Herpetofauna of Protected Areas in the Caatinga VII: Aiuaba Ecological Station (Ceará, Brazil)

Herpetology Notes, volume 11: 929-941 (2018) (published online on 11 November 2018)

Herpetofauna of protected areas in the Caatinga VII: Aiuaba Ecological Station (Ceará, Brazil)

Taís Borges Costa1, Daniel Orsi Laranjeiras1, Francis Luiz Santos Caldas 2, Daniel Oliveira Santana1, Cristiana Ferreira da Silva4, Edna Paulino de Alcântara4, Samuel Vieira Brito1, Jéssica Yara Galdino1, Daniel Oliveira Mesquita1, Renato Gomes Faria2, Frederico Gustavo Rodrigues França3, Robson Waldemar Ávila4, and Adrian Antonio Garda5,*

Abstract. We provide a list of amphibians and reptiles recorded in a strict protection area in the Brazilian semiarid Caatinga, the Aiuaba Ecological Station, Ceará State, Brazil. We conducted herpetofauna surveys totaling 110 days of fieldwork using pitfall trap arrays, glue traps, and active searches. We recorded 57 species distributed in 23 families: 16 lizards, 1 amphisbaena, 17 snakes, 20 amphibians, and 3 chelonians. Rarefaction curves for snakes and all herpetofauna combined suggest that species richness may still be underestimated for the area, while amphibian and lizard species numbers are similar to values suggested by diversity estimators. Despite its relatively small area, the Aiuaba Ecological Station serves as a herpetofaunal refuge, protecting a representative set of Caatinga species.

Keywords. Anura, Squamate reptiles, chelonians, distribution, conservation

Introduction The Caatinga originally covered 10% of the Brazilian territory, but today over 60% of its area is covered by The Caatinga biome is the largest patch of Seasonally anthropogenic ecosystems (Silva et al., 2017). The Dry Tropical Forests (STDF), a highly fragmented biome comprises the states of Ceará, most of Paraíba, biome widespread from Mexico to Argentina (Prado, Rio Grande do Norte and Pernambuco, southeastern 2000). Protected areas in the Caatinga encompass 7.4% Piauí, western Alagoas and Sergipe, northern and of the biome (Silva et al., 2017), but most are among the least restrictive category in Brazil, known as APA (Área de Proteção Ambiental, or Environmental Protection Area), and all are critically underfunded (Oliveira and Bernard, 2017). Moreover, the Caatinga is also the least protected of Brazilian biomes, with under 2% of its 1 Universidade Federal da Paraíba, Centro de Ciências Exatas territory inserted in strict protection areas (Fonseca et e da Natureza, Departamento de Sistemática e Ecologia, al., 2017). Cidade Universitária, 58051-000, João Pessoa, PB, Brasil. 2 For a long time, the Caatinga’s fauna and flora were Universidade Federal de Sergipe, Departamento de Biologia, Laboratório de Cordados (Herpetologia/Ictiologia), Cidade considered poor and with few endemic species and, Universitária, Av. Marechal Rondon, s/n, Jardim Rosa Elze, hence, given low priority for conservation (Vanzolini, 49100-000, São Cristóvão, SE, Brasil. 1976). This first impression resulted from insufficient 3 Universidade Federal da Paraíba, Centro de Ciências inventories and was gradually abandoned as recent Aplicadas e Educação, Departamento de Engenharia e Meio studies reported much higher species richness and Ambiente, 58297-000, Rio Tinto, PB, Brasil. significant rates of endemism (Araujo and Silva, 2017; 4 Universidade Regional do Cariri, Departamento de Ciências Carmignotto and Astúa, 2017; Garda et al., 2017; Lima Físicas e Biológicas. Rua Cel. Antonio Luiz Pimenta, et al., 2017; Mesquita et al., 2017). Nevertheless, the 63105100, Crato, CE, Brasil. 5 Universidade Federal do Rio Grande do Norte, Laboratório Caatinga is still neglected, receiving less financial de Anfíbios e Répteis-LAR, Departamento de Botânica, support, less scientific and conservation initiatives, Ecologia e Zoologia, Centro de Biociências, Campus and having fewer research groups compared with other Universitário, Lagoa Nova,59078-900, Natal, RN, Brasil. biomes in Brazil (Santos et al., 2011). * Corresponding author. E-mail: [email protected] 930 Taís Borges Costa et al.

amphibian and reptile species richness in the Caatinga (Garda et al., 2017; Mesquita et al., 2017). Still, many areas of the biome are understudied, and knowledge gaps can hamper conservation strategies and resource use prioritization. The present study integrates the results of three independent field surveys �� list of herpetofauna species for Aiuaba Ecological Station in Ceará State, Brazil. Our results show a high diversity of frogs and reptiles in a lowland area of Caatinga that now likely represents one of the best sampled areas for amphibian and reptiles in the biome.

Material and Methods

Figure 1. Aiuaba Ecological Station, Ceará, Brazil. The Study area.—The Aiuaba Ecological Station is a strict numbers 1 to 12 refer to the sampling points. Legend: 1 = first use protection area located in Aiuaba Municipality, set of pitfall traps; 2, 8, 10, 11, 12 = active search points; 7 = Ceará State, Brazil (6° 35’ 58.1”S, 40° 07’ 20.5”W; Fig. rock outcrop area near the dam; 3 = second set of pitfalls; 4 1). It encompasses 11,525 hectares between latitudes = third set of pitfalls; 5 = fourth set of pitfalls; 6 = fifth set of 06° 35’ and 06° 40’S and longitudes 40° 07’ and 40° pitfalls; 9 = protected area head office. 20’W. It is inserted in the “Sertão dos Inhamuns” and “Depressão Sertaneja Setentrional”, presenting litholic soils and flat reliefs where erosive formations are more frequent and phyllites are the predominant rocks central Bahia, and northern Minas Gerais (Prado, 2003). (Velloso et al., 2002; Medeiros, 2004). The area is also It is one of the most degraded biomes in Brazil (Leal predominantly covered by arboreal Caatinga, although et al., 2005), and most of the local economy depends presenting other phytophysiognomies like carrasco, on public services, with the lowest human development dense arboreal Caatinga, and arboreal-shrubby Caatinga indicators in the country (Silva et al., 2017).� complex (Oliveira et al., 1983; Medeiros, 2004). The For a long time, the scarcity of inventories with rainy period usually occurs from October to April, with adequate description of sampling efforts and comparable mean annual precipitation ranging from 590 to 684 mm methodologies in the Caatinga contributed to the lack and mean annual temperatures from 25.3°C to 25.9°C of knowledge about its herpetofauna (Rodrigues, 2003; (Velloso et al., 2002; Medeiros, 2004). Albuquerque et al., 2012; Guedes et al., 2014)��me Sampling methods.—We conducted surveys during standardized inventories were recently conducted different periods of the dry and rainy seasons (Table 1), in protected areas like Estação Ecológica Raso da totaling 110 days of fieldwork. We used a combination Catarina-BA (Garda et al., 2013), Parque Nacional da of different sampling methods, including active Serra da Capivara-PI (Cavalcanti et al., 2014), Parque searches, occasional encounters, pitfall traps with drift Nacional do Catimbau-PE (Pedrosa et al., 2014), fences, funnel traps, and glue traps. Funnel and glue Estação Ecológica do Seridó-RN (Caldas et al., 2016), traps were implemented only in the September/October and Parque Nacional da Chapada da Diamantina-BA 2013 survey, while the remaining methods were used in (Magalhães et al., 2015). all surveys (Table 1). These studies helped improve comparisons between Survey I— One of us (SVB) conducted two 10-day the herpetofaunas in different regions in the biome, surveys in the dry (October-November) and rainy (April- besides contributing directly to the knowledge of May) seasons (Table 1), using 120 pitfall traps arranged Protected Area’s amphibian and reptile faunas. These in Y shape connected with 5m plastic drift fences and concerted efforts, along with other studies providing equally distributed in 3 areas (40 traps pear area). Day lists and distribution data for many localities (Loebmann and night actives searches were also conducted by two and Haddad, 2010; Moura et al., 2010; Roberto et al., researchers to complement trap captures. 2013; Roberto and Loebmann, 2016), have allowed a Survey II— One of us (RWA) coordinated eight 5-day recent re-evaluation of the geographic distribution of surveys using a standardized protocol of the Biodiversity Herpetofauna of protected areas in the Caatinga VII: Aiuaba Ecological Station 931

Table 1. SamplingTable 1. procedures Sampling procedures used in three used separate in three field separate surveys field for surveys herpetofauna for herpetofauna species atspecies the Aiuaba at the AiuabaEcological Station, Ceará State,Ecological Brazil. Details Station, on duration,Ceará State, sampling Brazil. methods, Details on season, duration, and samplingtraps used methods, are given season, for each and survey. traps used are given for each survey.

Survey Year Month Days in Sampling Methods Number and Season field volume of traps I 2010 October 10 pitfall traps with drift 30 arrays (four 30L- Dry season fences buckets/array) Y shape I 2011 April 10 pitfall traps with drift 30 arrays (four 30L- Rainy fences buckets/array) Y season shape II 2012 June and 5+5 pitfall traps with drift 10 arrays (eight 60L Rainy/dry September fences, visual searches buckets/array) season straight line III 2013 September 30 pitfall traps with drift 37 arrays, (4 buckets, Dry season and fences, visual searches, 60L, per array), Y October hoop traps and glue shape traps, II 2013 January 5+5 pitfall traps with drift 10 arrays (eight 60L Rainy and April fences, visual searches buckets/array) season straight line II 2013 June 5 pitfall traps with drift 10 arrays (eight 60L Rainy/dry fences, visual searches buckets/array) season straight line II 2014 February 5 pitfall traps with drift 10 arrays (eight 60L Rainy fences, visual searches buckets/array) season straight line II 2014 May and 5+5 pitfall traps with drift 10 arrays (eight 60L Rainy/dry June fences, visual searches buckets/array) season straight line

Table 2. Species richness estimates for amphibians, lizards, snakes and all herpetofauna combined for Aiuaba Ecological Station using different estimators and the individual-based rarefaction methods. Research Program from the Brazilian government arrays), in the driest area above the dam (10 arrays) and (PPBio, see Magnusson et al., 2005). Ten plots (250 Meannear ±a Standardhilly area Deviation (20 arrays). Our sampling points were x 1 m, alongEstimators the same elevational Amphibians isocline) were Lizards similar to thoseSnakes of surveys I andHerpetofauna III because of logistics sampled usingACE visual searches during20 ± 0 both the diurnal16 ± 0 (road accessibility)21.34 ± 0 and because 61.28 all ±physiognomies 0 of and nocturnal period. At the end of each sampling plot, the protected area are represented in these points (Fig. CHAO 1 20 ± 0.14 16 ± 0.5 19.45 ± 2.85 58.62 ± 2.83 80 pitfall traps with drift fences consisting of eight 2). We conducted day and night active searches, starting Jacknife1 22 ± 1 16 ± 0 22.88 ± 2.27 63 ± 2.64 buried buckets (60 L), 5 m apart in a straight line were 8:00 am and ending about 10:00 pm, avoiding warmest installed. Jacknife2 20 ± 0 14 ± 0 hours of the23.94 day (11:00± 0 am to 2:00 63 ± pm). 0 We surveyed as Survey III—ACHAO1P total of 37 pitfall20 trap arrays and 16148 many physiognomies21.87 and habitats59.54 as possible, according glue traps were% de installed Singletons in the protected 0 area in an effort0 to the availability35.3 of roads and12.5 logistic limitations. We coordinated by AAG for 30 consecutive days. Each inspected microhabitats for herpetofauna (fallen logs, trap array consisted of four buried buckets disposed bushes, rocks and litter) as well as the areas near pitfall in a Y shape with 120º angles among 6-meter drift arrays, trails near hills and some areas in the buffer fences connecting the central bucket to buckets at the zone of the protected area. As an additional method to extremities. Within the 6-meter radius around the central collect chelonians we placed three hoop-traps (60 cm in bucket we placed four glue traps: two on the ground, diameter and 2 m long) in the dam during five days with above rocks and/or fallen tree trunks, and two on tree sardines as bait. branches and trunks (Table 1, Fig. 2). We distributed Amphibians were euthanized with lidocaine (topic trap arrays along three main tracks: near a dam (seven 5% cream) and reptiles with a lethal dose of Tiopental®, 932 Taís Borges Costa et al.

Figure 2. Sampled areas and traps used in the Aiuaba Ecological Station, Ceará, Brazil. A and B = shrubby caatinga associated with rocky soils; C = dam; D = pitfall trap array; E = glue trap on fallen log; F = glue trap on tree trunk.

preserved in 10% formalin and stored in 70% ethanol. collection of the Regional University of Cariri (URCA- Specimen collection was authorized through federal H). permits issued to AAG (SISBIO #32575-1), FLSC (SISBIO #36095-8), RWA (SISBIO #32758-2) and Data analysis.—We constructed rarefaction curves TBC (SISBIO #29550-4). Voucher specimens were to evaluate species richness sampling efficacy. housed in the herpetological collections of the Federal These curves were estimated based on the number of University of Paraíba (CHUFPB) and the herpetological individual frogs, lizards, snakes and for the whole Herpetofauna of protected areas in the Caatinga VII: Aiuaba Ecological Station 933 herpetofauna combined (Gotelli and Colwell, 2001). recorded by a single method. Indeed, active searches Using the software ESTIMATES 9.1.0 (Colwell, and occasional encounters are efficient in collecting 2013), we obtained species richness estimators based fossorial or less abundant species like snakes, turtles, on abundance data (CHAO 1, CHAO1P and ACE) and amphisbaenians, or even some amphibians, what is and based on nonparametric incidence (CHAO 2 and corroborated by other studies conducted in the Caatinga JACKKNIFE 1 and 2) to determine the expected (Magalhães et al., 2013; Cavalcanti et al., 2014; Pedrosa richness of amphibians, reptiles and herpetofauna as a et al., 2014). Some species considered common for the whole. We conducted 1,000 randomizations without Caatinga, like Leptodactylus fuscus and Mabuya heathi, replacement with the original data. were only recorded by us through active searches and occasional encounters, what is in some ways counter Results intuitive, but may be explained by one of two hypotheses. First, during the time our inventories were conducted We documented 2,732 individuals from 57 species the Caatinga underwent one of the most drastic droughts distributed in 23 families: 16 lizards, 1 amphisbaenian, ever recorded, with reduced rainfalls even during the 17 snakes, 3 chelonians and 20 amphibians (Appendix rainy seasons (Marengo et al., 2016). Second, regional 1; Fig. 3, 4, 5). The rarefaction curves did not reach variation in species abundances and detectability the asymptote for snakes or for all the herpetofauna are only starting to be unveiled in the Caatinga. It is combined, evidencing that more species still can possible that this severe drought and/or such unknown be added to the list as sampling effort increases. regional patterns of abundances and detectability were Considering lizards and amphibians, rarefaction curves responsible for such otherwise common species in the reached the asymptote. The richness estimators ranged Caatinga being found only through active searches and between 20 and 22 species of amphibians and around occasional encounters. 16 species of lizards close to the total recorded by us The Caatinga biome is characterized by seasonal, (Table 2, Fig. 6). temporally spaced and unpredictable periods of rainfall (Ab’sáber, 2003; Prado, 2003). Because amphibians are Discussion significantly associated with humidity, they are more Amphibian and lizard species richness recorded in active during the rainy season and are frequently found Aiuaba Ecological Station are similar to other Caatinga buried or inactive during dry seasons (Warburg, 1997; areas recorded in most lowland caatinga areas (e.g. Navas et al., 2004). Therefore, it is paramount that field Moura et al., 2010; Garda et al., 2013; Roberto et al., surveys targeting frogs in the Caatinga be conducted 2013; Roberto and Loebmann, 2016). In contrast, we during rainy seasons. Indeed, field work during rainy recovered more species of snakes at Aiuaba Ecological periods has recovered much higher richness for this Station than most other areas reported in the literature, group in the Caatinga (Caldas et al., 2016), even in approaching richness values from areas with long term rapid inventories of a few days after the first heavy rains surveys (Mesquita et al., 2013). This likely results from (Santana et al., 2015). the significant field effort we employed, compared to Accordingly, most species of amphibians in the present short term inventories, as snakes are more secretive and survey were registered during the rainy season, even with demand more intensive survey efforts to be appropriately scant rains because of the severe draught the region was recorded. Nevertheless, simulations suggest that the facing. These include common species for the Caatinga, number of species we recorded is still underestimated like Pleurodema diplolister and Physalaemus spp., but (Fig. 7), showing that snakes remain elusive even after also some less-common taxa. Proceratophrys aridus, large efforts dedicated to survey a single area. for example, whose distribution is known only from the By combining more than one sampling method type locality (Milagres Municipality, Ceará State; Cruz species with different ecological requirements were et al., 2012), was recorded, extending its distribution captured. Five amphibians, four snakes, and one turtle about 200 km west. Elachistocleis piauienses, previously were found only in occasional encounters. Three lizards known only from the states of Ceará, Maranhão, and and four snakes were recorded only in active searches, Piauí (Frost, 2018), and Pseudopaludicola pocoto, and one frog species was recorded solely in pitfall traps. recently described for the Caatinga (Magalhães et al., This reinforces the use of a combination of different 2014) are amongst the most abundant amphibians in this sample methodologies, because some species were part of the Caatinga and were also frequently recorded 934 Taís Borges Costa et al.

Figure 3. Amphibians collected in Aiuaba Ecological Station, Ceará, Brazil. A - Rhinella granulosa; B - Rhinella jimi; C – Dendropsophus nanus; D - Dendropsophus soaresi; E - Boana raniceps; F - Phyllomedusa nordestina; G - Scinax x-signatus; H - Proceratophrys aridus; I – Dermatonotus muelleri (juvenile); J - Elachistocleis piauiensis; K - Leptodactylus chaquensis; L - Leptodactylus troglodytes; M - Leptodactylus vastus; N - Physalaemus albifrons; O - Pseudopaludicola pocoto.

in the protected area during our inventories. (Werneck et al., 2012; Oliveira et al., 2015; Mesquita The most abundant lizard species in the area are widely et al., 2017). Coleodactylus meridionalis, however, has distributed in the Caatinga, such as Tropidurus hispidus, a relictual distribution in the Caatinga (Mesquita et al., Gymnodactylus geckoides, Ameivula ocellifera, 2017), being typically found in forested habitats and Vanzosaura multiscutata, and Phyllopezus pollicaris mesic enclaves (but see Ribeiro et al., 2013). This first Herpetofauna of protected areas in the Caatinga VII: Aiuaba Ecological Station 935

Figure 4. Species of lizards, and amphisbaenians recorded in Aiuaba Ecological Station, Ceará, Brazil. A - Phyllopezus pollicaris; B - Hemidactylus agrius; C - Lygodactylus klugei; D – Gymnodactylus geckoides; E - Coleodactylus meridionalis; F - Mabuya heathi; G - Tropidurus hispidus; H – Tropidurus jaguaribanus; I – Micrablepharus maximiliani; J – Vanzosaura multiscutata; K – Ameiva ameiva; L – Ameivula ocellifera; M – Iguana iguana; N – Polychrus acutirostris; O – Amphisbaena vermicularis.

report of C. meridionalis outside mesic enclaves or areas abundant lizard, Tropidurus jaguaribanus, is distributed under their influence in Ceará state shows that, despite along the Jaguaribe river valley (Piauí and Ceará states) having a relictual distribution and a very small body and is endemic to the Caatinga biome (Passos et al., size, the species seems to tolerate climates otherwise 2011). too harsh for mesic forest species. The second most The Aiuaba Ecological Station presents one of the 936 Taís Borges Costa et al.

Figure 5. Snakes and chelonians recorded in Aiuaba Ecological Station, Ceará, Brazil. A - Epictia borapeliotes; B - Boa constrictor; C - Leptodeira annulata; D - Erythrolamprus viridis; E - Erythrolamprus poecilogyrus; F - Leptophis ahaetulla; G - Oxyrhopus trigeminus; H - Philodryas nattereri; I - Pseudoboa nigra; J - Micrurus ibiboboca; K - Crotalus durissus; L - Phrynops geoffroanus.

richest herpetofauna reported for a Caatinga strictu and 126 reptiles are recognized throughout the state of sensu site. Some areas, including sites in Ceará state, Ceará, occurring in many distinct phytophysiognomies have higher overall richness, but include many species and under the influence of neighboring biomes, such typical of mesic enclaves. For the Ibiapaba-Araripe as the Amazon Forest and Cerrado (Roberto and complex, for example, 38 amphibian and 84 reptile Loebmann, 2016). species have been reported. However, this region has at The Aiuaba Ecological Station was recognized a least five different phytophysiognomies, including areas priority area for conservation in the Caatinga biome of Cerrado (savannas), Caatinga, and rainforest enclaves but, until now, no survey reporting amphibian and (Loebmann and Haddad, 2010). Fifty-seven amphibians reptiles existed for the area. We hope the species list Table 1. Sampling procedures used in three separate field surveys for herpetofauna species at the Aiuaba Ecological Station, Ceará State, Brazil. Details on duration, sampling methods, season, and traps used are given for each survey.

Table 2. Species richness estimates for amphibians, lizards, snakes and all herpetofauna combined for Aiuaba Ecological Station using differentTable estimators 2. Species and richness the individual-based estimates for amphibians, rarefaction lizards, methods. snakes and all herpetofauna combined for Aiuaba Ecological Station using different estimators and the individual-based rarefaction methods.

Mean ± Standard Deviation Estimators Amphibians Lizards Snakes Herpetofauna ACE 20 ± 0 16 ± 0 21.34 ± 0 61.28 ± 0 CHAO 1 20 ± 0.14 16 ± 0.5 19.45 ± 2.85 58.62 ± 2.83 Jacknife1 22 ± 1 16 ± 0 22.88 ± 2.27 63 ± 2.64 Jacknife2 20 ± 0 14 ± 0 23.94 ± 0 63 ± 0 CHAO1P 20 16 21.87 59.54 % de Singletons 0 0 35.3 12.5

we provide will assist the planning and implementation describe the areas local richness and effectively protect of conservation actions in this area. An eventual its biodiversity. Also, areas outside the sites we sampled management plan should aim to increase sampling for demand investigation, as our surveys were concentrated some groups, especially snakes, in order to adequately in areas near roads and protected area’s facilities.

Figure 6. Species rarefaction curves based on abundance data for Amphibians, Lizards, and Snakes collected at Aiuaba Ecological Station, Ceará, Brazil. 938 Taís Borges Costa et al.

Acknowledgements. Many students, protected area’s staff in Caatinga: The Largest Tropical Dry Forest Region in South members, and researchers helped during field work, and we are in America, p. 133–149. Silva, J.M.C., Leal, I. , Tabarelli, M., Ed., debt with their kind support and effort. We specifically thank the Berlin, Springer-Verlag. crew of ESEC AIUABA for logistic and personnel support during Gotelli, N.J., Colwell, R.K. (2001): Quantifying biodiversity: our fieldwork. TBC thanks to CAPES for her PhD fellowship. procedures and pitfalls in the measurement and comparison of This work was supported by grants from CNPq/ICMBio to AAG species richness. Ecology Letters 4: 379–391. (Grant #552031/2011-9) and RWA (Grant #551993/2011-1). Guedes, T.B., Nogueira, C., Marques, O.A. (2014): Diversity, natural history, and geographic distribution of snakes in the References Caatinga, Northeastern Brazil. Zootaxa 3863: 1–93. Leal, I.R., Silva, J.M.C., Tabarelli, M., Lacher, T.E. (2005): Ab’sáber, A.N. (2003): Os Domínios de Natureza no Brasil: Changing the course of biodiversity conservation in the Caatinga Potencialidades Paisagísticas, São Paulo, Ateliê Editorial. of northeastern Brazil. Conservation Biology 19: 701–706. Albuquerque, U.P., Araújo, E.L., El-Deir, A.C., De Lima, A.L., Lima, S.M.Q., Ramos, T.P.A., Da Silva, M.J., Rosa, R.S. (2017): Souto, A., Bezerra, B.M., et al. (2012): Caatinga revisited: Diversity, Distribution, and Conservation of the Caatinga ecology and conservation of an important seasonal dry forest. Fishes: Advances and Challenges. In: Biodiversity, Ecosystems The Scientific World Journal 2012: 205182. Services and Sustainable Development in Caatinga: The Largest Araujo, H.F.P., Silva, J.M.C. (2017): The Avifauna of the Caatinga: Tropical Dry Forest Region in South America, p. 97–131. Silva, Biogeography, Ecology, and Conservation. In: Biodiversity, J.M.C., Leal, I. , Tabarelli, M., Ed., Berlin, Springer-Verlag. Ecosystems Services and Sustainable Development in Caatinga: Loebmann, D., Haddad, C.F.B. (2010): Amphibians and reptiles The Largest Tropical Dry Forest Region in South America, p. from a highly diverse area of the Caatinga domain: composition 181–210. Silva, J.M.C., Leal, I. , Tabarelli, M., Ed., Berlin, and conservation implications. Biota Neotropica 10: 227–256. Springer-Verlag. Magalhães, F.M., Dantas, A.K.B.P., Brito, M.R.M., Medeiros, Caldas, F.L.S., Costa, T.B., Laranjeiras, D.O., Mesquita, D.O., P.H.S., Oliveira, A.F., Pereira, et al. (2013): Anurans from an Garda, A.A. (2016): Herpetofauna of protected areas in the Atlantic Forest-Caatinga ecotone in Rio Grande do Norte State, Caatinga V: Seridó Ecological Station (Rio Grande do Norte, Brazil. Herpetology Notes 6: 1–10. Brazil). Check List 12: 1929. Magalhães, F.M., Laranjeiras, D.O., Costa, T.B., Juncá, F.A., Carmignotto, A.P., Astúa, D. (2017): Mammals of the Caatinga: Mesquita, D.O., Röhr, D.L., et al. (2015): Herpetofauna of Diversity, Ecology, Biogeography, and Conservation. In: protected areas in the Caatinga IV: Chapada Diamantina Biodiversity, Ecosystems Services and Sustainable Development National Park, Bahia, Brazil. Herpetology Notes 8: 243–261. in Caatinga: The Largest Tropical Dry Forest Region in South Magalhães, F.M., Loebmann, D., Kokubum, M.N.D.C., Haddad, America, p. 211–254. Silva, J.M.C.D., Leal, I. , Tabarelli, M., C.F.B., Garda, A.A. (2014): A new species of Pseudopaludicola Ed., Berlin, Springer-Verlag. (Anura: Leptodactylidae: Leiuperinae) from northeastern Brazil. Cavalcanti, L.B.Q., Costa, T.B., Colli, G.R., Costa, G.C., França, Herpetologica 70: 77–88. F.G.R., Mesquita, D.O., et al. (2014): Herpetofauna of protected Magnusson, W.E., Lima, A.P., Luizão, R., Luizão, F., Costa, areas in the Caatinga II: Serra da Capivara National Park. Check F.R.C., Castilho, C.V., Kinupp, V.F. (2005): RAPELD: a List 10: 18–27. modification of the gentry method for biodiversity surveys in Colwell, R.K. (2013): EstimateS: Statistical Estimation of Species long-term ecological research sites. Biota Neotropica 5: 19–24. Richness and Shared Species from Samples. University of Marengo, J.A., Torres, R.R., Alves, L.M. (2016): Drought in Connecticut, USA. Northeast Brazil—past, present, and future. Theoretical and Cruz, C.A.G., Nunes, I., Juncá, F.A. (2012): Redescription of Applied Climatology 129: 1189–1200. Proceratophrys cristiceps (Müller, 1883)(Amphibia, Anura, Medeiros, J.B.L.P. (2004): Zoneamento fito-ecológico da Estação Odontophrynidae), with description of two new species without Ecológica de Aiuaba – uma contribuição à educação ambiental eyelid appendages from Northeastern Brazil. South American e à pesquisa científica. Unpublished Universidade Federal do Journal of Herpetology 7: 110–122. Ceará, Fortaleza, p. 141. Fonseca, C.R., Antongiovanni, M., Matsumoto, M., Bernard, E., Mesquita, D.O., Costa, G.C., Garda, A.A., Delfim, F.R. (2017): Venticinque, E.M. (2017): Conservation Opportunities in the Species Composition, Biogeography and Conservation of Caatinga. In: Biodiversity, Ecosystems Services and Sustainable Caatinga Lizards. In: Biodiversity, Ecosystems Services and Development in Caatinga: The Largest Tropical Dry Forest Sustainable Development in Caatinga: The Largest Tropical Region in South America, p. 429–443. Silva, J.M.C., Leal, I. , Dry Forest Region in South America, p. Silva, J.M.C., Leal, I. , Tabarelli, M., Ed., Berlin, Springer-Verlag. Tabarelli, M., Ed., Springer-Verlag. Garda, A.A., Costa, T.B., Santos-Silva, C.R., Mesquita, D.O., Mesquita, P.C.M.D., Passos, D.C., Borges-Nojosa, D.M., Cechin, Faria, R.G., Conceicão, B.M et al. (2013): Herpetofauna of S.Z. (2013): Ecologia e história natural das serpentes de uma protected areas in the Caatinga I: Raso da Catarina Ecological área de Caatinga no Nordeste Brasileiro. Papéis Avulsos de Station. Check List 9: 405–414. Zoologia (São Paulo) 53: 99–113. Garda, A.A., Stein, M.G., Machado, R.B., Lion, M.B., Juncá, F.A., Moura, G.J.B., Santos, E.M., Oliveira, M.A.B., Cabral, M.C.C. Napoli, M.F. (2017): Ecology, Biogeography and Conservation (2010): Herpetofauna no Estado de Pernambuco, Brasília, of Amphibians in the Semiarid Brazilian Caatinga. In: Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Biodiversity, Ecosystems Services and Sustainable Development Renováveis. Herpetofauna of protected areas in the Caatinga VII: Aiuaba Ecological Station 939

Navas, C.A., Antoniazzi, M.M., Jared, C. (2004): A preliminary Roberto, I.J., Ribeiro, S.C., Loebmann, D. (2013): Amphibians of assessment of anuran physiological and morphological the state of Piauí, Northeastern Brazil: a preliminary assessment. adaptation to the Caatinga, a Brazilian semi-arid environment. Biota Neotropica 13: 322–330. International Congress Series 1275: 298–305. Rodrigues, M.T. (2003): Herpetofauna da Caatinga. In: Ecologia e Oliveira, A.P.C., Bernard, E. (2017): The financial needs vs. the Conservação da Caatinga, p. 181–236. Leal, I.R., Tabarelli, M. , realities of in situ conservation: an analysis of federal funding for Silva, J.M.C., Ed., Recife, Editora Universitária da UFPE. protected areas in Brazil’s Caatinga. Biotropica 49: 745–752. Santana, D.J., Mângia, S., Silveira-Filho, R.R., Barros, L.C.S., Oliveira, E.F., Gehara, M., Sao Pedro, V.A., Chen, X., Myers, Andrade, I., Napoli, M.F., Juncá, F., Garda, A.A. (2015): E.A., Burbrink, F.T., et al. (2015): Speciation with gene flow Anurans from the middle Jaguaribe River region, Ceará State, in whiptail lizards from a Neotropical xeric biome. Molecular Northeastern Brazil. Biota Neotropica 15: 1–8. Ecology 24: 5957–5975. Santos, J.C., Leal, I.R., Almeida-Cortez, J.S.D., Fernandes, Oliveira, J.G.B., Cesar, H.L., Nunes, E.P. (1983): Vegetação. G.W., Tabarelli, M. (2011): Caatinga: the scientific negligence In: Projeto Aiuaba – Relatório técnico, p. 117–130. Oliveira, experienced by a dry tropical forest. Tropical Conservation J.G.B., Ed., Fortaleza, Science 4: 276–286. Passos, D.C., Lima, D.C., Borges-Nojosa, D.M. (2011): A Silva, J.M.C., Barbosa, L.C.F., Leal, I.R., Tabarelli, M. (2017): new species of Tropidurus (Squamata, Tropiduridae) of the The Caatinga: Understanding the Challenges. In: Biodiversity, semitaeniatus group from a semiarid area in Northeastern Brazil. Ecosystems Services and Sustainable Development in Caatinga: Zootaxa 2930: 60–68. The Largest Tropical Dry Forest Region in South America, p. 3– Pedrosa, I.M.M.C., Costa, T.B., Faria, R.G., França, F.G.R., 19. Silva, J.M.C., Leal, I. , Tabarelli, M., Ed., Berlin, Springer- Laranjeiras, D.O., Oliveira, et al. (2014): Herpetofauna of Verlag. protected areas in the Caatinga III: The Catimbau National Park, Vanzolini, P.E. (1976): On the lizards of a Cerrado-Caatinga Pernambuco, Brazil. Biota Neotropica 14: 1–12. contact: evolutionary and zoogeographical implications (Sauria). Prado, D.E. (2000): Seasonally dry forests of tropical South Papéis Avulsos de Zoologia (São Paulo) 29: 111–119. America: from forgotten ecosystems to a new phytogeographic Velloso, A.L., Sampaio, E.V.S.B., Pareyn, F.G.S. (2002): unit. Edinburgh Journal of Botany 57: 437–461. Ecorregiões: Propostas Para o Bioma Caatinga, Recife, The Prado, D.E. (2003): As Caatingas da América do Sul. In: Ecologia Nature Conservancy do Brasil. e Conservação da Caatinga, p. 3–73. Leal, I.R., Tabarelli, M. , Warburg, M.R. (1997): Ecophysiology of Amphibians Inhabiting Silva, J.M.C., Ed., Recife, Ed. Universitária da UFPE. Xeric Environments, Berlin, Springer. Ribeiro, L.B., Goliath, M., Rodrigues, R.G., Barreto, R.M.F., Werneck, F.P., Gamble, T., Colli, G.R., Rodrigues, M.T., Sites Jr, Freire, E.M.X. (2013): Two new records of Coleodactylus J.W. (2012): Deep diversification and long-term persistence in meridionalis (Boulenger, 1888) (Squamata, Sphaerodactylidae) South American ‘Dry Diagonal’: integrating continent-wide in north-eastern Brazil, including a map and comments regarding phylogeography and distribution modeling of geckos. Evolution its geographical distribution. Herpetology Notes 6: 23–27. 66: 3014–3034. Roberto, I.J., Loebmann, D. (2016): Composition, distribution patterns, and conservation priority areas for the herpetofauna of the state of Ceará, northeastern Brazil. Salamandra 52: 134– 152. 940 Taís Borges Costa et al.

Appendix 1. Herpetofauna of Aiuaba Ecological Station, Ceará, Brazil. Abbreviations: AS= Active search; 65GT= glue trap; PT= pitfall trap; OE= occasionalAppendix 1encounter;. Herpetofauna Hoop-trap=HT. of Aiuaba Ecological Station, Ceará, Brazil. Abbreviations: AS= Active search; GT= glue trap; PT= pitfall trap; OE= occasional encounter; Hoop-trap=HT.

Sampling Taxon Voucher Abundance Method Amphibia (n= 20) Bufonidae Rhinella granulosa (Spix, 1824) URCA-H 7443 AS, PT, OE 40 Rhinella jimi (Stevaux, 2002) FSCHUFPB 6527 AS, OE 29 Hylidae Corythomantis greeningi Boulenger, 1986 URCA-H 5550 AS, OE 12 Dendropsophus nanus (Boulenger, 1989) FSCHUFPB 3075 OE, AS 167 Dendropsophus soaresi (Caramaschi & Jim, 1983) URCA-H 7391 AS, OE 7 Boana raniceps (Cope, 1862) FSCHUFPB 3071 AS, OE, PT 34 Phyllomedusa nordestina Caramaschi, 2006 FSCHUFPB 6564 AS, OE 24 Scinax x-signatus (Spix, 1824) FSCHUFPB 3278 AS, OE, PT 36 Leptodactilydae Leptodactylus fuscus (Schneider, 1799) URCA-H 7545 AS, OE 19 Leptodactylus chaquensis Cei, 1950 FSCHUFPB 3017 AS, OE 143 Leptodactylus troglodytes Lutz, 1926 FSCHUFPB 6361 AS, OE, PT 33 Leptodactylus vastus Lutz, 1930 FSCHUFPB 3028 AS, OE 45 Physalaemus albifrons (Spix, 1824) URCA-H 7373 AS, OE, PT 41 Physalaemus cicada Bokermann, 1966 URCA-H 7443 AS, OE, PT 50 Physalaemus cuvieri Fitzinger, 1826 URCA-H 7454 AS, OE, PT 29 Pleurodema diplolister (Peters, 1870) URCA-H 7388 AS, OE 21 Pseudopaludicola pocoto Magalhães et al. 2014 FSCHUFPB 2000 AS, OE, PT 263 Microhylidae Dermatonotus muelleri (Boettger, 1885) URCA-H 7401 AS, OE, PT 8 Elachistocleis piauiensis Caramaschi and Jim, 1983 URCA-H 7461 AS, OE, PT 4 Odontophrynidae Proceratophrys aridus Cruz, Nunes, and Juncá, 2012 URCA-H 7523 AS, OE 19 Lacertoidea (n=17) Amphisbaenidae Amphisbaena vermicularis Wagler, 1824 FSCHUFPB 3101 PT, AS 9 Gekkonidae Hemidactylus agrius Vanzolini, 1978 FSCHUFPB 6368 PT, AS, GT, OE 35 Hemidactylus brasilianus (Amaral, 1935) FSCHUFPB 3161 PT, AS, GT, OE 10 Lygodactylus klugei (Smith, Martin & Swain, 1977) FSCHUFPB 3015 PT, AS, GT, OE 48 Gymnophthalmidae Micrablepharus maximiliani (Reinhardt & Lütken, 1862) FSCHUFPB 3332 PT, AS, GT 28 Vanzosaura multiscutata (Amaral, 1933) FSCHUFPB 3016 PT, AS, GT 180 Iguanidae Iguana iguana (Linnaeus, 1758) URCA-H 4765 AS 4

Phyllodactylidae Gymnodactylus geckoides Spix, 1825 FSCHUFPB 3021 PT, AS, GT, OE 233 Phyllopezus pollicaris (Spix, 1825) FSCHUFPB 3061 PT, AS, GT, OE 162 Mabuyidae Mabuya heathi (Schmidt & Inger, 1951) FSCHUFPB 6314 AS 13 Sampling Taxon Voucher Abundance Method Polychrotidae Polychrus acutirostris Spix, 1825 URCA-H 6536 OE 2 Sphaerodactylidae Coleodactylus meridionalis (Boulenger, 1888) FSCHUFPB 3301 PT, AS 9 Teiidae Ameiva ameiva (Linnaeus, 1758) FSCHUFPB 3067 PT, AS 40 Ameivula ocellifera (Spix, 1825) FSCHUFPB 3030 PT, AS 197 Salvator merianae (Duméril & Bibron, 1839) URCA-H 5140 AS 2 Tropiduridae Tropidurus hispidus (Spix, 1825) FSCHUFPB 3029 PT, AS, GT, OE 421 Tropidurus jaguaribanus Passos, Lima & Borges- FSCHUFPB 3268 PT, AS, OE 259 Nojosa, 2011 Snakes (n= 17) Boidae Boa constrictor Linnaeus, 1758 URCA-H 6735 OE, AS 2 Epicrates assisi Machado, 1945 OE 1 Colubridae Oxybelis aeneus (Wagler, 1824) Road kill AS 1 Leptophis ahaetulla (Linnaeus, 1758) URCA-H 5539 AS, OE 1 Dipsadidae Apostolepis cearensis Gomes, 1915 FSCHUFPB 3201 PT 1 Leptodeira annulata (Linnaeus, 1758) FSCHUFPB 3200 AS, OE 6 Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 FSCHUFPB 3025 AS, OE 12 Philodryas nattereri Steindachner, 1870 FSCHUFPB 6618 AS 2 Philodryas olfersii (Lichtenstein, 1823) URCA-H 1774 AS 1 Pseudoboa nigra (Duméril, Bibron & Duméril, 1854) URCA-H 9536 AS 2 Erythrolamprus poecilogyrus (Wied-Neuwied, 1825) URCA-H 3739 AS 3 Erythrolamprus viridis (Günther, 1862) URCA-H 3740 AS, OE 1 Elapidae Micrurus ibiboboca (Merrem, 1820) FSCHUFPB 3108 OE, AS, PT 4 Leptotyphlopidae Epictia borapeliotes (Vanzolini, 1996) FSCHUFPB 3270 AS, PT 4 Viperidae Bothrops erythromelas Amaral, 1923 URCA-H 3148 AS, OE 3 Bothrops leucurus Wagler, 1824 FSCHUFPB 3027 AS, OE 2 Phyllodactylidae HerpetofaunaGymnodactylus of protected geckoides areas in Spix, the 1825 Caatinga VII: AiuabaFSCHUFPB Ecological 3021 Station PT, AS, GT, OE 233 941 Phyllopezus pollicaris (Spix, 1825) FSCHUFPB 3061 PT, AS, GT, OE 162 Appendix 1. Continued.Mabuyidae Mabuya heathi (Schmidt & Inger, 1951) FSCHUFPB 6314 AS 13 Sampling Taxon Voucher Abundance Method Polychrotidae Polychrus acutirostris Spix, 1825 URCA-H 6536 OE 2 Sphaerodactylidae Coleodactylus meridionalis (Boulenger, 1888) FSCHUFPB 3301 PT, AS 9 Teiidae Ameiva ameiva (Linnaeus, 1758) FSCHUFPB 3067 PT, AS 40 Ameivula ocellifera (Spix, 1825) FSCHUFPB 3030 PT, AS 197 Salvator merianae (Duméril & Bibron, 1839) URCA-H 5140 AS 2 Tropiduridae Tropidurus hispidus (Spix, 1825) FSCHUFPB 3029 PT, AS, GT, OE 421 Tropidurus jaguaribanus Passos, Lima & Borges- FSCHUFPB 3268 PT, AS, OE 259 Nojosa, 2011 Snakes (n= 17) Boidae Boa constrictor Linnaeus, 1758 URCA-H 6735 OE, AS 2 Epicrates assisi Machado, 1945 OE 1 Colubridae Oxybelis aeneus (Wagler, 1824) Road kill AS 1 Leptophis ahaetulla (Linnaeus, 1758) URCA-H 5539 AS, OE 1 Dipsadidae Apostolepis cearensis Gomes, 1915 FSCHUFPB 3201 PT 1 Leptodeira annulata (Linnaeus, 1758) FSCHUFPB 3200 AS, OE 6 Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 FSCHUFPB 3025 AS, OE 12 Philodryas nattereri Steindachner, 1870 FSCHUFPB 6618 AS 2 Philodryas olfersii (Lichtenstein, 1823) URCA-H 1774 AS 1 Pseudoboa nigra (Duméril, Bibron & Duméril, 1854) URCA-H 9536 AS 2 Erythrolamprus poecilogyrus (Wied-Neuwied, 1825) URCA-H 3739 AS 3 Erythrolamprus viridis (Günther, 1862) URCA-H 3740 AS, OE 1 Elapidae Micrurus ibiboboca (Merrem, 1820) FSCHUFPB 3108 OE, AS, PT 4 Leptotyphlopidae Epictia borapeliotes (Vanzolini, 1996) FSCHUFPB 3270 AS, PT 4 Viperidae Bothrops erythromelas Amaral, 1923 URCA-H 3148 AS, OE 3 Bothrops leucurus Wagler, 1824 FSCHUFPB 3027 AS, OE 2 Crotalus durissus Linnaeus, 1758 FSCHUFPB 6401 AS 2 Testudines (n= 3) Chelidae Mesoclemmys tuberculata (Luederwaldt, 1926) URCA-H 1225 AS 1 Phrynops geoffroanus (SCHWEIGGER, 1812) FSCHUFPB 6637 HT, OE 6 Kinosternidae Kinosternon scorpioides (Linnaeus, 1766) vestige/shell OE 1 FSCHUFPB: Field Series, Coleção Herpetológica da Universidade Federal da Paraíba; URCA-H: Coleção Herpetológica da Universidade Regional do Cariri Accepted by Anamarija Zagar