Herpetology Notes, volume 9: 175-183 (2016) (published online on 01 September 2016)

Reptiles of an urban Atlantic Rainforest fragment in the state of Pernambuco, northeastern

Camila Nascimento de Oliveira¹,*, Sérgio Luiz da Silva Muniz² and Geraldo Jorge Barbosa de Moura²

Abstract. Knowledge of in strategic regions, even if only fragmentary, is an excellent way for making inferences regarding the local biodiversity, which is paramount for conservation strategies for any biological group. The objectives of the present study were to record the composing the fauna of the forest fragment studied and their habitat and microhabitat occupation. The inventory was carried out in the Tejipió forest, state of Pernambuco, northeastern Brazil, from October 2011 to April 2012. Sampling was performed by means of active searching, pitfall trapping, accidental sightings and local collectors. A total of 24 species in 15 different families were reported (one tortoise, eleven , three amphisbaenians, eight and one crocodile). The habitat and microhabitat with greatest occurrence of species were the edge of the forest and soil with vegetation, respectively.

Keywords: , Inventory, Species richness, Microhabitat, Tejipió forest.

Introduction temporal distribution of species (Bernardo et al., 2012), among other matters. Inventories are the basis for biological characterization The Atlantic Rainforest is of worldwide importance of a given area. They provide biogeographical data for biological diversity and, because of the high levels and quantitative information of species, and enable of forest degradation and species endemism, this is a evaluation of the quality of forest fragments. Moreover, priority area for conservation (Myers et al., 2000; inventories may present complementary information on Conservation International, 2013). This status has been species, which in combination, aid in monitoring and given because of its constant losses and fragmentation evaluating their conservation status (Sousa et al., 2012; of habitats (Fahrig, 2003; Rocha et al., 2007; Martensen França et al., 2012). Inventories published regarding et al., 2008; Ribeiro et al., 2009), among other causes. Atlantic Rainforest reptiles of Brazil have supplied These actions alter the composition of biological groups, information such as on expansion of the distribution potentially causing species extinction (Tabarelli et al., of species (Santana et al., 2008), endemism situation 1999; Brooks et al., 2002; Fahrig, 2003) and decreased (Condez et al., 2009; Sousa et al., 2012) and spatial- genetic diversity of populations (Dixo et al., 2009). According to Gomides (2010), forest fragments created through human action become “islands” of biodiversity and act as alternatives for ensuring the survival of 1 Universidade Federal de Pernambuco, Programa de Pós- species. Thus, the Atlantic Rainforest is particularly graduação em Biologia (PPGBA), Av. Prof. Moraes important because of the occurrence of endemic species Rego, 1235, Cidade Universitária, CEP: 50670-901, Recife, of reptiles (Marques and Sazima, 2004), which occupy Pernambuco, PE, Brazil. a wide range of habitats and microhabitats (Sales et 2 Universidade Federal Rural de Pernambuco, Laboratório de al., 2009). Knowledge of how species use or share Estudos Herpetológicos e Paleoherpetológicos, Rua Dom microhabitat is important for understanding how the Manoel de Medeiros, s/n, Dois Irmãos, CEP: 52171-900, Recife, Pernambuco, PE, Brazil. community is structured and how species respond * Corresponding author e-mail: to changes in the environment (Santana et al., 2008; [email protected] Bertoluci et al., 2009). 176 Camila Nascimento de Oliveira et al.

Materials and Methods Study site Reptile survey took place in an Atlantic Rainforest fragment of 172 ha (Tejipió forest) (08°05’45.59” S, 34°57’04.91” W) (Figure 1), located at Km 73 of the BR-101 Sul Highway, in the district of Tejipió, municipality of Recife, state of Pernambuco. This area has the phytophysiognomy of a rainforest (Veloso et al., 1991), with a mean minimum temperature of 21.8°C and mean maximum temperature of 29.1°C and mean annual rainfall of 2,458 mm (World Weather Information Service, 2013). The site is located within the Tejipió river hydrographic basin (Araújo and Pires, 1998). According to Feitosa (2004), this fragment presents low heterogeneity of arboreal inventory, because the vegetation has been observed to be going through secondary succession stages, with regeneration processes that began approximately 46 years ago. The study site contains a lentic water body (i.e. a lake) in the forested area and, on the edges of the forest, there are local communities and a military construction area, with another smaller lake nearby.

Data collection Sampling was performed between the months of October 2011 and April 2012 using pitfall traps with drift fences (Campbell and Christman, 1982; Cechin and Martins, 2000), time-constrained active searching (manual capture and visual identification) (Campbell and Christman, 1982), accidental sightings and local collectors. The traps were installed at six sampling stations. Figure 1. Map showing the location of the study site (Tejipió Each station had four buckets (two with 22 L capacity forest), together with the military area. The yellow dots show and one with 60 L capacity, intercalated), which were the location of the pitfall traps. arranged linearly and connected by 10 m of plastic drift fences. Active searches were carried out for four hours per day at different points of the study site, with diurnal and nocturnal searches. The sampling effort totalized 16.128 hours of trapping and 112 man-hours of active However, some fragments of this biome still need searching. to be characterized regarding the composition and The specimens caught were identified and environmental occupation of reptile species. Thus, the released (collecting permit 31795-1 – ICMBio) and present study aim to record the composition and spatial any individuals found dead were deposited in the specificity (habitat and microhabitat) of reptile species Herpetology Collection of the Federal Rural University that occur in a fragment of Atlantic Rainforest in the of Pernambuco (CHP-UFRPE; Appendix 1). state of Pernambuco. Data analysis The constancy of occurrence index (C) was used to indicate the frequency of occurrence of species, as Reptiles of an urban Atlantic Rainforest fragment in the state of Pernambuco, Brazil 177 proposed by Dajoz (2005). According to these results, and Kentropyx calcarata were sampled exclusively by the species were considered to be constant (species that pitfall traps. Three individuals were visually identified occurred in more than 50% of the samples), accessory at family level (Mabuyidae) and were found on the edge (species that occurred in 25% to 50% of the samples) or of the forest, in soil with no vegetation. Outside of the accidental (species that occurred in fewer than 25% of sampling period, another three species were captured, the samples). Eunectes murinus, Norops ortonii and Pseudoboa nigra: To evaluate the sampling effect, a rarefaction curve was these were identified by means of photographs and from constructed. Species richness was calculated through the specimens handed in. The Pseudoboa nigra were the richness estimators Ace, Chao 1, Jackknife 1 and deposited in the Herpetology Collection of the Federal Bootstrap, using 500 random additions of the samples. University of Pernambuco (CHUFPE, Appendix 1). Graphs based on the estimators were also created in The Cercosaura ocellata was also identified, thus order to compare the observed richness. All the analyses demonstrating that its distribution (with coordinates) were carried out using the EstimateS® software, version has expanded to the state of Pernambuco (Oliveira and 8.2.0 (Colwell, 2009). Moura, 2013). To determine the microhabitats, only the reports Results and Discussion from the manual captures, chance encounters, visual identification and data from local collectors were A total of 24 reptile species belonging to 21 genera considered. The habitat with the greatest number of that were distributed among 15 families were species was the edge of the forest (10 spp.), followed by recorded: (3 spp.), (2 spp.), the open area, forested area and constructed area, all with (1 sp.), (1 sp.), (1 the same number of species (9 spp.). The microhabitat sp.), (1 sp.), (1 sp.), of soil with vegetation showed the greatest richness of Sphaerodactylidae (1 sp.), (3 spp.), species (10 spp.), followed by paved ground (9 spp.), (1 sp.), (2 spp.), Dipsadidae (3 spp.), soil with no vegetation (7 spp.) and dry leaf cover (5 (2 spp.), Chelidae (1 sp.) and Alligatoridae (1 spp.) (Table 1). sp.) (Table 1) (Figure 2). Some species shared the same habitats, such as the open Families with greatest richness were Dipsadidae, area, constructed area and edge of the forest (Tropidurus Amphisbaenidae and Teiidae, all with three species hispidus, Amphibaena alba and Boa constrictor). On each. In turn, the families that presented greatest the other hand, the open area and the edge of the forest dominance of individuals, i.e. specimen abundance, had six species in common (Iguana iguana, Ameiva were Tropiduridae (29 specimens) and Gekkonidae (21 ameiva, Salvator merianae, Tropidurus hispidus, specimens) (Table 1). Amphiabaena alba and Boa constrictor), while the The rarefaction curve presented a strong tendency constructed area and the edge of the forest also had six towards stabilization after the 16th sample, thus species in common (Hemidactylus mabouia, Tropidurus indicating that an approximation to the real number hispidus, Amphiabaena alba, Boa constrictor, Chironius of species had been attained (Figure 3). The richness flavolineatus and Micrurus lemniscatus). estimators that were used, i.e. ACE, Chao 1, Jack 1 The microhabitats shared by the greatest number and Bootstrap, respectively estimated 23, 23, 24 and of species were the soil with vegetation and paved 24 species (Figure 4), which were values equal to or ground (Tropidurus hispidus, Amphibaena alba, lower than the number found in the present study (24 Boa constrictor, Erythrolamprus viridis, Chironius spp.). Regarding frequency of occurrence, two species flavolineatus and Micrurus lemniscatus), soils with were considered constant (Hemidactylus mabouia and without vegetation (Ameiva ameiva, Tropidurus and Tropidurus hispidus), three were accessory (Boa hispidus, Salvator merianae, Amphisbaena alba and constrictor, darwinii and Chironius flavolineatus) and soils without vegetation meridionalis) and the remaining species presented and paved ground (Tropidurus hispidus, Amphibaena accidental occurrence (Table 1). alba, Amphisbaena vermicularis and Chironius The species Boa constrictor, Amphisbaena alba, flavolineatus). Amphisbaena polystegum and Phrynops geoffroanus Among the lizard species, Dryadosaura nordestina is were gathered by local collectors and the only specimen endemic to the Atlantic Rainforest of northeastern Brazil. of Caiman latirostris was found on the margin of the lake The distribution of this species does not extend beyond located within the forest. Only Dryadosaura nordestina the coastal forest, with the exception of the occurrence 178 Camila Nascimento de Oliveira et al.

Figure 2. Species of reptiles from the Tejipió forest, municipality of Recife, state of Pernambuco, northeastern Brazil. A) Iguana iguana; B) Norops fuscoauratus; C) Norops ortonii; D) Dryadosaura nordestina; E) Ameiva ameiva; F) Kentropyx calcarata; G) Salvator merianae; H) Tropidurus hispidus; I) Hemidactylus mabouia; J) Phyllopezus lutzae; K) Gymnodactylus darwinii; L) Coleodactylus meridionalis; M) Amphisbaena alba; N) Amphibaena vermicularis; O) Leposternon polystegum; P) Boa constrictor; Q) Chironius flavolineatus; R) Oxybelis aeneus; S) Erythrolamprus viridis; T) Oxyrhopus petolarius; U) Philodryas olfersii; V) Micrurus lemniscatus; W) Micrurus ibiboboca; X) Phrynops geoffroanus. 3hotos by R. Mota (C), C. Castro (P), S. Muniz (G), G. Gomes (K), T. Laurindo (M-N) e M. Freitas (O, R, V, W). Reptiles of an urban Atlantic Rainforest fragment in the state of Pernambuco, Brazil 179

Table 1. Reptile species recorded during the months from October 2011 to April 2012 in the Tejipió forest. Habitat: 1. Open area, 2. Forest area, 3. Constructed area, 4. Lake; 5. Edge of the forest; Microhabitat: 1. Leaf litter, 2. Ground with no vegetation, 3. Ground with vegetation, 4. Tree trunk, 5. Palm stem, 6. Palm leaf sheath, 7. Dry branch on the ground, 8. Fallen tree trunk, 9. Bush branch, 10. Wall, 11. Paved ground (constructed); Form of recording: a. Pitfall trap, b. Visual identification, c. Manual capture, d. Traces, e. Accidental encounter, f. Gathered by third parties, g. Dead animal; Frequency of occurrence (FO): I. Accidental, II. Accessory, III. Constant. ¹Oliveira and Moura, 2013; ² Identified by means of photographs; ³ deposited in collection.

Habitat Microhabitat Form of FO Number of recording specimens LACERTILIA Gekkonidae Hemidactylus mabouia (Moreau de Jonnès, 1818) 3, 5 4, 5, 10, 11 b, c, e III 21 Gymnophthalmidae Dryadosaura nordestina Rodrigues, Freire, Pellegrino & 2 - a I 5 Sites Jr., 2005 Cercosaura ocellata Wagler, 1830¹ 1 Iguanidae Iguana iguana (Linnaeus, 1758) 1, 5 2, 4 b, f I 3 Phyllodactylidae Phyllopezus lutzae (Loveridge, 1941) 2, 5 6, 7 b, c I 2 Gymnodactylus darwinii (Gray, 1845) 2 1 a, c II 7 Dactyloidae Norops fuscoauratus (D'Orbigny, 1837) 2 1, 4, 9 b, c I 5 Norops ortonii (Cope, 1868)² 1 Sphaerodactylidae Coleodactylus meridionalis (Boulenger, 1888) 1, 2 1, 3 a, b, c II 9 Teiidae Ameiva ameiva (Linnaeus, 1758) 1, 5 2, 3 a, b I 4 Kentropyx calcarata Spix, 1825 2 - a I 5 Salvator merianae Duméril & Bibron, 1839 1, 2, 5 2, 3 b, d, f I 4 Tropiduridae Tropidurus hispidus (Spix, 1825) 1, 3, 5 2, 3, 4, 5, 8, 10, b, c, e III 29 11 AMPHISBAENAS Amphisbaenidae Amphisbaena alba Linnaeus, 1758 1, 3, 5 2, 3, 11 e, f I 4 Leposternon polystegum (Duméril, 1851) 3 3 f I 1 Amphisbaena vermicularis Wagler, 1824 1, 2 2, 11 e, f, g I 3 OPHIDIA Boidae Boa constrictor Linnaeus, 1758 1, 3, 5 3, 11 f, g II 10 Eunectes murinus (Linnaeus, 1758)² 1 Colubridae Chironius flavolineatus (Jan, 1863) 2, 3, 5 2, 3, 9, 11 b, c, e I 5 Oxybelis aeneus (Wagler, 1824) - - c, f I 2 Dipsadidae Erythrolamprus viridis Günther, 1862 1, 2, 3 1, 3, 11 c, f, g I 4 Oxyrhopus petolarius (Linnaeus, 1758) - - f I 1 Philodryas olfersii (Lichtenstein, 1823) - - b, e. f I 4 Pseudoboa nigra 1 (Duméril, Bibron e Duméril, 1854)³ Elapidae Micrurus ibiboboca (Merrem, 1820) 2, 3 1, 11 e, f I 2 Micrurus lemniscatus (Linnaeus, 1758) 3, 5 3, 11 f I 2 TESTUDINES Chelidae Phrynops geoffroanus (Schweigger, 1812) 4 - f - 2 CROCODYLIA Alligatoridae Caiman latirostris (Daudin, 1802) 4 - g - 1 A total of 15 families and 27 species 180 Camila Nascimento de Oliveira et al.

as the Mata do Buraquinho Permanent Protection Area in the state of Paraíba (37 spp.) (Santana et al., 2008), although this has a larger area. On the other hand, the Lagoa Encantada and Rio Almada Permanent Preservation Area, in the state of Bahia, presented only 17 spp. (Dias et al., 2014), probably due to a shorter sampling period. In the present study, the Amphisbaenidae family presented greater richness than other Atlantic Rainforest remnants (Araújo et al., 2010; Vrcibradic et al., 2011; Figure 3. Rarefaction curves representing the accumulated Morato et al., 2011; Moura et al., 2012). The same richness of the species of reptiles in the Tejipió forest recorded was also observed for the Teiidae family (Forlani et between October 2011 and April 2012. The continuous line al., 2010; Dias et al., 2014), although higher richness corresponds to the mean of each sampling period, randomized was found in Mata do Junco (Morato et al., 2011). The 500 times, and the dotted lines represent the associated Dipsadidae family frequently presented the greatest standard deviation. number of species (Forlani et al., 2010; Morato et al., 2011; Vcbradic et al., 2011; Dias et al., 2014), which was expected since this is the family with the greatest number of reptile species in Brazil (246 spp.) (Bérnils and Costa, 2014). in the Brejos de Altitude (northeastern upland forest) The two dominant species in the Tejipió forest were (Rodrigues et al., 2005; Delfino and Soeiro, 2012; Garda Tropidurus hispidus (n = 29) and Hemidactylus mabouia et al., 2014). In turn, Gymnodactylus darwinii presented (n = 21). Tropidurus hispidus is considered to be a broader geographical distribution, since it is endemic to habitat generalist (Van Sluys et al., 2004; Miranda et the Atlantic Rainforest extending from the state of São al., 2012), and is dominant in other fragments (Sales et Paulo to the northeast of the state of Bahia (Vanzolini, al., 2009). Moreover, this species prefers areas with sun 1953), with more recent expansion northwards to other exposure (Santana et al., 2014) and frequently occupies states, as far as the state of Rio Grande do Norte (Freire, anthropic areas (Sales et al., 2009). 1998; Santana et al., 2008; Moura et al., 2011). The lizard H. mabouia is an introduced species in Brazil. Other Atlantic Rainforest remnants in northeastern It is highly adapted to different phytophysiognomies and Brazil present similar richness to the found in our study, can be found in the Amazon Rainforest (Ferrão et al., such as the Mata do Junco Wildlife Refuge in the state 2012), Caatinga, Cerrado, Brejos de Altitude (Borges- of Sergipe (26 spp.) (Morato et al., 2011). However, Leite et al., 2014), Atlantic Rainforest (Santana et al., there are fragments with higher reptile richness, such 2008), Chaco (Souza et al., 2010) and Pampas (Souza Filho and Verrastro, 2012). The greatest number of H. mabouia individuals occurred in the constructed area, thus corroborating other studies, in which the species was found occupying human edifications (Ferrão et al., 2012) and therefore showing a certain affinity towards anthropic environments. Teixeira (2002) suggested that increasing levels of fragment degradation could result in a loss of living area for the lizard Gymnodactylus darwinii, which would lose out in competition with H. mabouia. Regarding the frequency of occurrence, Tropidurus hispidus and Hemidactylus mabouia presented constant frequency during the sampling, probably because these species have continuous reproduction, as observed by Figure 4. Richness estimators based on the abundance of Anjos and Rocha (2008) for H. mabouia and by Santana reptile species recorded in the Tejipió forest between October et al. (2014) for T. hispidus, who found the species 2011 and April 2012. throughout the year. These species are generalists and Reptiles of an urban Atlantic Rainforest fragment in the state of Pernambuco, Brazil 181 are highly adaptable to anthropic and peri-anthropic exist at the study site. Santana et al. (2008) observed environments (Santana et al., 2008; Sales et al., 2009; A. alba, B. constrictor and M. ibiboboca on the forest Miranda et al., 2012; Santana et al., 2014), such as litter, which was similar to the results obtained in construction sites and the edge of forests, as observed in the present study, although with a lower number of the present study in which the forest fragment is located occupied microhabitats. The lizard Phyllopezus lutzae in an urban area with several human constructions in is considered to be bromelicolous (Loveridge, 1941), the proximities. and this species can occupy other microhabitats, such Among the 22 species that were evaluated regarding as palm tree leaves accumulated on the ground, bush their frequency of occurrence, 77.3% were species with vegetation and rocky outcrops (Vanzolini and Gomes, only accidental occurrence. Among these species, some 1979). In the present study, this species presented low present fossorial and semifossorial habits: Amphisbaena occurrence, with only two specimens. However, they spp. (Condez et al., 2009; Salles and Silva-Soares, 2010) were not found on bromeliads, since these did not occur and Micrurus ibiboboca (Rocha and Prudente, 2010); in the study site, but on palm sheaths and on sticks on some are arboreal: Iguana iguana (Vitt et al., 2008) and the ground. Oxybelis aeneus (Santana et al., 2008); and some are The Tejipió forest needs greater investments towards medium to large in size: Ameiva ameiva and Salvator biodiversity conservation, since human communities merianae (Silva and Araújo, 2008). Thus, recording and can be found surrounding the area. People enter the catching these individuals is difficult. Caiman latirostris forest and occasionally alter the environment negatively, and Phrynops geoffroanus were occasionally reported by removing soil, creating water channels, forest and, since no appropriate methodology for sampling fires and littering. The work developed by the Fourth these groups was applied, these species were not Communications Battalion of the has included in the analyses on abundance and frequency been very important for maintenance and restoration of of occurrence. the rainforest (Guimarães et al., 2012). Nonetheless, a The greatest number of species was recorded on considerable amount of garbage has accumulated in the the edge of the forest, probably because these species battalion’s area, which originated from training events occupy open areas: T. hispidus and A. ameiva (Morato or even simply from dumping within the forest. Thus, et al., 2011); or both open and forested areas: S. environmental intervention is necessary in order to merianae (Araújo et al., 2010; Morato et al., 2011; educate both the inhabitants and the military personnel, Moura et al., 2012), Kentropyx calcarata and Micrurus regarding the importance of maintaining this fragment ibiboboca (Morato et al., 2011); or occur in urban areas: of the Atlantic Rainforest, which has the potential for M. lemniscatus (Costa et al., 2010). Unlike what was maintaining the reptile fauna. These fragments are observed by Araújo et al. 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Appendix 1.

Dryadosaura nordestina – CHP-UFRPE 0916, 1012; Norops fuscoauratuus – CHP-UFRPE 1013; Philodryas olfersii – CHP-UFRPE 1018, 1065; Micrurus lemniscatus – CHP- UFRPE 1020; Erythrolamprus viridis – CHP-UFRPE 1035, 1064; Oxybelis aeneus – CHP-UFRPE 1063; Pseudoboa nigra - CHUFPE 109.

Accepted by Robson Ávila