Anurans of Amapá National Forest, Eastern Amazonia, Brazil

Home , Adenomera andreae, Adenomera hylaedactyla, Dendropsophus brevifrons, Dendropsophus minusculus, Dendropsophus nanus, Dendropsophus parviceps

Herpetology Notes, volume 10: 627-633 (2017) (published online on 10 November 2017)

Ronildo Alves Benício1,* and Jucivaldo Dias Lima2

Abstract. Eastern Amazonia has an elevated biological diversity and a relatively high degree of preservation. However, there are still considerable gaps in knowledge about the herpetofauna of the area. The anuran fauna of the Brazilian Amapá State is little known and the studies are scarce. Here, we present the first list of species of anurans of Amapá National Forest, Eastern Amazonia. We recorded a total of 53 species of anurans, being the inventory with the second highest number of specimens registered in Amapá State. We present the conservation status of the species and discuss species diversity in comparison to other areas. Amapá State presents a knowledge gap about its anurans with only five published inventories from localities throughout the State.

Keywords: Amphibians, Conservation Unit, Conservation Status, FLONA Amapá, Guiana Shield

Introduction conservation status, little is known about the diversity of amphibians of this part of Eastern Amazonia. Currently there are 7,729 species of amphibians in To date, 156 species of amphibians have been the world, and the Neotropical region is home to the recorded for Tumucumaque Mountains National Park greatest diversity of amphibians (Frost, 2017). Brazil (Amapá State), being one of the regions with elevated is the country with the greatest richness of the world’s species richness in the Guiana Shield (Lima, 2008). amphibians, with 1,080 species described to date, of Specifically, Amapá State was little studied in relation to which 60% are endemic (Segalla et al., 2016). their anuran fauna (e.g., Bitar et al., 2017): the majority Brazilian Amazonia is home to 308 species of anurans of studies are descriptions of species and new records (Hoogmoed & Galatti, 2017), which represents 29% of species’ occurrences (Bokermann, 1967; Silverstone, of all species of Brazilian anurans. Located in Eastern 1975, 1976; Hoogmoed, 1979a,b; Hoogmoed & Gruber, Amazonia, Amapá State is part of the Guiana Shield, 1983; Caldwell & Hoogmoed, 1998; Señaris & Avila- and has an elevated diversity of habitats such as terra Pires, 2003; Señaris & MacCuolloch, 2005; Avila-Pires firme (upland) forests, flooded forests, complex lakes, et al., 2007; Costa-Campos et al., 2014; Silva e Silva extensive portions of mangrove, vegetation types & Costa-Campos, 2014; Costa-Campos & Freire 2015; associated with rocky outcrops, open marshy areas, and Fouquet et al., 2015; Silva e Silva & Costa-Campos, a significant portion of Amazonian savannahs. Amapá 2016; Fouquet et al., 2016). State has more than 90% of its surface unaltered by Amapá regions were classified as high importance human activities and about 70% of its area is protected for fauna inventories in Brazilian Amazonia (Bernard, by federal legislation being a mosaic of 12 conservation 2008). Despite this, there are still large sampling gaps units and five indigenous lands (Bernard, 2008). (Azevedo-Ramos & Galatti, 2002). There are only five Despite this vast richness in vegetation types and good inventories throughout the State (Lima, 2008; Queiroz et al., 2011; Pereira-Júnior et al., 2013; Araújo & Costa- Campos, 2014; Lima et al., 2017). The Amapá National Forest (FLONA Amapá) was the first Sustainable Use 1 Programa de Pós-Graduação em Ecologia e Recursos Naturais, Conservation Unit (established in 1989) of the State, Universidade Federal de São Carlos, São Carlos, São Paulo, and there is still no officially published list of species of Brazil. amphibians from this FLONA. Most of the information 2 Programa de Pós-Graduação em Biodiversidade e Biotecnologia da Rede BIONORTE - UFAM/UNIFAP, available comes from unpublished reports. Thus, this Macapá, Amapá, Brazil. study aims to present the first list of species of anurans * Corresponding author. E-mail: [email protected] of Amapá National Forest, Eastern Amazonia. 628 Ronildo Alves Benício & Jucivaldo Dias Lima

Figure 1. Geographical location of the study area and sampling transects, Amapá National Forest, Amapá State, Brazil.

Materials and Methods rains. As each expedition was considered as a sample in the total inventory it was not possible to produce a Study area.—We conducted the study in Amapá curve of species accumulation. We sampled 10 transects National Forest (FLONA), municipality of Ferreira of 1 km each (Figure 1), visited during the day (8:00 Gomes, Amapá State, Brazil (0°55’29”N, 51°35’45”W, to 12:00 h) and night (18:00 to 22:00 h). The transects Figure 1). With approximately 460,000 hectares, Amapá National Forest has a high degree of preservation. It is were distant by at least 1 km. Two people participated in located between the rivers Araguari, Falsino and Mutum, the collections and the search effort corresponded to 8 in the central region of Amapá, with a predominance of person-hours per day for each transect. Therefore, each terra firme forest. transect had the same sampling effort of 32 person-hours, totalling 320 person-hours for the 10 transects, and each Sampling.—We conducted three expeditions within an transect was visited by day and night at least once in area of rapid assessment surveys at long-term ecological each expedition. We collect at least 10 individuals of research (RAPELD) sites of the Brazilian Program for each species on each expedition. Collected specimens Biodiversity Research (PPBio). The RAPELD is a were killed by overdose of anaesthetic (lidocaine liquid standardized arrangement of trails and permanent plots 10%), fixed in 10% formalin solution and preserved in (Magnusson et al., 2013). We sampled the area during 70% alcohol solution. All the specimens were housed in 56 days in the period of the most intense rains in Amapá the Coleção Herpetológica do Museu Paraense Emílio FLONA, in January 2012 (first expedition), February Goeldi (MPEG) and Instituto de Pesquisas Científicas e 2012 (second expedition), and February to March 2014 Tecnológicas do Estado do Amapá (IEPA). Taxonomic (third expedition). We used the method of visual active nomenclature follows Frost (2017), including recent search (Crump & Scott Jr., 1994). Pitfall traps were not changes proposed by Duellman et al. (2016) and used because of regular flooding of the grid area after Dubois (2017). Unidentified species are candidate taxa Anurans of Amapá National Forest, Eastern Amazonia, Brazil 629 or part of species complexes. The conservation status of 2008); in Reserva Extrativista do Rio Cajari (Queiroz et species was obtained from the international Red List of al., 2011); in a forest fragment in metropolitan Macapá endangered species (IUCN 2017). (Pereira-Júnior et al., 2013); in Reserva Biológica do Parazinho (Araújo & Costa-Campos, 2014), and in the Results savannah of the Rio Curiaú Environmental Protection Area (Lima et al., 2017). We recorded a total of 515 individuals of 53 species The list of species of anurans for FLONA Amapá until of anurans, belonging to the following families: now was based only on unpublished reports. Thus, we Allophrynidae (1 sp.), Aromobatidae (3 spp.), Bufonidae present the first list of species of anurans of Amapá (5 spp.), Centrolenidae (2 spp.), Ceratophryidae (1 sp.), National Forest, Eastern Amazonia. Furthermore, we Craugastoridae (5 spp.), Dendrobatidae (2 spp.), Hylidae present the status of conservation of the amphibian (25 spp.), Leptodactylidae (7 spp.) and Microhylidae (2 species occurring in the area. Total number of species spp.) (Table 1, Figure 2). recorded in this study was higher than that found The most abundant species were Rhinella margaritifera in the Reserva Biológica do Parazinho (13 species; (n = 82), Boana cinerascens (n = 34), Pristimantis Araújo & Costa-Campos, 2014), in a forest fragment chiastonotus (n = 32), Adenomera andreae (n = 30), in metropolitan Macapá (20 species, Pereira-Júnior et Trachycephalus coriaceus (n = 25), Osteocephalus al., 2013), in the Reserva Extrativista do Rio Cajari taurinus (n = 23), Pristimantis marmoratus (n = 22), (40 species, Queiroz et al., 2011), and in the savannah Allophryne ruthveni (n = 21) and Rhinella castaneotica of the Rio Curiaú Environmental Protection Area (28 (n = 20). Thirty-two species presented intermediate species, Lima et al., 2017); but lower than that found abundance (between fifteen and two records); and in other State Conservation Unit, the Parque Nacional eleven species (Anomaloglossus sp1., Pristimantis Montanhas do Tumucumaque (66 species, Lima, 2008). zeuctotylus, Ameerega pulchripecta, Dendropsophus It is important to note that richness assessments, and leucophyllatus, Dendropsophus nanus, Dendropsophus consequently comparisons among sites, are highly sp1., Dendropsophus sp2., Adenomera hylaedactyla, influenced by sampling design, techniques and effort. Leptodactylus fuscus, Chiasmocleis sp1., Otophryne The number of species recorded here for the FLONA pyburni) were rare, with only one record each (Table Amapá is still underestimated, as sampling effort 1). has been concentrated in particular months and was Eight species (Anomaloglossus sp1., Anomaloglossus restricted to the PPBio research grid, covering an area sp2., Pristimantis sp1., Pristimantis sp2., Dendropsophus of 25 km2. sp1., Dendropsophus sp2., Scinax sp1. and Chiasmocleis The amphibian richness for the Amazonian biome sp1.) may represent new species or are part of species is highly underestimated considering taxonomic complexes. None of the species studied are currently problems, recent descriptions of species and taxonomic considered threatened with extinction. However, revisions (e.g., Funk et al., 2012; Vaz-Silva et al., Allophryne ruthveni have declining populations, and 2015). Furthermore, the magnitude of cryptic diversity five species (Vitreorana ritae, Ameerega pulchripecta, remains unknown, especially in relatively poorly Boana dentei, Trachycephalus resinifictrix and explored tropical regions. Part of the reason that cryptic Otophryne pyburni) have currently unknown population diversity remains poorly characterized in the tropics is trends (IUCN 2017). insufficient sampling because these regions are often difficult to access (Funk et al., 2012). Descriptions of Discussion species and new records in Amapá State (e.g., Costa- In Brazilian Amazonia, inventories of amphibians Campos et al., 2014; Silva e Silva & Costa-Campos, were developed mostly in Amazonas State, especially 2014; Costa-Campos & Freire, 2015; Fouquet et al., in Manaus region (e.g., Lima et al., 2012). Furthermore, 2015; Silva e Silva & Costa-Campos 2016; Fouquet many other inventories have been conducted in Roraima et al., 2016) show the lack of knowledge in the region State (e.g., Macculloch et al., 2007), Pará (e.g., Avila- due to insufficient sampling. Thus, inventories are Pires et al., 2010), Rondônia (e.g., Piatti et al., 2012), and important tools for Amazonian conservation, since Acre (e.g., Bernarde et al., 2013). However, in Amapá biological surveys stimulate the discovery of new State, to date, only five inventories were performed: in species, revealing endemic areas and the current levels Parque Nacional Montanhas do Tumucumaque (Lima, of biodiversity (França & Venâncio, 2010). 630 Ronildo Alves Benício & Jucivaldo Dias Lima

Figure 2. Some species of anurans recorded in Amapá National Forest, Eastern Amazonia, Brazil. A - Atelopus hoogmoedi; B - Ceratophrys cornuta; C - Dendrobates tinctorius; D - Boana geographicus; E - Osteocephalus oophagus; F - Phyllomedusa vaillantii; G - Leptodactylus knudseni; H - Otophryne pyburni. Anurans of Amapá National Forest, Eastern Amazonia, Brazil 1 631

1 Table 1. List of anuran species recorded in Amapá National Forest, Eastern Amazonia, Brazil. N = number of records. Table 1. List of anuran species recorded in Amapá National Forest, Eastern Amazonia, Brazil. N = number of records.

Family Species N Allophrynidae Allophryne ruthveni Gaige, 1926 21

Aromobatidae Allobates femoralis (Boulenger, 1884) 3

Anomaloglossus sp1. 1

Anomaloglossus sp2. 2 Bufonidae Amazophrynella sp1. 15 Atelopus hoogmoedi Lescure, 1974 13

Rhaebo guttatus (Schneider, 1799) 3 Rhinella castaneotica (Caldwell, 1991) 20 Rhinella margaritifera (Laurenti, 1768) 82 Centrolenidae Hyalinobatrachium taylori (Goin, 1968) 4 Vitreorana ritae (Lutz, 1952) 2 Ceratophryidae Ceratophrys cornuta (Linnaeus, 1758) 6 Craugastoridae Pristimantis chiastonotus (Lynch & Hoogmoed, 1977) 32 Pristimantis marmoratus (Boulenger, 1900) 22 Pristimantis sp1. 2 Pristimantis sp2. 2 Pristimantis zeuctotylus (Lynch & Hoogmoed, 1977) 1 Dendrobatidae Ameerega pulchripecta (Silverstone, 1976) 1 Dendrobates tinctorius (Cuvier, 1797) 4

Hylidae Boana boans (Linnaeus, 1758) 4 Boana calcarata (Troschel, 1848) 10 Boana cinerascens (Spix, 1824) 34 Boana dentei (Bokermann, 1967) 6 Boana fasciata (Günther, 1858) 6 Boana geographica (Spix, 1824) 11 Dendropsophus brevifrons (Duellman & Crump, 1974) 3 Dendropsophus leucophyllatus (Beireis, 1783) 1 Dendropsophus microcephalus (Cope, 1886) 2 Dendropsophus minutus (Peters, 1872) 12 Dendropsophus minusculus (Rivero, 1971) 15 2 Dendropsophus nanus (Boulenger, 1889) 1

2 Dendropsophus parviceps (Boulenger, 1882) 9 Dendropsophus sp1. 1 Dendropsophus sp2. 1 Osteocephalus leprieurii (Duméril & Bibron, 1841) 14 Osteocephalus oophagus Jungfer & Schiesari, 1995 6 Osteocephalus taurinus Steindachner, 1862 23 Phyllomedusa bicolor (Boddaert, 1772) 2 Phyllomedusa vaillantii Boulenger, 1882 15 Pithecopus hypochondrialis (Daudin, 1800) 9 Trachycephalus coriaceus (Peters, 1867) 25 Trachycephalus typhonius (Linnaeus, 1758) 3 Trachycephalus resinifictrix (Goeldi, 1907) 2 Scinax sp1. 3 Leptodactylidae Adenomera andreae (Müller, 1923) 30 Adenomera hylaedactyla (Cope, 1868) 1 Leptodactylus fuscus (Schneider, 1799) 1 Leptodactylus knudseni Heyer, 1972 3 Leptodactylus mystaceus (Spix, 1824) 7 Leptodactylus rhodomystax Boulenger, 1884 13 Leptodactylus stenodema Jiménez de la Espada, 1875 4 Microhylidae Chiasmocleis sp1. 1 Otophryne pyburni Campbell & Clarke, 1998 1 Total 515

1 Table 1. List of anuran species recordedTrachycephalus in Amapá National coriaceus Forest, (Peters, Eastern 1867) Amazonia, Brazil. N = number25 of records. Table 1. Continued. Trachycephalus typhonius (Linnaeus, 1758) 3 Trachycephalus resinifictrix (Goeldi, 1907) 2 Family SpeciesScinax sp1. N3 AllophrynidaeLeptodactylidae AllophryneAdenomera ruthveniandreae Gaige,(Müller, 1926 1923) 2130

Aromobatidae Adenomera hylaedactyla (Cope, 1868) 1 AllobatesLeptodactylus femoralis fuscus (Boulenger, (Schneider, 1884) 1799) 31

AnomaloglossusLeptodactylus knudseni sp1. Heyer, 1972 13

AnomaloglossusLeptodactylus mystaceus sp2. (Spix, 1824) 27 Bufonidae Leptodactylus rhodomystax Boulenger, 1884 13 AmazophrynellaLeptodactylus stenodema sp1. Jiménez de la Espada, 187515 4 Microhylidae Atelopus hoogmoedi Lescure, 1974 13

RhaeboChiasmocleis guttatus sp1. (Schneider, 1799) 31 RhinellaOtophryne castaneotica pyburni Campbell (Caldwell, & Clarke, 1991) 1998 210 Total Rhinella margaritifera (Laurenti, 1768) 82515 Centrolenidae Hyalinobatrachium taylori (Goin, 1968) 4 Vitreorana ritae (Lutz, 1952) 2 Ceratophryidae This checklist provides the first list of Ceratophrys species withcornuta (Linnaeus,Biological 1758) Conservation 103: 6103–111. information about the Craugastoridae richness and composition Bernard, E. (2008): Inventários Biológicos Rápidos no Parque of species of anurans for the first SustainablePristimantis chiastonotus Use (LynchNacional & Hoogmoed, Montanhas 1977) do Tumucumaque,32 Amapá, Brasil. Pristimantis marmoratus (Boulenger,RAP Bulletin 1900) of Biological 22 Assessment, 48. Arlington, VA, Conservation Unit of Amapá. Our results are preliminary Pristimantis sp1. Conservation International. 2 but contribute to an increase in the knowledge of the Pristimantis sp2. Bernarde, O.S., Albuquerque, S.,2 Miranda, D.B., Turci, L.C.B. anuran fauna of Eastern Amazonia and GuianaPristimantis Shield. zeuctotylus (Lynch(2013): & Hoogmoed, Herpetofauna 1977) da floresta1 do baixo rio Moa em Cruzeiro Dendrobatidae do Sul, Acre - Brasil. Biota Neotropica 13: 220–244. Acknowledgements. We thank Instituto ChicoAmeerega Mendes pulchripecta de Bitar,(Silverstone, Y.O.C., 1976) Tuomisto, H., Pinheiro,1 L.C., Juen, L., Santos- Conservação da Biodiversidade (ICMBio) for logisticDendrobates support tinctorius (Cuvier,Costa, 1797) M.C. (2017): Species turnover4 in Amazonian frogs: low and for the collection license (Nº 32994-3); Sistema Nacional de Hylidae predictability and large differences among Forests. Biotropica Pesquisa em Biodiversidade: Sisbiota Herpeto-Helmintos (MCT/ Boana boans (Linnaeus, 1758)49: 696–705. 4 CNPq/MEC/CAPES/FNDCT/FAPESPA, Proc. 563355/2010- Boana calcarata (Troschel,Bokermann, 1848) W.C.A. (1967): Nova10 espécie de Hyla do Amapá 7 e ICAAF 011/2012) for financial support; Marinus Steven Boana cinerascens (Spix, 1824)(Amphibia, Hylidae). Revista34 Brasileira de Biologia 27: 109– Hoogmoed for identifying the material. RAB thanks Conselho Boana dentei (Bokermann, 112.1967) 6 Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Boana fasciata (Günther,Caldwell, 1858) J.P., Hoogmoed, M.S. (1998):6 Allophrynidae, Allophryne, Proc. 131905/2013-9; 142120/2015-4) and Fundação de Amparo Boana geographica (Spix, 1824)A. ruthveni . Catalogue of American11 Amphibians and Reptiles à Pesquisa do Estado de São Paulo (FAPESP, Proc. 2015/11821- 666: 1–3. 0) for financial support. JDL thanks InstitutoDendropsophus de Pesquisas brevifrons (Duellman & Crump, 1974) 3 Costa-Campos, C.E., Gama, S.L., Galeno, E.O., Silva, D.W.S., Científicas e Tecnológicas do Estado do AmapáDendropsophus for financial leucophyllatus (Beireis, 1783) 1 Corrêa, K.J.G., Almeida, D.P., Santiago, A.G. (2014): New support. We thank Associate Editor Igor KaeferDendropsophus for valuable microcephalus (Cope, 1886) 2 record and distribution map of Hypsiboas lanciformis (Cope, comments and suggestions. Dendropsophus minutus (Peters, 1872) 12 Dendropsophus minusculus1871) (Rivero, (Amphibia, 1971) Anura, Hylidae)15 in Eastern Amazonia, Brazil. Dendropsophus nanus (Boulenger,Check List1889) 10 : 960–961. 1 References Costa-Campos, C.E., Freire, E.M.X. (2015): Distribution extension Araújo, A.S., Costa-Campos, C.E. (2014): Anurans of the Reserva and geographic distribution map of Elachistocleis helianneae Biológica do Parazinho, Municipality of Macapá, state of (Anura: Microhylidae):new record for state of Amapá, Eastern Amapá, eastern Amazon. Check List 10: 1414–1419. Amazon. Check List 11: 1747. Avila-Pires, T.C.S., Hoogmoed, M.S., Vitt, L.J. (2007): Crump, M.A., Scott Jr., N.J. (1994): Visual Encounter Surveys. Herpetofauna da Amazônia. In: Herpetologia no Brasil II, p. In: Measuring and Monitoring Biological Diversity: Standard 13–43. Nascimento, L.B., Oliveira, M.E., Eds., Belém, BRA, Methods for Amphibians, p. 84–92. Heyer, W.R., Donnelly, Sociedade Brasileira de Herpetologia. M.A., Mcdiarmid, R.W., Hayek, L.C., Foster, M.S., Eds., Avila-Pires, T.C.S., Hoogmoed, M.S., Rocha, W.A. (2010): Notes Washington, USA, Smithsonian Institution Press. on the Vertebrates of northern Pará, Brazil: a forgotten part of the Dubois, A. (2017): The nomenclatural status of Hysaplesia, Guiana Region, I. Herpetofauna. Boletim do Museu Paraense Hylaplesia, Dendrobates and related nomina (Amphibia, Emílio Goeldi 5: 13–112. Anura), with general comments on zoological nomenclature and Azevedo-Ramos, C., Galatti, U. (2002): Patterns of amphibian its governance, as well as on taxonomic databases and websites. diversity in Brazilian Amazonia: conservation implications. Bionomina 11: 1–48. Anurans of Amapá National Forest, Eastern Amazonia, Brazil 633

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