Anurans of the Reserva Biológica Do Parazinho, Municipality of Macapá

of Anurans of the Reserva Biológica do Parazinho, ists L Municipality of Macapá, state of Amapá, eastern Amazon Ananda Silva Araújo and Carlos Eduardo Costa-Campos *

Universidade Federal do Amapá,[email protected] Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia. Rod. Juscelino Kubitschek, km 02, Jardim Marco Zero. CEP 68.903-419. Macapá, Amapá, Brasil. * Corresponding author. Email: Abstract:

We report a list of anurans from the Reserva Biológica do Parazinho (00°52′30″ N, 49°59′15″ W), a strictly protected area, part of the Bailique archipelago, in the municipality of Macapá, state of Amapá, Brazil. The study was carried out in September–October 2010 (dry season) and May–June 2011 (rainy season). We recorded 13 species of anurans, distributed among four families: Bufonidae (1), Hylidae (8), Leptodactylidae (3) and Pipidae (1). The accumulation curves did not stabilize, suggesting that the community was not completely sampled. This study provides the first information on anurans in insular areas of the state of Amapá, and highlights the importance of these areas for the conservation of anurans.

DOI: 10.15560/10.6.1414

Introduction

et al. a constant influence of the Amazon River and the Atlantic Brazil has the highest richness of amphibians in the Ocean, the area exhibits marine characteristicset al. 2008). with the world, represented by 1,026 species (Segalla 2014). formation of sandbanks, subjected to periodic flooding and etA substantialal. portion of the species occurs in the Amazon constant sediment deposition (Drummond region, with 232 recorded amphibian species (Ávila-Pires In this study, 4- to 7-day field trips were carried out 2007). However, these numbers are likely to be between September and October 2010 (dry season) underestimated,et al. as many regions of the Brazilian Amazon and May and June 2011 (rainy season), totaling 28 days. remain poorly studied or have as yet not been sampled Observations began at sunsetcf. and ended when anuran (Bernarde 2011, 2013). According to Azevedo-Ramos etactivity al. decreased. Anurans were sampled using visual and and Galatti (2001), only 29 localities have been surveyed acoustic survey methods ( Crump and Scott 1994; Heyer in the Brazilian Amazon. 1994). Visual and acoustic searches consisted of Studies on theet composition al. of amphibians in the Brazilianet slowly walking trails (four trails of 200 m). On each side of al.Amazon have been carriedet al. out mostly in theet al. states of the trail, an area of five meters was sampled up to a height Amazonas (Lima 2006; Ilha and Dixo 2010;et al. Prudente of 3–4 m. We searched the leaf litter, decomposing trees, 2013), Pará (Ávila-Pireset al. 2010; Bernardo 2012), tree holes, vegetation, burrows, and other sites suitable for Rondônia (Bernarde and Macedo 2008; Piatti 2012) and sheltering anurans. Six hours of searching were conducted Acre (Bernarde 2011, 2013). Located in the northern on each trail per month, totaling 64 h of observations. Amazon Basin, the state of Amapáet al.has 2008). approximately 75% To analyze anuran species richness, rarefaction curves of its territory protected by 19 Conservation Units and five were generated, based on the number of individuals and Indigenous reserves (Drummond number of samples, using the program EstimateS 9.1, with Herein, we report for the first time a list of anuran 1,000 randomizations (Gotelli and Colwell 2011). Species species from Reserva Biológica do Parazinho, a fluvial richness among physiognomies was also compared with island located in the Amazon River basin. These records the richness estimators Chao 1, Chao 2, Jacknife 1, Jacknife aim to fill the knowledge gap in the occurrence and 2, and Bootstrap using the program EstimateS 9.1 (Colwell Materialsdistribution andof amphibians Methods in eastern Amazonia. 2013). Climate rainfall variables were also obtained from the Nucleus of Hydrometeorology and Renewable Energy of The study was carried out in the Reserva Biológica do the Institute of Scientific and Technological Research of Parazinho, a strictly. protected area (biological reserve, as thee.g., state of Amapá (NHMET/IEPA/AMAPÁ).et al. defined by Brazilian environmental laws; see Rylands and Specimens were identified based on specialized literature Brandon 2005) Parazinho is a fluvial island and part of ( Lescure and Marty 2001; Lima 2006; AmphibiaWeb the Islands of Bailique in the municipalityRhyzophora of Macapá, mangue and 2011; Ouboter and Jairam 2012). Voucher specimens were theAvicennia Amazon Rivernitida Basin, , BrazilClitoria (Figures arborea 1 and 2). collected, anesthetized with 5% lidocaine, fixed with 10% The vegetation cover consists of formalin and preserved in 70% ethanol. Voucher specimensCollection L., Jacq. and Benth., which were deposited at the Herpetological collection of the Federal form a low forest with an understory. A flat area with clayey, University of Amapá, Macapá, state of Amapá, Brazil. salt marsh, and sandy sediments of mixed origin, fluvial permits were provided by the Amapá State Institute of the and marine, characterizes the relief. Since the humidity is Environment. Voucher numbers are listed in Appendix 1. 1414 Araújo and Costa-Campos | Insular anurans of Amazon basin, state of Amapá

Figure 1. et al.

Study area showing the Reserva Biológica do Parazinho, state of Amapá, eastern Amazonia, Brazil, after Drummond (2008).

Figure 2.

Breeding habitats used by anurans on the Reserva Biológica do Parazinho, state of Amapá, Brazil: (A) permanent pond in low forest; (B) temporary pond in sandbanks; (C) temporary pond in flat area; (D) flat area during low tide.

1415 Araújo and Costa-Campos | Insular anurans of Amazon basin, state of Amapá

Figure 3. Rhinella marina Hypsiboas boans Hypsiboas raniceps Osteocephalus oophagus AnuransOsteocephalus species taurinus found in thePseudis Reserva laevis BiológicaPseudis do Parazinho, paradoxa stateScinax of Amapá, ruber Brazil.Trachycephalus (A) typhonius; (B) Leptodactylus ;petersii (C) Leptodactylus; (D) podicipinus Leptodactylus; (E) latrans Pipa pipa; (F). ; (G) ; (H) ; (I) ; (J) ; (K) ; (L) gr. ; (M)

1416 Araújo and Costa-Campos | Insular anurans of Amazon basin, state of Amapá

Results

2010), the richness of 13 species of anurans recorded We recorded 189 individuals distributed among four in this study is underestimated, as the collector curve families and 13 species. The most representative family was did not reach the asymptote and the highest values Hylidae with eight species, followed by Leptodactylidae recorded for the other Amazonian localities range with three species, and Bufonidae and Pipidae with one between 23 and 54 species. In addition, further studies species each (Table 1; Figure 3). on Amazonian et al. communities and anurans with larger The accumulation curves did notOsteocephalus stabilize, suggesting taurinus sample size and effort and longer duration are needed thatn the community was not completely sampledPipa pipa (Figure n (Bernarde 2011). 4). The most abundant species was In the present study, Hylidae and Leptodactylidae ( =30). The least abundant species was ( =4) were the families with the greatest number (of species, (Figure 5). Abundance was higher in the rainy season (May similar to that reported in otheret al. studies and following the to June) than in the dry season (September and October) pattern found in Neotropical environments Duellman Discussion(Figure 6). and Trueb 1994; Ávila-Pires 2010). For example, in

Species accumulation curves have been widely used to make inferenceset al. and evaluate the sampling effort in studies of anuran communities (Armstrong and Contee.g., 2010; Zina 2012). The richness indices observed for the study sites were higher in continental areas ( Amazon region). This result is very common in studies comparing islands and continentset al. and agrees with the theory of island biogeography proposed by MacArthur and Wilson (2001) and Silva (2008). These differences in species richness may result from the way the islands were formedet al and the habitats that are available for the Figure 4. establishment and/or maintenance of a given population (Santos . 2004). Accumulated curve of anurans in the Reserva Biológica do Parazinho, state of Amapá, Brazil. Despite differences in sampling efforts, environmentale.g. conditions and size of sampled areas when comparing this study with others sensu in the Amazon et al. region ( , 54 spp. in the Urucu Petrol Base, municipality of Coari, state sensuof Amazonas et al.Prudente 2013; 50 spp. in the forest of Lower Moa River, Cruzeiro sensu do Sul, state of Acre Bernarde 2013; 23 spp. in municipality of Rio Preto da Eva, east of Manaus Ilha and Dixo Table 1.

List of anurans species registered in the Reserva Biológica do Parazinho,FAMILY/SPECIES state of Amapá, Brazil. N Bufonidae Figure 5. Rhinella marina Osteocephalus taurinus Hypsiboas boans RelativeOsteocephalus abundance oophagus of anurans inTrachycephalus the Reserva Biológicathyphonius do Hylidae (Linnaeus, 1758) 15 Parazinho,Scinax ruber state of Amapá:Rhinella Ot ( marina Pseudis), Hbparadoxa ( Hypsiboas), Oo raniceps ( Leptodactylus), Tt podicipinus ( Leptodactylus), Hypsiboas boans Sr (latrans ),Pipa Rm pipa ( Pseudis), laevis Ppar ( Leptodactylus), Hr Hypsiboas raniceps(Linnaeus, 1758) 29 (petersii). ), Lpod ( ), Ll ( gr. ), Pp ( ), Pl ( ) e Lpet ( Osteocephalus taurinus(Günther, 1859 “1858”) 12

Osteocephalus oophagus Steindachner, 1862 3028

Pseudis laevis Jungfer & Schiesari, 1995

Pseudis paradoxaParker, 1935 1

Scinax ruber (Linnaeus, 1758) 13

Trachycephalus(Laurenti, typhonius 1768) 17

Leptodactylidae (Linnaeus, 1758) 27

Leptodactylus petersii

Leptodactylus podicipinus(Steindachner, 1864) 1

Leptodactylus latrans (Cope, 1862) 6

Pipidae gr. (Steffen, 1815) 6 Figure 6.

Pipa pipa Relative abundance of anurans species registered in in the Reserva Biológica do Parazinho, state of Amapá, Brazil and rainfall (Linnaeus, 1758) 4 accumulation (mm). 1417 Araújo and Costa-Campos | Insular anurans of Amazon basin, state of Amapá

10.1590/S1676- 06032011000300010 the Reserva Biológica do Parazinho, the larger number Bernarde, P.S.,Biota S. Albuquerque,Neotropica D.B. Miranda and L.C.B. Turci. 2013. of hylid species was partly due to the presence of Herpetofauna da floresta). do baixo rio Moa em Cruzeiro do Sul, Acre temporary ponds that provided suitable conditions for –Brasil. 13(1): 220–244 (doi: 10.1590/S1676- breeding. All species registered are widely distributed 06032013000100023 Rhinella marina Scinax ruber Bernardo, P.H., R.A. Guerra-Fuentes,Check List W. Matiazzi and H. Zaher. 2012. in the Amazon Basin and surrounding areas, such as Checklist of Amphibians and Reptiles). of Reserva Biológica do and (IUCN 2013). Tapirapé, Pará, EstimateS: Brazil. Statistical 8(5):Estimation 839–846 of Species (http://www. Richness andchecklist.org.br/getpdf?SL037-12 Shared Species from Samples. Version 9.1 Abundance was higher in the rainy season than in the Colwell, R.K. 2013. dry season, which is associated to the permeable skin of . Accessible at http:// anurans and their stronget al. dependence on humidity, mild air purl.oclc.org/estimates. Captured on 10 July 2013. temperatures, and rainfall for reproduction (Duellman and Crump, M.A. and MeasuringN.J. Scott Jr. and 1994. Monitoring Visual Encounter Biological Surveys; Diversity: pp. Standard 84–92, Methodsin: W.R. Heyer,for Amphibians M.A. Donnelly, R.W. Mcdiarmid, L.C. Hayek and M.S. Trueb 1994; Santos 2007). For anurans, differences Foster (eds). Atlas das Unidades de observed in species composition and abundance in conservação do Estado do. Washington: Amapá Smithsonian Institution Press. different environments can be strongly correlated with Drummond, J.A., T.C.A. Dias and D.M.C. Brito. 2008. . 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Biota Neotropica ). Lima, J.D. 2008. A Inventários Herpetofauna Biológicos do Parque Rápidos Nacional no Parque Montanhas Nacional do Brazil. 12(1): 251–260 (doi: 10.1590/S1676- MontanhasTumucumaque, do Amapá,Tumucumaque, Brasil, ExediçõesAmapá, Brasil. I a V; pp.RAP 38–50,Bulletin in: of E. 06032012000100020 BiologicalBernard (ed.). Assessment Received: November 2013 48. Arlington: Conservation International/ Accepted: October 2014 Center for Applied Biodiversity Science. Published online: December 2014 Santos, T.G., D.C. Rossa-Feres and L. Iheringia, Casatti. 2007.Série Zoologia Diversidade e Editorial responsibility: Natan Maciel distribuição espaço-temporal de anuros em região com). pronunciada Appendix 1. estação seca no sudeste do Brasil. 97(1): 37–49 (doi: 10.1590/S0073-47212007000100007 Rhinella marina: Voucher specimens. Hypsiboas Segalla,Herpetologia M.V., U. Caramaschi, Brasileira C.A.G. Cruz, T. Grant, C.F.B. Haddad, J. Langone boans: Hypsiboas raniceps: and P.C.A. Garcia. 2014. Brazilian amphibians—List of species. Macapá: Parazinho (CECCAMPOSOsteocephalus 00668); taurinus: Scinax 3(2): perpusillus 37–48. Macapá: Parazinho (CECCAMPOS 00819); Osteocephalus oophagus: Silva, H.R. and R. Alves-Silva, R. 2008.Zootaxa New coastal and insular species of Macapá: Parazinho (CECCAMPOS 00059); Pseudis laevis: the bromeligenous group, from). the State of Rio de Macapá: Parazinho (CECCAMPOS Pseudis 00079); paradoxa: Janeiro, Brazil (Anura, Hylidae). 1914: 34–44 (http://www. Macapá: Parazinho (CECCAMPOS Scinax ruber: 00334); Macapá: mapress.com/zootaxa/2008/f/z01914p044f.pdf Parazinho Trachycephalus (CECCAMPOS 00066);typhonius: Macapá: Parazinho Souza, V.M., M.B. Souza and E.F. Morato. 2008. Revista Efeitos Brasileira da sucessão de (CECCAMPOS Leptodactylus 00073); petersii: Macapá: Parazinho (CECCAMPOS florestalZoologia sobre a anurofauna (Amphibia: Anura) da Reserva Catuaba). Leptodactylus00084); podicipinus: Macapá: Parazinho (CECCAMPOS e seu entorno, Acre, Amazônia sul-ocidental. Leptodactylus00584); latrans: Macapá: Parazinho (CECCAMPOS 00782);Pipa 25(1): 49–57 (doi: 10.1590/S0101-81752008000100008 pipa: Macapá: Parazinho (CECCAMPOS 00065); Zina, J., C.P.A. Prado, C.A. Brasileiro and C.F.B. Haddad. 2012. Anurans of gr. Macapá: Parazinho (CECCAMPOS 00070); the sandy coastal plains of the Lagamar Paulista, State of São Paulo, Macapá: Parazinho (CECCAMPOS 00934).

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