Checklist of reptiles (Testudines, Squamata)

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
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.
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 (ÁvilaPires, 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
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 76803260 Porto Velho, Rondônia, Brazil.
E-mail: [email protected]
*Corresponding author: [email protected]
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)
474
Miquéias Ferrão et al.
Figure 1. Location of the municipality of Alto Alegre dos Parecis (triangle), state of Rondônia, Brazil.
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 Methods
The 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 toApril 2007, summing up 60 pitalls.day.
For identifying reptiles we used keys and descriptions by Peters
and Orejas-Miranda (1970), Cunha and Nascimento (1993), SilvaJr (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),
Checklist of reptiles from Alto Alegre dos Parecis
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
475
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; SilvaJr. 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).
476
Miquéias Ferrão et al.
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).
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Checklist of reptiles from Alto Alegre dos Parecis
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.
ORDER/FAMILY
SPECIES
HABITAT
TESTUDINES
Chelidae
1
Platemys platycephala (Schneider, 1792)
WE
Anolis fuscoauratus D´Orbigny, 1837
FO
Anolis ortonii Cope, 1869
FO
Anolis transversalis Duméril, 1851
FO
Uranoscodon superciliosus (Linnaeus, 1758)
FO
Hemidactylus mabouia (Moreau de Jonnès, 1818)
HE
Chatogekko amazonicus (Andersson, 1918)
FO
Gonatodes hasemani Griffin, 1917
FO
Gonatodes humeralis (Guichenot, 1855)
FO
Ameiva ameiva (Linnaeus, 1758)
PA; HE
Cercosaura eigenmani (Griffin, 1917)
FO
Mabuya nigropunctata (Spix, 1825)
FO
Anilius scytale (Linnaeus, 1758)
WE
Boa constrictor Linnaeus, 1758
FO
Corallus hortulanus (Linnaeus, 1758)
FO; NF
Eunectes murinus (Linnaeus, 1758)
WE
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
SQUAMATA
Polychrotidae
Tropiduridae
Gekkonidae
Sphaerodactylidae
Teiidae
Gymnophthalmidae
Scincidae
Anillidae
1
Boidae
2
Colubridae
2
Helicops angulatus (Linnaeus, 1758)
WE
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)
NF
Micrurus lemniscatus (Linnaeus, 1758)
FO
Micrurus surinamensis (Cuvier, 1817)
WE
Bothrops atrox (Linnaeus, 1758)
FO; NF
Lachesis muta (Linnaeus, 1766)
FO
Elapidae
1
Viperidae
478
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 AvilaPires 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 GuajaráMirim 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
Miquéias Ferrão et al.
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 Grosso, 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), Imantodes cenchoa (UFMT 7027), Leptodeira annulata (UFMT 7025,
UFMT 7100), Leptophis ahaetulla (UFMT 7019), Mabuya nigropunctata (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), Rhinobothryum lentiginosum (UFMT 6943), Uranoscodon superciliosus (UFMT 6912, UFMT 6913), Xenodon severus (UFMT 7097,
UFMT 7098), Xenopholis scalaris (UFMT 7023).
Accepted by Mirco Solé