Herpetology Notes, volume 12: 799-807 (2019) (published online on 28 July 2019)

Anurans and of the Reserva Extrativista Beija-Flor Brilho de Fogo, Amapá state, eastern Amazon

Fillipe Pedroso-Santos1, Patrick Ribeiro Sanches1, and Carlos Eduardo Costa-Campos1,*

Abstract. We present a checklist for anurans and reptiles of the Reserva Extrativista Municipal Beija-Flor Brilho de Fogo, located in the southeastern part of the municipality of Pedra Branca do Amapari, Amapá State, and compare its richness of herpetofauna with that of other eight localities of the state of Amapá. Using active visual and auditory search, we recorded 50 species: 25 anurans, 14 , 10 and one crocodilian. Our results will provide subsidies for the conservation and management plan of this conservation unit, as well as increase knowledge of the fauna of anurans and reptiles in the Eastern Amazon, especially in the Guiana Shield.

Keywords. Herpetofauna, Amazon, Richness, Protected areas

Introduction in these areas for better knowledge and preservation of biodiversity, since these are unaltered environments The herpetofauna of the Neotropical region, especially with real possibilities of access (Bruner et al., 2001). the Amazon, is considered one of the most diversified In addition, Amapá state plays an important role in in the world (Ávila-Pires et al., 2007; Fouquet et al., ’s conservation network, becoming a region of high 2007; Ávila-Pires et al., 2010). Brazilian Amazonia importance for fauna sampling in Brazilian Amazonia, is home to 308 species of anurans (Hoogmoed and with more than 95% of its original vegetation being well- Galatti, 2017) and about 795 species of reptiles (Costa preserved and close to 70% of its extent lying within and Bérnils, 2018). In Amapá state, situated in the far protected areas (Drummond et al. 2008, Bernard, 2008; northeast of the Amazon region, is composed of areas Hilário et al. 2017). Despite this, only eight sampling such as flooded forests, complex lakes, portions of were carried throughout the Amapá State (see Lima, mangrove, terra firme (upland) forests and a portion of 2008; Queiroz et al., 2011; Pereira-Júnior et al., 2013; Amazonian savannahs, as well as vegetation associated Araújo and Costa-Campos, 2014; Campos et al., 2015; with rocky outcrops and open marshy areas (Benício Benício and Lima, 2017; Lima et al., 2017; Silva e Silva and Lima, 2017). In addition, this area is part of the and Costa-Campos, 2018), and there are large sampling Guiana Shield and has been considered as an endemic gaps and unknown areas that possibly have never been zone to herpetofauna (Silva et al., 2005). For example, sampled (Azevedo-Ramos and Galatti, 2002). a complex study consisting of five samplings was Despite the knowledge fragmented of anurans and conducted in the conservation unit called Tumucumaque reptiles of the Amapá state, basic information on the Mountains National Park (Amapá State), in which 156 composition and richness of species still remains scarce, of amphibians and reptiles species were recorded, with gaps and limitation of conservation strategies. This classifying it as one of the regions with the highest is due to the difficult to access in several Amazonian species richness of the herpetofauna in the Guiana Shield areas (Funk et al., 2012), as well as the fact that most (Lima, 2008). Thus, studies of this context are important studies in the region deal only with descriptions of species and new records of species occurrences, which does not contribute to the detailed knowledge of the local herpetofauna (e.g., Bokermann, 1967; Silverstone, 1975, 1976; Hoogmoed, 1979a, b; Hoogmoed and 1 Universidade Federal do Amapá, Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia. Macapá, Gruber, 1983; Caldwell and Hoogmoed, 1998; Señaris AP, Brazil, CEP: 68.903-419. and Ávila-Pires, 2003; Señaris and MacCuolloch, 2005; * Corresponding author. E-mail: [email protected] Ávila-Pires et al., 2007; Costa-Campos et al., 2014; 800 Fillipe Pedroso-Santos et al.

Silva e Silva and Costa-Campos, 2014; Costa-Campos fragment of Universidade Federal do Amapá; Cancão and Freire 2015; Fouquet et al., 2015; Silva e Silva and Municipal Natural Park; River Curiaú Environmental Costa-Campos, 2016; Fouquet et al., 2016, Ribeiro- Protection Area; Amapá National Forest; River Cajari Júnior et al., 2016). In this context, in this study we Extractive Reserve; Tumucumaque Mountains National present the first list of species of anurans and reptiles Park; Fazendinha Environmental Protection Area. We of Reserva Extrativista Beija-Flor Brilho de Fogo, a conducted the richness comparisons using the Jaccard Conservation Unit of sustainable use, located in the similarity index and pair-group method with averaging southeastern part of the municipality of Pedra Branca (UPGMA) (Magurram, 2004). The cophenetic do Amapari, Amapá state. correlation coefficient was calculated to indicate the degree of representability of the similarity matrix in the Materials and Methods dendrogram, allowing for the identification of groups formed by the evaluated localities, considering the Study area.—Fieldwork was conducted in Reserva similarities they presented in relation to species richness. Extrativista Beija-Flor Brilho de Fogo, municipality The cluster analysis was performed on the software Past of Pedra Branca do Amapari, Amapá state, Brazil 3.06 (Hammer et al., 2001). (0º47’30.6’’N, 51º58’42.1’’W). It is located in the southeastern part of the municipality, with approximately Results 68,550 hectares, and predominance of dense forest with large trees and sandy and clayey ground with We recorded a total of 168 individuals of 25 species of low fertility and high degree of acidity, being the anurans and 61 individuals of 25 species of reptiles (14 Araguari River its main watercourse (Drummond et lizards, 10 snakes and one crocodilian). Among anuran al., 2008). The climate of the region is Equatorial (Am) amphibians, not surprisingly the most representative according Köppen-Geiger classification and the average family was Hylidae (7 species), followed by Bufonidae temperature is 27.6°C, varying seasonally between 25.8 (5 species), Leptodactylidae and Craugastoridae (3 to 29.0oC, with annual rainfall approximately 2,850 mm species each) (Figure 1, Table 1). In reptiles the most (Alvares et al., 2013). representative family for lizards was (6 species), followed by Dactyloidae and Teidae (two Sampling.—We conducted the study from 17 species each). To snakes, the family Dipsadidae was the September 2015 to 18 October 2015. The herpetofauna most representative, with 6 species (Figure 2, Table 1). was sampled using active visual and auditory search The most abundant species of anurans were (Crump and Scott Jr., 1994; Heyer et al., 1994) in Osteocephalus cabrerai (n = 32), Allobates femoralis (n areas close to aquatic environments (swamps, streams = 27) and Rhinella cf. margaritifera (n = 14). In addition, and temporary ponds). These included searching for we recorded Atelopus hoogmoedi, Hyalinobatrachium anurans and reptiles in all possible microenvironments, iaspidiense and Ameerega pulchripecta (see Table 1); by disturbing the leaf litter, raising fallen logs, looking this species are classified as vulnerable and data deficient, inside tree barks and under stones, inspecting epiphytes, respectively, by the IUCN (2017). A. pulchripecta is holes in the ground and hollow trees. Five men were endemic to the Amapá State, with distribution restricted involved and they searched during the day (between to the Serra do Navio, northeastern of the Brazilian 7:00 a. m. and 11:00 a. m.) and night (between 7:00 p. m. Amazon (Silva e Silva and Costa-Campos, 2018), and 11:00 p. m.), totalling four hours in each sampling and the frog Hyalinobatrachium iaspidiense has been transect. The total sampling effort was 256 hours/man. currently recorded for the State (Silva e Silva and Costa- All the specimens were killed with 5% lidocaine, Campos, 2016). For reptiles, the most abundant species fixed in 10% formalin and preserved in 70% ethanol, was Uranoscodon superciliosus (n = 15). and were deposited in the Herpetological Collection Two species (Rhinella cf. margaritifera and Pristimantis of the Universidade Federal do Amapá. Taxonomic sp.) may represent new species or are part of species nomenclature follows Ávila-Pires (1995), Duellman et complexes. Furthermore, four species of anurans were al. (2016), Dubois (2017) and Frost (2018). recorded in reproductive activity, in which we observed Data analysis.—The richness of herpetofauna species spawning of Hyalinobatrachium iaspidiense and Boana at Reserva Extrativista Beija-Flor Brilho de Fogo boans, and couples in amplexus of Phyllomedusa was compared to other eight localities of the state of vaillantii and Osteocephalus cabrerai. Amapá: 1 – Biological Reserve of Parazinho; Forest Anurans and reptiles of the Reserva Extrativista Beija-Flor Brilho de Fogo 801

Figure 1. Some species of frogs recorded at Reserva Extrativista Beija-Flor Brilho de Fogo, during 17 September 2015 to 18 October 2015. 1) Allobates femoralis; 2) Atelopus hoogmoedi; 3) Rhaebo guttatus; 4) Hyalinobatrachium iaspidiense; 5) Pristimantis chiastonotus; 6) Pristimantis zeuctotylus; 7) Ameerega pulchripecta; 8) Dendrobates tinctorius; 9) Adelophryne gutturosa; 10) Boana geographica; 11) Osteocephalus cabrerai; 12) Leptodactylus petersii. 802 Fillipe Pedroso-Santos et al.

Figure 2. Some species of reptiles recorded at Reserva Extrativista Beija-Flor Brilho de Fogo, during 17 September 2015 to 18 October 2015. 1) Caiman crocodilus crocodilus; 2) Gonatodes humeralis; 3) Copeoglossum nigropunctatum; 4) Norops fuscoauratus; 5) Uranoscodon superciliosus; 6) bicarinatus; 7) kockii; 8) Loxopholis guianense; 9) Kentropyx calcarata; 10) Corallus hortulanus; 11) flammigerus; 12) Dipsas catesbyi.

Considering the similarity between the studied Natural Park; second group, formed by Biological localities in relation to herpetofauna species composition, Reserve of Parazinho, River Curiaú Environmental the cluster analysis (cophenetic correlation coefficient Protection Area, Fazendinha Environmental Protection = 0.7801), resulted in two well-defined groups (Figure Area and Forest fragment of Universidade Federal do 3, Table 2): first group, formed by Tumucumaque Amapá Mountains National Park, River Cajari Extractive Reserve, Amapá National Forest, Reserva Extrativista Beija-Flor Brilho de Fogo and Cancão Municipal Anurans and reptiles of the Reserva Extrativista Beija-Flor Brilho de Fogo 803

Table 1. Checklist of anuran and species recorded at Reserva Extrativista Beija-Flor Brilho de Fogo, municipality of Pedra Branca doTable Amapari, 1. Checklist Amapá State, of anuran Brazil. and reptile species recorded at Reserva Extrativista Beija-Flor Brilho de Fogo, municipality of Pedra Branca do Amapari, Amapá State, Brazil.

Family/species Number of individuals AMPHIBIA Aromobatidae (Allobatinae) Allobates femoralis (Boulenger, 1884) 27 Bufonidae Atelopus hoogmoedi Lescure, 1974 8 Rhaebo guttatus (Schneider, 1799) 5 Rhinella cf. margaritifera (Laurenti, 1768) 14 Rhinella marina (Linnaeus, 1758) 3 Rhinella martyi Fouquet, Gaucher, Blanc & Vélez-Rodriguez, 2007 2 Centrolenidae (Hyalinobatrachinae) Hyalinobatrachium iaspidiense (Ayarzaqüena, 1992) 4 Craugastoridae (Ceuthomantinae) Pristimantis chiastonotus (Lynch & Hoogmoed, 1977) 6 Pristimantis zeuctotylus (Lynch & Hoogmoed, 1977) 2 Pristimantis sp. 4 Dendrobatidae (Colostethinae) Ameerega pulchripecta (Silverstone, 1976) 8 Dendrobatidae (Dendrobatinae) Dendrobates tinctorius (Cuvier, 1797) 3 Eleutherodactylidae (Phyzelaphryninae) Adelophryne gutturosa Hoogmoed & Lescure, 1984 4 Hylidae Boana boans (Linnaeus, 1758) 7 Boana calcarata (Troschel in Schomburgk, 1848) 2 Boana fasciata (Günther, 1859 “1858’’) 1 Boana geographica (Spix, 1824) 12 Osteocephalus cabrerai (Cochran & Goin, 1970) 32 Osteocephalus oophagus Jungfer & Schiesari, 1955 5 Trachycephalus resinifictrix (Goeldi, 1907) 2 Leptodactylidae (Leptodactylinae) Adenomera andreae (Müller, 1923) 9 Adenomera hylaedactyla (Cope, 1868) 2 Leptodactylus petersii (Steindachner, 1864) 4 Phyllomedusidae Phyllomedusa bicolor (Boddaert, 1772) 1 Phyllomedusa vaillantii Boulenger, 1882 1 REPTILIA Alligatoridae Caiman crocodilus crocodilus (Linnaeus, 1758) 1

804 Fillipe Pedroso-Santos et al.

Table 1. Continued.

Family/species Number of individuals Sphaerodactylidae Gonatodes humeralis (Guichenot, 1855) 2 Mabuyidae Copeoglossum nigropunctatum (Spix, 1825) 1 Dactyloidae Dactyloa punctata (Daudin, 1802) 1 Norops fuscoauratus D'Orbigny, 1837 4 Iguanidae Iguana iguana iguana (Linnaeus, 1758) 2 Tropiduridae Uranoscodon superciliosus (Linnaeus, 1758) 15 Gymnophthalmidae agilis (Ruthven, 1916) 1 Cercosaura aff. argulus Peters, 1863 1 Neusticurus bicarinatus (Linnaeus, 1758) 3 Arthrosaura reticulata (O'Shaughnessy, 1881) 1 Arthrosaura kockii (Lidth de Jeude, 1904) 1 Loxopholis guianense (Ruibal, 1952) 3 Teiidae Ameiva ameiva ameiva (Linnaeus, 1758) 2 Kentropyx calcarata Spix, 1825 4 Boidae Corallus hortulanus (Linnaeus, 1758) 1 Chironius fuscus (Linnaeus, 1758) 1 Phrynonax poecilonotus polylepis (Peters, 1867) 1 Dipsadidae Atractus flammigerus (Boie, 1827) 1 Dipsas catesbyi (Sentzen, 1796) 2 Helicops leopardinus (Schlegel, 1837) 5 Siphlophis compressus (Daudin, 1803) 1 occipitalis (Wied-Neuwied, 1824) 2 Oxyrhopus petolarius digitalis Reuss, 1834 1 Viperidae Bothrops atrox (Linnaeus, 1758) 4

Discussion Júnior et al., 2013); but lower than that found in others The composition of anurans recorded here was higher study conducted in Conservation Units (see Silva e than that found in some studies carried out in the state of Silva and Costa-Campos, 2018; Lima et al., 2017; Amapá (see Araújo and Costa-Campos, 2014; Pereira- Benício and Lima, 2017; Queiroz et al., 2011; Lima, Anurans and reptiles of the Reserva Extrativista Beija-Flor Brilho de Fogo 805

Area and Lima et al. (2008) has recorded 34 species in an area of dense and open forest in the Tumucumaque Mountains National Park. However, it should be emphasized that the sampling effort applied to obtain knowledge on the Reserva Extrativista Beija-Flor Brilho de Fogo herpetofauna (two months) was much less than in the other locations compared herein, caution must be taken when interpreting the results. The number of species recorded here for the Reserva Extrativista Beija-Flor Brilho de Fogo is still preliminary, as sampling effort was concentrated in only one method (active visual and auditory search). Most of these species may have secretive habits, in which their camouflage strategies make them less detectable by active visual search. The combination of complementary methods in Figure 3. Dendrogram of a cluster analysis based on herpetofauna species richness of the Reserva Extrativista sampling will help improve sample representation and, Beija-Flor Brilho de Fogo, municipality of Pedra Branca do thus, the understanding of species distributions (Ribeiro- Amapari, Amapá State, Brazil, and eight localities of the state Júnior et al 2008; Pantoja and Fraga, 2012). of Amapá: Biological Reserve of Parazinho (RBP); Forest Considering the analysis similarity for the herpetofauna fragment of Universidade Federal do Amapá (FFCU); Cancão species composition, the Reserva Extrativista Beija-Flor Municipal Natural Park (PNMC); River Curiaú Environmental Brilho de Fogo is inserted in cluster “1”. The species Protection Area (APARC); Amapá National Forest (FNA); of these four areas was similar to those of other areas River Cajari Extractive Reserve (RERC); Tumucumaque in Cancão Municipal Natural Park (Silva e Silva and Mountains National Park (PNMT); Fazendinha Environmental Campos, 2018), characterized by primary forest with Protection Area (APAF), using Jaccard index and and group- a wide variety of environments and geographically average method “UPGMA” (cophenetic correlation coefficient = 0.7801). close. Most of the species we recorded in cluster “1” have a large geographic distribution in Amazon basin (Santorelli et al., 2018), whereas other species have distributions typically associated with the ecotonal zone 2008) (Table 2). To reptiles, we recorded 24 species of of the Cerrado-Amazon Forest (Lima et al., 2017). reptiles and one crocodilian, while Campos Additionally, these localities are situated in regions et al. (2015) recorded only 23 species in an ecosystem that show strong influence of Amazon forest, with of floodplain at Fazendinha Environmental Protection few species commonly observed in open areas. The

Table 2. Herpetofauna species richness (amphibian and reptile) of the Reserva Extrativista Beija-Flor Brilho de Fogo, municipality Tableof Pedra 2. Herpetofauna Branca do speciesAmapari, richness Amapá (amphibian State, Brazil, and reptile) and eight of the localities Reserva ofExtrativista the state ofBeija-Flor Amapá �.Brilho de Fogo, municipality of Pedra Branca do Amapari, Amapá State, Brazil, and eight localities of the state of Amapá

Localities Amphibian Reptile Source richness richness Reserva Extrativista Beija-Flor Brilho de Fogo 25 25 This study Biological Reserve of Parazinho 13 - Araújo and Costa-Campos (2014) Forest fragment of Universidade Federal do Amapá 20 - Pereira-Júnior et al. (2013) Cancão Municipal Natural Park 49 - Silva e Silva and Costa-Campos (2018) River Curiaú Environmental Protection Area 28 - Lima et al. (2017) Amapá National Forest 53 - Benício and Lima (2017) River Cajari Extractive Reserve 40 - Queiroz et al. (2011) Tumucumaque Mountains National Park 66 34 Lima (2008); Lima et al. (2008) Fazendinha Environmental Protection Area - 23 Campos et al. (2015)

806 Fillipe Pedroso-Santos et al. other localities, with a low degree of relation between Biological Conservation 103: 103–111. the analysed herpetofauna species composition, are Benício, R. A., Lima, J. D. (2017): Anurans of Amapá National also those with the lowest known species richness. It Forest, Eastern Amazonia, Brazil. Herpetology Notes 10: 627– 633. is possible that the low number of species recorded Bernard, E. (2008): Inventários Biológicos Rápidos no Parque in these localities has been influenced by the distant Nacional Montanhas do Tumucumaque, Amapá, Brasil. geographically and association of these localities with RAP Bulletin of Biological Assessment, 48. Arlington, VA, the urban matrix. Conservation International. Although our results were preliminary in a rapid Bokermann, W.C.A. (1967): Nova espécie de Hyla do Amapá assessment, the anurans registered represents 38% of the (Amphibia, Hylidae). Revista Brasileira de Biologia 27: 109– species recorded for the Amapá state, while the reptiles 112. Bruner, A. G., Gullison, R. E., Rice, R. E., Fonseca, G. A. B. (2001): represents 19.3% of reptiles Squamata and Crocodylia, Effectiveness of Parks in Protecting Tropical Biodiversity. according to Hollowell and Reynolds (2005). Science 291: 125–128. Concluding, this checklist provides the first preliminary Caldwell, J.P., Hoogmoed, M.S. (1998): Allophrynidae, Allophryne, list of species with information on the anurans and A. ruthveni. Catalogue of American Amphibians and Reptiles reptiles composition at Reserva Extrativista Beija-Flor 666: 1–3. Brilho de Fogo. Our results show that the richness of Campos, C.E.C., Lima, J. D., Lima, J. R. F. (2015): Riqueza e composição de répteis Squamata (lagartos e anfisbenas) da Área species of anurans and reptiles recorded in this study, de Proteção Ambiental da Fazendinha, Amapá, Brasil. Biota compared to other herpetofaunal samples conducted in Amazônia 5(2): 84–90. the Amapá State, contributes to the knowledge on species Costa, H.C., Bérnils, R.S. (2018): Répteis do Brasil e suas Unidades fauna in the region, because in our sampling there are Federativas: Lista de espécies. Herpetologia Brasileira 8(1): populations of species considered Vulnerable or Data 11–57. Deficient, which have little know areas of occurrence, Costa-Campos, C.E., Freire, E.M.X. (2015): Distribution extension status and ecological requirements (IUCN, 2017). and geographic distribution map of Elachistocleis helianneae (Anura: Microhylidae): new record for state of Amapá, Eastern In addition, this study reinforces the importance of Amazon. Check List 11: 1747. conservation and planning actions in this Conservation Costa-Campos, C.E., Gama, S.L., Galeno, E.O., Silva, D.W.S., Unit. Corrêa, K.J.G., Almeida, D.P., Santiago, A.G. 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