz, 1989 “1988” LC VU X X Pithecopus gonzagai Andrade et al. 2020 NA NA X X

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Appendix 1. Anuran amphibians from the Pedra Talhada Biological Reserve, municipality of Quebrangulo, Alagoas, Brazil. Conservation status: NA= Not Available; VU= Vulnerable; 1002 LC= Least Concern; DD= Data Deficient; EN= Endangered. References:Marcos 2015 Jorge= Carvalho-e- Matias Dubeux et al. Silva et al. (2015); 2020= Present study. *Species endemic this Conservation Unit. C= name Appendixcorrected. 1. Continued.Leptodactylus New latransrecords (Steffen, in bold. 1815) LC LC X - Leptodactylus macrosternum Miranda-Ribeiro, 1926 LC LC C X LeptodactylusSPECIES mystacinus (Burmeister, 1861) ConservationLC LC status Reference X - Leptodactylus natalensis A. Lutz, 1930 IUCNLC ICMBio LC 2015 X 2020 X BUFONIDAELeptodactylus troglodytes A. Lutz, 1926 LC LC X X LeptodactylusRhinella crucifer vastus (Wied-Neuwied, A. Lutz, 1930 1821) LC LC X X PhysalaemusRhinella granulosa albifrons (Spix, (Spix, 1824) 1824) LCLC LC X- X PhysalaemusRhinella jimi cuvieri(Stevaux, Fitzinger, 2002) 1826 LLCC LC X X CRAUGASTORIDAEPseudopaludicola mystacalis (Cope, 1887) LC LC - X MICROHYLIDAEHaddadus binotatus (Spix, 1824) LC LC X - PristimantisChiasmocleis aff. alagoana ramagii Cruz, (Boulenger, Caramaschi, 1888) Freire, 1999 DDLC ENLC - X HYLIDAEDermatonotus muelleri (Boettger, 1885) LC LC X - ODONTOPHRYNIDAE Boana albomarginata (Spix, 1824) LC LC X X OdontophrynusBoana crepitans carvalhoi (Wied-Neuwied, Savage 1824)and Cei, 1965 LLCC LC X- X ProceratophrysBoana exastis (Caramaschi renalis (Miranda-Ribeiro, and Rodrigues, 1920) 2003) NDAD LC X X PHYLLOMEDUSIDAEBoana faber (Wild-Neuwied, 1821) LC LC X X HylomantisBoana raniceps granulosa Cope, 1862Cruz, 1989 “1988” LLCC VULC X X PithecopusBoana semilineata gonzagai (Spix, Andrade 1824) et al. 2020 NLCA NALC X X Dendropsophus branneri (Cochran, 1948) LC LC X X Dendropsophus decipiens (Lutz, 1925) LC LC X - Dendropsophus dutrai (Gomes and Peixoto, 1996) DD DD X - Dendropsophus elegans (Wied-Neuwied, 1824) LC LC X X Dendropsophus haddadi (Bastos and Pombal, 1996) LC LC X X Dendropsophus minutus (Peters, 1872) LC LC X X Dendropsophus oliveirai (Bokermann, 1963) LC LC X X Dendropsphus studerae (Carvalho-e-Silva et al. 2003) DD DD X X Scinax auratus (Wied-Neuwied, 1821) LC LC X X Scinax eurydice (Bokermann, 1968) LC LC X X Scinax nebulosus (Spix, 1824) LC LC X X Scinax pachycrus (Miranda-Ribeiro, 1937) LC LC X X Scinax x-signatus (Spix, 1824) LC LC X X *Sphaenorhynchus cammaeus Roberto et al. 2017 NA NA C X Sphaenorhynchus prasinus Bokermann, 1973 LC LC -X Trachycephalus mesophaeus (Hensel, 1867) LC LC X - LEPTODACTYLIDAE Adenomera aff. hylaedactyla (Cope, 1868) LC LC - X Leptodactylus fuscus (Schneider, 1799) LC LC X X

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2 Accepted by Christoph Liedtke