checklist of reptiles (testudines, squamata) from alto

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Introduction Approximately 732 reptile species occur in Brazil (Bérnils and Costa, 2011), of which 273 species are recorded from Amazonia, including 16 chelonians, four crocodilians, 104 snakes, and 149 lizards (Ávila- Pires, Hoogmoed and Vitt, 2007). Due to the inventories carried out in new areas and to the description of new species in the past few years, the number of reptile species that occur in Amazonia has been constantly increasing (França and Venancio, 2010). Among studies on reptile assemblages in the state of Rondônia stand out those carried out along the road BR-364 (Vanzolini, 1986; Nascimento, Avila-Pires and Cunha, 1988) and in the municipalities of Espigão do Oeste (Bernarde and Abe, 2006; Macedo, Bernarde and Abe, 2008), Cacoal (Turci and Bernarde, 2008), Guajará-Mirim (Avila-Pires et al., 2009), and Candeias do Jamari (Silva-Jr, 1993). Rapid biological inventories were carried in Pimenta Bueno (Yuki, Galatti and Rocha, 1999) and Costa Marques (Brandão, 2002). Gainsbury and Colli (2003) studied the ecology of lizard assemblages of Cerrado enclaves in Guajará-Mirim, Pimenta Bueno, and Vilhena. The feeding habits of snakes in Espigão do Oeste were assessed by Bernarde and Abe (2010). Despite considerable number of studies carried out in the state of Rondônia, there are still many knowledge gaps regarding reptile richness and diversity in several regions, mainly in the regions more distant from the area of influence of the road BR-364. Deforestation in Brazilian Amazonia has been continuously increasing since 1991, varying in time according to changes in economical pressures (Fearnside, 2001; 2006). Causes of accelerated deforestation in the Amazon are several and include expansion of cattle farming, logging, and agriculture (Fearnside, 2001). In 2003, deforested areas covered 16% of Amazonia and were more expressive in the ‘deforestation arch’, a large region that extends from Rondônia to Maranhão (Ferreira, Venticinque and Almeida, 2005). Rondônia is one of the Brazilian states that deforest the most (Ferreira, Venticinque and Almeida, 2005); small farmers are one of the main agents of deforestation (Fearnside, 2006). Because of the intensive deforestation that Rondônia undergoes, the state has been suggested as a region of high interest for herpetofauna studies (Vogt, Moreira and Duarte, 2001). These studies are of fundamental importance, and may help in the decision making related to conservation (e.g. creation of reserves). The old Brazilian Forest Code (Federal Law nº 4.771, 15th September 1965) was known to be restrictive and conservative concerning the conservation and maintenance of the environment. However, a new Brazilian Forest Code (Federal Law nº 12.651, 25th may 2012) was approved in 2012. Several are the changes in the new code, among them: (1) Herpetology Notes, volume 5: 473-480 (2012) (published online on 12 October 2012) Checklist of reptiles (Testudines, Squamata) from Alto Alegre dos Parecis, southwestern Amazonia, Brazil Miquéias Ferrão 1,* , José Alexandre Soares Rodrigues Filho 2 and Mitzi Oliveira da Silva 3 1 Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade, Instituto de Biociências, Universidade Federal do Mato Grosso, Av. Fernando Correa 2367, CEP 78060-900 Cuiabá, Mato Grosso, Brazil. 2 Faculdade da Amazônia – FAMA, Rua 743 2043 - CEP 78995-000 Vilhena, Rondônia, Brazil. E-mail: [email protected] 3 Instituto Chico Mendes de Conservação da Biodiversidade, Avenida Lauro Sodré, 6500 Bairro Aeroporto, CEP 76803- 260 Porto Velho, Rondônia, Brazil. E-mail: [email protected] *Corresponding author: [email protected] Abstract. We present a list of reptiles from Alto Alegre dos Parecis, state of Rondônia, northern Brazil, within southwestern Amazonia, and discuss possible effects of the approval of a new Brazilian Forest Code on the local reptile fauna. Specimens were collected in 2007 through time-constrained search, occasional encounters, collection by third parties, and pitfall traps. We recorded 38 reptile species in the study area, distributed into two orders (Testudines, and Squamata) and 13 families: Chelidae (one), Polychrotidae (three), Tropiduridae (one), Gekkonidae (one), Sphaerodactylidae (three), Teiidae (one), Gymnophthalmidae (one), Scincidae (one), Anillidae (one), Boidae (three), Colubridae (18), Elapidae (two), and Viperidae (two). Records of the snakes Dipsas variegata and Pseudoboa nigra represent the third and the second formal records of these species, respectively, for the state of Rondônia. Keywords. reptiles, Amazon, Brazilian Forest Code, conservation.

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IntroductionApproximately 732 reptile species occur in Brazil

(Bérnils and Costa, 2011), of which 273 species are recorded from Amazonia, including 16 chelonians, four crocodilians, 104 snakes, and 149 lizards (Ávila-Pires, Hoogmoed and Vitt, 2007). Due to the inventories carried out in new areas and to the description of new species in the past few years, the number of reptile species that occur in Amazonia has been constantly increasing (França and Venancio, 2010).

Among studies on reptile assemblages in the state of Rondônia stand out those carried out along the road BR-364 (Vanzolini, 1986; Nascimento, Avila-Pires and Cunha, 1988) and in the municipalities of Espigão do Oeste (Bernarde and Abe, 2006; Macedo, Bernarde and Abe, 2008), Cacoal (Turci and Bernarde, 2008), Guajará-Mirim (Avila-Pires et al., 2009), and Candeias do Jamari (Silva-Jr, 1993). Rapid biological inventories were carried in Pimenta Bueno (Yuki, Galatti and Rocha, 1999) and Costa Marques (Brandão, 2002). Gainsbury and Colli (2003) studied the ecology of lizard

assemblages of Cerrado enclaves in Guajará-Mirim, Pimenta Bueno, and Vilhena. The feeding habits of snakes in Espigão do Oeste were assessed by Bernarde and Abe (2010). Despite considerable number of studies carried out in the state of Rondônia, there are still many knowledge gaps regarding reptile richness and diversity in several regions, mainly in the regions more distant from the area of influence of the road BR-364.

Deforestation in Brazilian Amazonia has been continuously increasing since 1991, varying in time according to changes in economical pressures (Fearnside, 2001; 2006). Causes of accelerated deforestation in the Amazon are several and include expansion of cattle farming, logging, and agriculture (Fearnside, 2001). In 2003, deforested areas covered 16% of Amazonia and were more expressive in the ‘deforestation arch’, a large region that extends from Rondônia to Maranhão (Ferreira, Venticinque and Almeida, 2005).

Rondônia is one of the Brazilian states that deforest the most (Ferreira, Venticinque and Almeida, 2005); small farmers are one of the main agents of deforestation (Fearnside, 2006). Because of the intensive deforestation that Rondônia undergoes, the state has been suggested as a region of high interest for herpetofauna studies (Vogt, Moreira and Duarte, 2001). These studies are of fundamental importance, and may help in the decision making related to conservation (e.g. creation of reserves).

The old Brazilian Forest Code (Federal Law nº 4.771, 15th September 1965) was known to be restrictive and conservative concerning the conservation and maintenance of the environment. However, a new Brazilian Forest Code (Federal Law nº 12.651, 25th may 2012) was approved in 2012. Several are the changes in the new code, among them: (1)

Herpetology Notes, volume 5: 473-480 (2012) (published online on 12 October 2012)

Checklist of reptiles (Testudines, Squamata) from Alto Alegre dos Parecis, southwestern Amazonia, Brazil

Miquéias Ferrão1,*, José Alexandre Soares Rodrigues Filho2 and Mitzi Oliveira da Silva3

1 Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade, Instituto de Biociências, Universidade Federal do Mato Grosso, Av. Fernando Correa 2367, CEP 78060-900 Cuiabá, Mato Grosso, Brazil.

2 Faculdade da Amazônia – FAMA, Rua 743 2043 - CEP 78995-000 Vilhena, Rondônia, Brazil. E-mail: [email protected]

3 Instituto Chico Mendes de Conservação da Biodiversidade, Avenida Lauro Sodré, 6500 Bairro Aeroporto, CEP 76803-260 Porto Velho, Rondônia, Brazil. E-mail: [email protected]

*Corresponding author: [email protected]

Abstract. We present a list of reptiles from Alto Alegre dos Parecis, state of Rondônia, northern Brazil, within southwestern Amazonia, and discuss possible effects of the approval of a new Brazilian Forest Code on the local reptile fauna. Specimens were collected in 2007 through time-constrained search, occasional encounters, collection by third parties, and pitfall traps. We recorded 38 reptile species in the study area, distributed into two orders (Testudines, and Squamata) and 13 families: Chelidae (one), Polychrotidae (three), Tropiduridae (one), Gekkonidae (one), Sphaerodactylidae (three), Teiidae (one), Gymnophthalmidae (one), Scincidae (one), Anillidae (one), Boidae (three), Colubridae (18), Elapidae (two), and Viperidae (two). Records of the snakes Dipsas variegata and Pseudoboa nigra represent the third and the second formal records of these species, respectively, for the state of Rondônia.

Keywords. reptiles, Amazon, Brazilian Forest Code, conservation.

Miquéias Ferrão et al. 474

possibility of reduction of the legal reserve (LR) in many areas of Amazonia from 80% to 50%; (2) permission to reforest LR areas with exotic species.

Due to the intensive deforestation in Rondônia and the lack of knowledge regarding composition of the reptile fauna in several regions of this state, we present here the species list of a locality in the municipality of Alto Alegre dos Parecis, Brazil and briefly discuss possible effects of the approval of the new forest code on the local reptile assemblage.

Materials and MethodsThe study was carried out in Santa Rita Farm (12º07’ S, 61º51’

W), located in the municipality of Alto Alegre dos Parecis, state of Rondônia, Brazil, southwestern Amazon (Fig. 1). The region of Alto Alegre dos Parecis comprises several kinds of vegetation, such as submontane open rainforest, open lowland rainforest, open savanna forest, submontane semideciduous seasonal forest, as well as areas of ecological tension of savanna/rainforest. The vegetation of the Santa Rita Farm consists of secondary rainforest and deforested area (pasture), forming a fragmented landscape. It is under the influence of the mountain range Serra dos Parecis in the state of Mato Grosso. Annual rainfall in the municipality varies annually between 1,400 mm and 1,800 mm. Dry season occurs from June to August, rainy season

from December to May. Average air temperature is 25 °C.Reptile sampling was carried out between January 2007 and

May 2007, with sporadic collections between June 2007 and December 2007. Specimens were captured through four methods: (1) time-constrained search (Campbell and Christman, 1982); (2) occasional encounters (Martins and Oliveira, 1998); (3) collection by third parties (see Cunha and Nascimento, 1993); and (4) pitfall traps with drift fences (Campbell and Christman, 1982; Cechin and Martins, 2000). Pitfalls were divided into four groups, three in secondary forest and one in deforested area (pasture). Each group containing four recipients of 60 L, 10 m apart from each other, arranged in a straight line and united by a plastic canvas of approximately 1 m height. Traps remained opened for three days each month from January to April 2007, summing up 60 pitalls.day.

For identifying reptiles we used keys and descriptions by Peters and Orejas-Miranda (1970), Cunha and Nascimento (1993), Silva-Jr (1993), Ávila-Pires (1995), Roze (1996), and Zaher (1996). Nomenclature of Colubroidea followed Pyron et al. (2011).

Voucher specimens were deposited in the Zoological Collection of Vertebrates of the Federal University of Mato Grosso (Universidade Federal de Mato Grosso – UFMT), Cuiabá, and in Capão da Imbuia Natural History Museum, Curitiba, Paraná, Brazil.

Results and Discussion

We recorded 38 reptile species in Santa Rita Farm, distributed in three orders and 13 families: Chelidae (1),

Figure 1. Location of the municipality of Alto Alegre dos Parecis (triangle), state of Rondônia, Brazil.

Checklist of reptiles from Alto Alegre dos Parecis 475

Polychrotidae (3), Tropiduridae (1), Gekkonidae (1), Sphaerodactylidae (3), Teiidae (1), Gymnophthalmidae (1), Scincidae (1), Anillidae (1), Boidae (3), Colubridae (18), Elapidae (2), and Viperidae (2).

The number of species recorded exclusively in forest environments (secondary forest and water environment in forest) and anthropic environments (human edification, pasture and water environment in deforested

area) accounted for approximately 61% and 16% of total species sampled, respectively (Tab. 1).

Based on the current knowledge of the geographic distribution of reptiles in Rondônia (Vanzolini, 1986; Nascimento, Ávila-Pires and Cunha, 1988; Silva-Jr. 1993; Yuki, Galatti and Rocha, 1999; Brandão, 2002; Bernarde and Abe 2006; Turci and Bernarde, 2008; Avila-Pires et al., 2009), we expected the sub-

Figure 2. Lizard species recorded from Santa Rita Farm, Alto Alegre dos Parecis, state of Rondônia, southwestern Amazonia, Brazil. A- Gonatodes humeralis; B- Chatogekko amazonicus; C- Anolis ortonii; D- Uranoscodon superciliosus; E- Cercosaura eigenmani (male); F- Cercosaura eigenmani (female). Photos: Miquéias Ferrão (A, B, C, D); Adriano M. Silva (E, F).

Miquéias Ferrão et al. 476

Figure 3. Snake species recorded in Santa Rita Farm, Alto Alegre dos Parecis, state of Rondônia, southwestern Amazonia, Brazil. A- Xenodon severus (juvenile); B- Liophis reginae; C- Leptodeira annulata; D- Mastigodryas boddaerti (juvenile); E- Leptophis ahaetulla; F- Corallus hortulanus; G- Philodryas viridissima; H- Boa constrictor. Photos: Miquéias Ferrão (A, B, C, D, H); Aldes Lamounier (E); Adriano M. Silva (F, G).

Checklist of reptiles from Alto Alegre dos Parecis 477

ORDER/FAMILY SPECIES HABITAT

TESTUDINESChelidae

Platemys platycephala (Schneider, 1792) WE1

SQUAMATA Polychrotidae

Anolis fuscoauratus D´Orbigny, 1837 FO

Anolis ortonii Cope, 1869 FO

Anolis transversalis Duméril, 1851 FOTropiduridae

Uranoscodon superciliosus (Linnaeus, 1758) FOGekkonidae

Hemidactylus mabouia (Moreau de Jonnès, 1818) HESphaerodactylidae

Chatogekko amazonicus (Andersson, 1918) FO

Gonatodes hasemani Griffin, 1917 FO

Gonatodes humeralis (Guichenot, 1855) FOTeiidae

Ameiva ameiva (Linnaeus, 1758) PA; HE Gymnophthalmidae

Cercosaura eigenmani (Griffin, 1917) FOScincidae

Mabuya nigropunctata (Spix, 1825) FOAnillidae

Anilius scytale (Linnaeus, 1758) WE1

Boidae Boa constrictor Linnaeus, 1758 FO

Corallus hortulanus (Linnaeus, 1758) FO; NF

Eunectes murinus (Linnaeus, 1758) WE2

Colubridae Clelia plumbea (Wied, 1820) PA

Dipsas catesbyi (Sentzen, 1796) FO

Dipsas indica Laurenti, 1768 FO

Dipsas variegata (Duméril, Bibron & Duméril, 1854) NF

Drymarchon corais (Boie, 1827) PA

Helicops angulatus (Linnaeus, 1758) WE2

Imantodes cenchoa (Linnaeus, 1758) FO

Leptodeira annulata (Linnaeus, 1758) FO; NF

Leptophis ahaetulla (Linnaeus, 1758) FO

Liophis reginae (Linnaeus, 1758) FO

Mastigodryas boddaerti (Sentzen, 1796) FO; PA

Oxybelis aeneus (Wagler, 1824) FO

Oxyrhopus melanogenys (Tschudi, 1845) FO

Philodryas viridissima (Linnaeus, 1758) NF

Pseudoboa nigra (Duméril, Bibron & Duméril, 1854) NF; PA

Rhinobothryum lentiginosum (Scopoli, 1785) FO

Xenodon severus (Linnaeus, 1758) FO; NF

Xenopholis scalaris (Wucherer, 1861) NFElapidae

Micrurus lemniscatus (Linnaeus, 1758) FO

Micrurus surinamensis (Cuvier, 1817) WE1

Viperidae Bothrops atrox (Linnaeus, 1758) FO; NF

Lachesis muta (Linnaeus, 1766) FO

Table 1. Species of reptiles recorded in Santa Rita Farm, Alto Alegre dos Parecis, state of Rondônia, southwestern Amazonia, Brazil. Habitat FO = secondary forest; HE = human edification; NF = edge secondary forest; PA = deforested area (pasture); WE1 = water environment in forest; WE2 = water environment in deforested area.

arboreal snakes Chironius exoletus, C. scurrulus, Spilotes pullatus, and Philodryas olfersii, the fossorial/cryptozoic snakes Atractus albuquerquei, Typhlops reticulatus, and Tantilla melanocephala, and the terricolous snake Epicrates cenchria in Alto Alegre dos Parecis, which were not sampled. The lizards Iguana iguana, Anolis punctatus, Plica spp., Tupinambis sp., Cercosaura ocellata, Leposoma spp. and the chelonian Chelonoidis denticulata were expected to occur in the region, since local residents reported observing these species. Further reptile inventories in the region of Alto Alegre dos Parecis with larger sampling effort and the use of additional capture methods (e.g., entomological nets and funnel-traps) will probably reveal several other species. Additionally, new sampling in areas of primary forests should reveal species not registered in this study, once primary environments have a greater diversity of reptile species (Gardner et al., 2007).

Dipsas variegata has been recorded in the Guyana, French Guiana, Suriname, Venezuela, Peru, Colombia, Ecuador, Brazil (Cunha and Nascimento, 1993), and Bolívia (Harvey and Embert, 2008). According to Harvey and Embert (2008), Dipsas variegata commonly occurs only in the Guianas, but isolated populations may occur all over the Amazon. One of these populations was found in Rondônia. Harvey and Embert (2008) recognize as Dipsas variegata the specimen captured in Guajará-Mirim State Park, mentioned later by Avila-Pires et al. (2009). Passos, Fernandes and Caramaschi (2004) reported one specimen in the municipality of Porto Velho. The specimen collected in the present study is the third record for the state of Rondônia and is approximately 400 and 435 km away from Guajará-Mirim and Porto Velho, respectively, where the two previous records were made. According to Harvey and Embert (2008), populations of Dipsas variegata occur together with populations of Dipsas indica and Dipsas catesbyi, as observed in Alto Alegre dos Parecis.

In Rondônia, Pseudoboa nigra was recorded in Guajará-Mirim by França, Mesquita and Colli (2006), in a checklist of the snakes of Amazonian savannas. Two individuals were captured in Santa Rita Farm, which is located approximately 400 km away from the locality where the species was sampled for the first time, representing the second record of Pseudoboa nigra for the state of Rondônia.

Alto Alegre dos Parecis had until 2006 a total of 28.36% of its native areas deforested (Secretaria de estado do Desenvolvimento Ambiental – Rondônia, 2009). Due to the intensive deforestation in this municipality, many

areas need to be reforested. The new Brazilian Forest Code allows these areas could be reforested with exotic species (e.g., Eucalyptus spp. and Pinus spp.). Altered environments with exotic vegetation sustain a lower reptile diversity than natural environments (Marques and Sazima, 2004; Macedo, Bernarde and Abe, 2008; Gardner et al., 2007), dominated by generalist species with widespread distributions. According to Marques et al. (2010), large part of Brazilian reptiles cannot survive in altered environments by human activities (including exotic species forests). Recolonization of areas reforested with exotic species by forest reptiles, mainly the ones of arboreal or semi-arboreal habits (e.g. Anolis spp., Corallus hortulanus, Dipsas spp., Imantodes cenchoa, Leptodeira annulata, Philodryas viridissima, and Oxybelis aeneus) would be hindered.

The exigencies of the new Brazilian Forest Code are excessively liberal and abusive, and are reproachable in terms of generalization (Ab’Saber, 2010). Represent an immensurable risk to the biological and genetic heritage (Metzger, 2010). Many changes should be carried out in the new Brazilian Forest Code so that it meets the interests of conservation and agribusiness in a sustainable way, without threatening the rich Brazilian biodiversity.

Acknowledgements. We thank José Alexandre Rodrigues Soares and Ivone Maria Posse for allowing us to collect in Santa Rita Farm. Francisca Cândida de Assis gave us logistic support. Christine Strüssmann made the first reading of this manuscript and gave us invaluable suggestions. Lilian Cristina Macedo, Weslei Valteran dos Santos, Adriano Martins and Valquiria Selhorst helped us in the fieldwork. Júlio César de Moura Leite identified the specimens of Pseudoboa nigra and Philodryas viridissima. Pedro Ivo Simões made the map of the study area. CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) granted MF a scholarship.

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Appendix 1. Voucher list (UFMT – Coleção de Vertebrados da Universidade Federal de Mato Grosso, Cuiabá, state of Mato Gros-so, Brazil; MHNCI – Museu de História Natural Capão da Imbuia, Curitiba, State of Paraná, Brazil).Ameiva ameiva (UFMT 6911, UFMT 6925), Anilius scytale (UFMT 6939), Anolis fuscoauratus (UFMT 6920, UFMT 6921, UFMT 6923, UFMT 6924), Anolis transversalis (UFMT 6914), Cercosaura eigenmani (UFMT 6934, UFMT 6935, UFMT 6936), Clelia plumbea (UFMT 7099), Chatogekko amazonicus (UFMT 6931, UFMT 6932, UFMT 6933), Corallus hortulanus (UFMT 7026, UFMT 7044, UFMT 7096), Dipsas catesbyi (UFMT 6938), Dipsas indica (UFMT 7022), Dipsas variegata (UFMT 6937), Gonatodes hasemani (UFMT 6915, UFMT 6916, UFMT 6917), Gonatodes humeralis (UFMT 6918), Helicops angulatus (UFMT 7047, UFMT 7092), Hemidactylus mabouia (UFMT 6922), Iman-todes cenchoa (UFMT 7027), Leptodeira annulata (UFMT 7025, UFMT 7100), Leptophis ahaetulla (UFMT 7019), Mabuya nigro-punctata (UFMT 6919), Mastigodryas boddaerti (UFMT 6940, UFMT 7045, UFMT 7046), Liophis reginae (UFMT 7018, UFMT 7021, UFMT 7028, UFMT 7093), Micrurus lemniscatus (UFMT 6944), Micrurus surinamensis (UFMT 6942), Oxybelis aeneus (UFMT 6941), Oxyrhopus melanogenys (UFMT 7020, UFMT 7024, UFMT 7094, UFMT 7095), Philodryas viridissima (MHNCI 12783), Pseudoboa nigra (MHNCI 12781, MHNCI 12782), Rhi-nobothryum lentiginosum (UFMT 6943), Uranoscodon supercili-osus (UFMT 6912, UFMT 6913), Xenodon severus (UFMT 7097, UFMT 7098), Xenopholis scalaris (UFMT 7023).

Miquéias Ferrão et al. 480

Accepted by Mirco Solé