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Papéis Avulsos de Zoologia

Print version ISSN 0031-1049On-line version ISSN 1807-0205

Pap. Avulsos Zool. vol.57 no.28 São Paulo  2017

http://dx.doi.org/10.11606/0031-1049.2017.57.28 

Article

REPTILE SPECIES COMPOSITION IN THE MIDDLE GURGUÉIA AND COMPARISON WITH INVENTORIES IN THE EASTERN PARNAÍBA RIVER BASIN, STATE OF PIAUÍ, BRAZIL

CLÁUDIA RENATA MADELLA-AURICCHIO1 

PAULO AURICCHIO2 

ENIO SARAIVA SOARES3 

1Universidade Federal do Ceará (UFC), Centro de Ciências, Departamento de Biologia, Programa de Pós-Graduação em Ecologia e Recursos Naturais. Rua Campus do Pici, Bloco 906, Pici, CEP 60440-554, Fortaleza, CE, Brasil. ORCID: 0000-0003-3015-496X. E-mail: clauremade@gmail.com

2Universidade Federal do Piauí (UFPI), Centro de Ciências da Natureza (CCN), Departamento de Biologia. Campus Universitário Ministro Petrônio Portella. Avenida Universitária, Ininga, CEP 64049-550, Teresina, PI, Brasil. ORCID: 0000-0002-7578-1097. E-mail: paulo.auricchio@ufpi.edu.br

3Universidade Federal do Piauí (UFPI), Centro de Ciências da Natureza (CCN), Departamento de Biologia. Campus Universitário Profª Cinobelina Elvas. BR 135, km 3, Planalto Horizonte, CEP 64900-000, Bom Jesus, PI, Brasil. E-mail: eniomyrddin@hotmail.com

ABSTRACT

The reptile diversity of the Middle Gurguéia River Basin in southern Piauí, Brazil, is little known. The rapid expansion of agriculture in the region is converting the Cerrado and Caatinga into large farming areas, which threatens biodiversity and hastens its loss. In this study, 68 specimens of reptiles from a university collection were examined, comprising 29 species: ten lizards, one amphisbaenian, 15 snakes, two turtles and one crocodilian. They were collected from five locations in the Middle Gurguéia Basin, a region not previously evaluated for reptiles. The most abundant species is a member of Tropidurus. Comparison with eight other areas in the eastern Parnaíba Basin indicated that the diversity of reptiles in the Middle Gurguéia is similar to that in other Caatinga-Cerrado ecotone areas. The reptile assemblage in the eastern Parnaíba Basin comprises 100 species of reptiles: 39 lizards, five amphisbaenians, 50 snakes, four chelonians and two crocodilians. This study expanded the known distributions of some reptiles and recorded the first occurrence of Helicops leopardinus (Schlegel, 1837) for Piauí. A cluster analysis showed that the reptile composition concords with the habitat where species were found, i.e. Cerrado, Caatinga or ecotone. Studies that associate habitat structure with each species are essential to propose efficient strategies for reptile management and conservation for the entire Parnaíba River Basin, mostly in areas that are not yet protected.

KEY-WORDS: Reptilia; Helicops; Ecotone; Cerrado; Caatinga

RESUMO

Pouco se sabe sobre a diversidade de répteis na bacia do Médio rio Gurguéia, sul do Piauí, Brasil. A rápida expansão da agricultura na região que converte o Cerrado e a Caatinga em grandes áreas de plantio, ameaça a biodiversidade e acelera sua perda. Neste estudo foram examinados 68 espécimes de répteis de uma coleção universitária que compreende 29 espécies: dez lagartos, uma anfisbena, 15 serpentes, duas tartarugas e um crocodiliano, de cinco localidades do Médio Gurguéia, uma região até então não avaliada para esse grupo zoológico. As espécies mais abundantes pertencem ao gênero Tropidurus. Uma análise comparativa com outras oito áreas do leste da bacia do Parnaíba indicou que a diversidade de répteis no Médio Gurgueia é consistente com trabalhos realizados em áreas ecotonais Caatinga-Cerrado. A diversidade de répteis no leste da bacia do Parnaíba compreende 100 espécies de répteis: 39 lagartos, cinco anfisbenas, 50 serpentes, quatro tartarugas e dois crocodilianos. Além disso, este estudo expande a distribuição para os répteis e registra pela primeira vez a ocorrência da serpente Helicops leopardinus (Schlegel, 1837) para o Piauí. A análise de agrupamento mostrou que os répteis possuem identidade com o ambiente em que foram encontrados: Cerrado, Caatinga ou área de ecótono. Desta forma, estudos que associem a estrutura de hábitat com cada espécie são necessários para propor estratégias eficientes de manejo e conservação de répteis para toda a bacia do rio Parnaíba, principalmente em áreas ainda não protegidas.

PALAVRAS-CHAVE: Reptilia; Helicops; Ecótono; Cerrado; Caatinga

INTRODUCTION

Although knowledge of the biodiversity of the Cerrado, Caatinga and ecotone areas has increased, the fauna of these vegetation complexes is still little known and many areas have never been inventoried (Rodrigues, 2005a). Reptilia is a well-understood group, but in the five largest Brazilian collections, reptiles from many key areas and ecosystems are not represented (Rodrigues, 2005b). Except for the well-known Crocodilia, the number of Brazilian reptile species is still underestimated, due to insufficient inventories and the small number of taxonomists (Rodrigues, 2005b).

According to Costa & Bérnils (2015), 773 reptile species can be found in Brazil: six crocodilians, 36 chelonians, 73 amphisbaenians, 266 lizards and 392 snakes. The 185 species known from the Cerrado include five crocodilians, ten turtles, 33 amphisbaenians (20 endemic), 76 lizards (32 endemic) and 158 snakes (51 endemic) (Colli et al., 2002). Records from the Caatinga show 47 lizards, ten amphisbaenians, 112 snakes (Guedes et al., 2014), four chelonians and three crocodilians, totaling 176 species (Rodrigues, 2005b).

In the eastern Parnaíba Basin, State of Piauí, some areas have been inventoried: Parque Nacional Serra da Capivara (Cavalcante et al., 2014), Estação Ecológica Uruçuí-Una (Dal Vechio et al., 2013), Parque Nacional Serra das Confusões (Dal Vechio et al., 2016), Parque Nacional Sete Cidades (Rocha & Prudente, 2010), and sites in the municipalities of Valença (Vanzolini, 1976), Castelo do Piauí (Rodrigues & Prudente, 2011), Picos (Benício et al., 2015a), Barras (Benício et al., 2015b) and Batalha (Silva et al., 2015).

Southern Piauí State is among the Brazilian regions most coveted by agribusiness (Reydon & Monteiro, 2006) Here we provide a list of reptiles for the Middle Gurguéia region (MG) and a cluster analysis of the reptile species composition within the MG, comparing with eight previous inventories in the eastern Parnaíba River Basin in the state.

MATERIAL AND METHODS

Study site

The collection studied includes reptiles from five municipalities in the Middle Gurguéia region (MG), southwestern Piauí: Alvorada do Gurguéia (AG) 08°27’03.6”S, 43°52’05.05”W; Cristino Castro (CC) 08°47’36.0”S, 44°12’26.2”W; Palmeira do Piauí (PP) 08°43’32.7”S, 44°14’04.5”W; Redenção do Gurguéia (RG) 09°28’24.8”S, 44°36’2.30”W, and Bom Jesus (BJ) 09°05’18.6”S, 44°19’41.4”W. Figure 1 shows these areas in the Gurguéia River Basin and eight other areas previously inventoried in the Parnaíba River Basin, used here for comparison: the municipalities of Batalha (BT; Silva et al., 2015), Barras (BR; Benício et al., 2015b), Castelo do Piauí (CP; Rodrigues & Prudente, 2011), Picos (PC; Benício et al., 2015a), and the conservation units Parque Nacional Sete Cidades (7C; Rocha & Prudente, 2010), Parque Nacional Serra da Capivara (CA; Cavalcante et al., 2014), Estação Ecológica de Uruçuí-Una (UU; Dal Vechio et al., 2013), and Parque Nacional Serra das Confusões (CO; Dal Vechio et al., 2016). Notes on the geographic distribution of reptiles of the Parnaíba River Basin are provided in the discussion. Authors of species are listed only in the tables.

FIGURE 1: Study areas in the Middle Gurguéia and previously studied areas. (A): northeastern Brazil: Piauí (PI), Bahia (BA) and Maranhão (MA). Black dots show the locations where other studies were conducted: Barras (BR), Batalha (BT), Parque Nacional Sete Cidades (7C), Castelo do Piauí (CP), Picos (PC), Parque Nacional Serra da Capivara (CA), Parque Nacional Serra das Confusões (CO) and Estação Ecológica do Uruçuí-Una (UU); (B): The five municipalities in this study in the Middle Gurguéia (MG), Gurguéia River Basin, southeastern Piauí: 1: Alvorada do Gurguéia (AG), 2: Palmeira do Piauí (PP), 3: Cristino Castro (CC), 4: Bom Jesus (BJ) and 5: Redenção do Gurguéia (RG). 

Data collection

The data from the Gurguéia River Basin are based on a reptile collection formerly housed in the Laboratório de Zoologia, Universidade Federal do Piauí (UFPI), Campus Professora Cinobelina Elvas (CPCE), Bom Jesus, Piauí. Labels found with the specimens indicate that they were fixed in 10% formalin, preserved in 70% ethanol, and collected by active searching from 2010 to 2012. No collecting effort was available. The nomenclature follows recent taxonomic literature (Zaher et al., 2009; Wüster & Bérnils, 2011; Harvey et al., 2012; Dal Vechio et al., 2016). Following this study, all specimens were deposited in the Laboratório Especial de Coleções Zoológicas (LECZ), Instituto Butantan, São Paulo, Brazil (Appendix 1). The conservation status of the species was obtained from the report of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES, 2016).

Data analysis

We first analyzed the similarity among the five sites in the Middle Gurguéia. In a second analysis, we considered all these five sites as one, termed MG. We compared the species composition in MG with eight other areas previously inventoried in the eastern Parnaíba River Basin, termed PRB (Fig. 1): 7C, BT, BR, CP, PC, CA, UU and CO. Inventories in areas CP and 7C, which included only snakes, were not included in the analysis for all taxa, as this would have biased the results. For both analyses, similarity dendrograms were constructed using the Unweighted Pair Group Method with Arithmetic Mean (UPGMA) algorithm, using the Jaccard coefficient in the software R version 3.0.3 (R Development Core Team, 2014), Vegan package (Oksanen et al., 2016). The Jaccard distance measures dissimilarities among sites, based on species incidences (presences-absences) (Magurran, 2013).

RESULTS

Reptiles in the Middle Gurguéia

We analyzed a total of 69 specimens: 33 lizards; five amphisbaenians; 28 snakes; two chelonians, Mesoclemmys tuberculata and Phrynops geoffroanus: and one crocodilian, Paleosuchus palpebrosus. The lizards belong to eight families (nine genera, ten species) and the snakes to four families (15 genera, 15 species). A species of Amphisbaenidae was also represented. Tables 1 and 2 list the reptile species, their families, and the number of specimens recorded from each location. Four species are listed as vulnerable in Appendix 2 of CITES (2016): Iguana iguana, Salvator merianae, Boa constrictor and P. palpebrosus.

TABLE 1: Species of reptiles and number of individuals recorded in each study area of the Middle Gurguéia River Basin. Municipalities: AG: Alvorada do Gurguéia, BJ: Bom Jesus, CC: Cristino Castro, PP: Palmeira do Piauí, RG: Redenção do Gurguéia. MG* refers to samples with no specific point of collection, but certainly within the MG region. T = Total number of specimens. 

AG BJ CC PP RG MG * T
REPTILIA
AMPHISBAENIDAE
Amphisbaena vermicularis Wagler, 1824 3 2 5
GEKKONIDAE
Hemidactylus mabouia (Moreau de Jonnès, 1818) 1 1 2
IGUANIDAE
Iguana iguana (Linnaeus, 1758) 1 1
POLYCHROTIDAE
Polychrus acutirostris Spix, 1825 1 1
TEIIDAE
Ameiva ameiva (Linnaeus, 1758) 3 3
Salvator merianae (Duméril & Bibron, 1839) 1 1
TROPIDURIDAE
Tropidurus hispidus (Spix, 1825) 1 1 9 11
Tropidurus semitaeniatus (Spix, 1825) 7 7
SCINCIDAE
Mabuya heathi (Schmidt & Inger, 1951) 2 2
PHYLLODACTYLIDAE
Gymnodactylus geckoides Spix, 1825 1 1
GYMNOPHTHALMIDAE
Micrablepharus maximiliani (Reinhardt & Lütken, 1862) 4 4
BOIIDAE
Boa constrictor Linnaeus, 1758 1 1
Epicrates assisi Machado, 1945 1 1 2
COLUBRIDAE
Chironius flavolineatus (Boettger, 1885) 1 1
Helicops leopardinus (Schlegel, 1837) 1 1
Oxybelis aeneus (Wagler, 1824) 1 1
Spilotes pullatus (Linnaeus, 1758) 1 1
DIPSADIDAE
Apostolepis cearensis Gomes, 1915 1 1
Erythrolampus poecilogyrus (Wied, 1825) 2 2
Leptodeira annulata (Linnaeus, 1758) 1 1
Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 4 2 6
Philodryas nattereri Steindachner, 1870 1 3 2 6
Phimophis iglesiasi (Gomes, 1915) 1 1
Psomophis joberti (Sauvage, 1884) 1 1
Xenodon merremii (Wagler, 1824) 2 2
VIPERIDAE
Crotalus durissus Linnaeus, 1758 1 1
CHELIDAE
Mesoclemmys tuberculata (Luederwaldt, 1926) 1 1
Phrynops geoffroanus (Schweigger, 1812) 1 1
ALLIGATORIDAE
Paleosuchus palpebrosus (Cuvier, 1807) 1 1
TOTAL 1 26 8 29 2 3 69

TABLE 2: Diversity of nine areas in the Parnaíba River Basin: MG: Middle Gurguéia (this study); CP: Castelo do Piauí; PC: Picos; CO: Parque Nacional Serra das Confusões; CA: Parque Nacional Serra da Capivara; UU: Estação Ecológica do Uruçuí-Una; 7C: Parque Nacional Sete Cidades; BR: Barras and BT: Batalha municipalities. Asterisks indicate number of animals collected not provided. CP and 7C did not inventory lizards. Symbols refer to individuals found only in: ∆: Cerrado, □: Caatinga and ◊: Cerrado-Caatinga ecotone. 

MG CP PC CO CA UU 7C BR BT
REPTILIA
DACTYLOIDAE
Norops brasiliensis Vanzolini & Williams, 1970 ∆ 2
Norops meridionalis (Boettger, 1885) ∆ 15
GEKKONIDAE
Hemydactylus agrius Vanzolini, 1978 ◊ *
Hemydactylus brasilianus (Amaral, 1935) 16 28 15
Hemidactylus mabuia (Moreau de Jonnès, 1818) 2 * 3 * *
Lygodactylus klugei (Smith, Martin & Swain, 1977) * 14
GYMNOPHTALMIDAE
Calyptommatus confusionibus Rodrigues, Zaher & Curcio, 2001 □ 14
Colobosauroides cearensis Cunha, Lima-Verde & Lima 1991 ◊ *
Colobosaura modesta (Reinhardt & Lütken, 1862) 45 7 44
Micrablepharus maximiliani (Reinhardt & Lütken, 1862) 32 100 85 *
Procellosaurinus erythrocercus Rodrigues, 1991 □ 16 92
Vanzosaura rubricauda (Boulenger, 1902) ◊ *
HOPLOCERCIDAE
Hoplocercus spinosus Fitzinger, 1843 18 13
IGUANIDAE
Iguana iguana (Linnaeus, 1758) 1 * 2 1 7 * *
LEIOSAURIDAE
Enyalius bibronii Boulenger, 1885 □ 18 6
SCINCIDAE
Copeoglossum nigropunctatum (Spix, 1825) 6 10
Mabuya frenata (Cope, 1862) □ 10
Mabuya heathi (Schmidt & Inger, 1951) 2 * 11 * *
Mabuya nigropunctata (Spix, 1825) □ 17
PHYLLODACTYLIDAE
Gymnodactylus geckoides Spix, 1825 ◊ 1 *
Phyllopezus pollicaris (Spix, 1825) * 12 33 25 *
POLYCHROTIDAE
Polychrus acutirostris Spix, 1825 1 * 4 *
SPHAERODACTYLIDAE
Coleodactylus brachystoma (Amaral, 1935) 1 19
Gonatodes humeralis (Guichenot, 1855) ◊ * *
TEIIDAE
Ameiva ameiva (Linnaeus, 1758) 3 * 29 16 109 * *
Ameivula ocellifera (Spix, 1825) * *
Ameivula confusioniba (Arias, De Carvalho, Rodrigues & Zaher, 2011) □ *
Ameivula cf. mumbuca Colli et al., 2003 ∆ 162
Ameivula sp. □ *
Glaucomastix venetacauda (Arias, De Carvalho, Rodrigues & Zaher, 2011) * 23 56
Kentropyx calcarata Spix, 1825 ∆ 5
Salvator merianae (Duméril & Bibron, 1839) 1 * 2 1 1 * *
Tupinambis quadrilineatus Manzani & Abe, 1997 ∆ 12
Tupinambis teguixin (Linnaeus, 1758) ◊ *
TROPIDURIDAE
Stenocercus squarrosus Nogueira & Rodrigues, 2006 □ 13 5
Tropidurus helenae (Manzani & Abe, 1990) □ 61
Tropidurus hispidus (Spix, 1825) 11 * 84 100 * *
Tropidurus oreadicus Rodrigues, 1987 ∆ 301
Tropidurus semitaeniatus (Spix, 1825) 7 32 52 45 *
AMPHISBAENIDAE
Amphisbaena alba Linnaeus, 1758 ∆ 8
Amphisbaena frontalis Vanzolini, 1991 □ 5
Amphisbaena miringoera Vanzolini, 1971 1 5
Amphisbaena polystega (Duméril, 1851) 1 14
Amphisbaena vermicularis Wagler, 1824 5 * 2 17 *
TYPHLOPIDAE
Trilepida cf. fuliginosa 5
Typhlopsbron gersmianus Vanzolini, 1972 ∆ 5
LEPTOTYPHLOPIDAE
Tricheilostoma brasiliensis (Laurent, 1949) ∆ 4
BOIDAE
Boa constrictor Linnaeus, 1758 1 1 * 6 3
Corallus hortulanus (Linnaeus, 1758) 3 2 6
Epicrates assisi Machado, 1945 2 2 1 3 1 *
Eunectes murinus (Linnaeus, 1758) 4 1 *
COLUBRIDAE
Chironius exoletus (Linnaeus, 1758) ∆ 1
Chironius flavolineatus (Boettger, 1885) 1 14
Drymarcon corais (Boie, 1827) 3 3
Drymoluber brazili (Gomes, 1918) □ 2
Helicops leopardinus (Schlegel, 1837) ◊ 1
Leptophis ahaetulla (Linnaeus, 1758) 1 2 3
Mastigodryas bifossatus (Raddi, 1820) 1 6
Mastigodryas boddaerti (Sentzen, 1796) 2 1
Oxybelis aeneus (Wagler, 1824) 1 * 1 2 2
Spilotes pullatus (Linnaeus, 1758) 1 1 3 1 6 4 *
Tantilla melanocephala (Linnaeus, 1758) 2 5 2
DIPSADIDAE
Apostolepis cearensis Gomes, 1915 1 4 10 11 1
Apostolepis polylepis Amaral, 1921 ∆ 1
Boiruna sp. ∆ 2
Erythrolampus poecilogyrus (Wied-Neuwied, 1825) 2 9 * 62 2
Erythrolamprus miliaris (Linnaeus, 1758) □ 1
Erythrolamprus reginae (Linnaeus, 1758) ∆ 17
Erythrolamprus taeniogaster (Jan, 1863) ∆ 3
Erythrolampus viridis (Günther, 1862) 8 * 1 4 *
Helicops angulatus (Linnaeus, 1758) ∆ 7
Hydrops triangularis (Wagler, 1824) ∆ 8
Leptodeira annulata (Linnaeus, 1758) ◊ 1 3 3 *
Lygophis paucidens Hoge, 1953 2 2
Oxyrhopus trigeminus A.M.C. Duméril, Bibron & A.H.A. Duméril, 1854 6 7 * 3 2 20 9 *
Oxyrhopus rhombifer A.M.C. Duméril, Bibron & A.H.A. Duméril, 1854 ∆ 14
Philodryas nattereri Steindachner, 1870 6 10 * 1 4 30 1 *
Phylodryas cf. aestiva Duméril, Bibron & A.H.A. Duméril, 1854 ◊ *
Phylodryas olfersii (Lichtenstein, 1823) 1 1 17 1 * *
Phylodryas joberti (Sauvage, 1884) ◊ * *
Phimophis iglesiasi (Gomes, 1915) 1 5 1 4
Pseudoboa nigra (Duméril, Bibron & A.H.A. Duméril, 1854) 2 * 5 1 2 6 *
Psomophis joberti (Sauvage, 1884) 1 1 15 2 *
Rodriguesophis iglesiasi (Gomes, 1915) 1 4
Sibynomorphus mikanii (Schlegel, 1837) ∆ 1
Taeniophallus occipitalis (Jan, 1863) 3 1
Thamnodynastes sp. 8 6 17
Xenodon merremii (Wagler, 1824) 2 1 1 110 6
Xenodon nattereri (Steindachner, 1867) 5 1 1
ELAPIDAE
Micrurus ibiboboca (Merrem, 1820) 1 * 7 9
VIPERIDAE
Bothrops lutzi (Miranda-Ribeiro, 1915) 3 2 2
Bothrops moojeni Hoge, 1966 ∆ 104 *?
Bothropoides erythromelas Amaral, 1923 *
Crotalus durissus (Linnaeus, 1758) 1 1 1 15 5
CHELIDAE
Mesoclemmys perplexa Bour & Zaher, 2005 □ 3
Mesoclemmys tuberculata (Luederwaldt, 1926) 1 6 1 *
Phrynops cf. tuberosus (Peters, 1870) ∆ 4
Phrynops geoffroanus (Schweigger, 1812) ◊ 1 * * *
ALLIGATORIDAE
Caiman crocodilus (Linnaeus, 1758) ∆ 3
Paleosuchus palpebrosus (Cuvier, 1807) ◊ 1 * *
Total Specimens 69 74 * 460 602 1,471 70 * *
Total Species 29 19 25 47 28 64 22 24 18

Among the lizards collected in MG, the most abundant was Tropidurus hispidus (11 specimens), recorded in BJ, CC and PP, followed by Tropidurus semitaeniatus (seven specimens), recorded in MG, CO, CA and UU. These two species likely also occur in the other areas, because both are widespread in northeastern Brazil (Passos et al., 2016).

The municipalities of Bom Jesus (BJ) and Cristino Castro (CC) had three species in common, Amphisbaena vermicularis, Hemidactylus mabouia and T. hispidus; only T. hispidus occurred in both Cristino Castro (CC) and Palmeira do Piauí (PP). For snakes, Philodryas nattereri was present in AG, BJ and PP, and Oxyrhopus trigeminus in BJ and PP. All other snakes each appeared at only one site. The most abundant family was Dipsadidae, with eight species.

The dendrogram for all reptile species of the MG region showed BJ and PP as the most similar, while RG differed most from the other localities (Fig. 2).

FIGURE 2: Dendrogram for similarity of reptile species compositions in five areas in the Middle Gurguéia (MG), southern Piauí. The rule bar shows the Jaccard coefficient. RG: Redenção do Gurguéia, AG: Alvorada do Gurguéia, CC: Cristino Castro, BJ: Bom Jesus, PP: Palmeira do Piauí. 

Similarity between reptiles in MG and other areas in the eastern Parnaíba River Basin

We compared the results for MG with eight previously studied areas in the eastern Parnaíba River Basin (CP, PC, CO, CA, UU, 7C, BR and BT). The richness of reptiles from all studies comprised 100 species: 39 lizards, five amphisbaenians, 50 snakes, four turtles and two crocodilians (Table 2).

Of the nine inventories carried out in the eastern Parnaíba River Basin (PRB), the most specimens and highest richness were found in the Estação Ecológica de Uruçuí-Una (Dal Vechio et al., 2013) and the Parque Nacional Serra das Confusões (Dal Vechio et al., 2016), respectively (Table 2).

Helicops leopardinus (Schlegel, 1837) was found only in MG. From the label, this specimen was found in a small stream near the municipality of Bom Jesus, Piauí (see Appendix 1).

The species found in more than seven localities were Iguana iguana, Ameiva ameiva, Salvator merianae, Epicrates assisi, Spilotes pullatus, Oxyrhopus trigeminus, Philodryas nattereri, and Pseudoboa nigra (Table 2).

The largest number of reptile species shared by two sites was between CO and UU with 27 species, followed by CO and CA with 23 species. The smallest number of shared species was between 7C and BT, with one species only. The dendrogram for lizards indicated two groups: (1) MG, PC, BT, BR and (2) CA, CO and UU (Fig. 3).

FIGURE 3: Dendrogram for similarity of lizard species composition in the Middle Gurguéia (MG) with previously studied areas in Piauí. The rule bar shows the Jaccard coefficient. BR: Barras, BT: Batalha, MG: Middle Gurguéia, PC: Picos, UU: Estação Ecológica do Uruçuí-Una, CA: Parque Nacional Serra da Capivara, CO: Parque Nacional Serra das Confusões. Castelo do Piauí (CP) and Parque Nacional Sete cidades (7C) were not included in this analysis. 

The most common snakes recorded were B. constrictor (except in CO, CA, BR, and BT), Epicrates assisi (except in PC, CA and BT), Spilotes pullatus (except in PC and BT), Apostolepsis cearensis (except in PC, CA, BR and BT), Xenodon merremii (except in CP, PC, BR and BT), Oryrhopus trigeminus, Philodryas nattereri (except in BT), P. olfersi (except in MG, CP and PC), Pseudoboa nigra (except in MG and BT), and Crotalus durissus (except in PC, CA, BR and BT).

The dendrogram for snakes showed similar compositions between (1) MG, CP, 7C and UU; (2) BT and CO; and (3) CA and BR; while PC was less similar, forming a separate cluster (Fig. 4).

FIGURE 4: Dendrogram for similarity of snake species compositions in the Middle Gurguéia (MG) with other previously studied areas in Piauí. The rule bar shows the Jaccard coefficient. PC: Picos, CA: Parque Nacional Serra da Capivara, BR: Barras, BT: Batalha, CO: Parque Nacional Serra das Confusões, UU: Estação Ecológica do Uruçuí-Una, CP: Castelo do Piauí, 7C: Parque Nacional Sete Cidades. 

The dendrogram resulting from a comparison of all sites and all species showed two groups: (1) MG, BT, BR and PC, and (2) CA, CO and UU (Fig. 5). Areas CP and 7C (only snakes) were not included in this analysis. However, even if these areas were included, the result would show no bias, resulting in the same topology as Fig. 5, only CP and 7C grouping with UU.

FIGURE 5: Dendrogram for similarity of all reptile species compositions in the Middle Gurguéia (MG) and other previously studied areas in Piauí. The rule bar shows the Jaccard coefficient. PC: Picos, BR: Barras, BT: Batalha, UU: Estação Ecológica do Uruçuí-Una, CA: Parque Nacional Serra da Capivara, CO: Parque Nacional Serra das Confusões. Castelo do Piauí (CP) and Sete Cidades (7C) were not included in this analysis. 

Surprisingly, all dendrograms for the Parnaíba River Basin (Figs. 3-5), including MG, demonstrated a close relationship of the reptile fauna with the environments where they were found: Cerrado (UU), Caatinga (CA and CO) and Cerrado-Caatinga ecotone (PC, BR, MG, BT, 7C, CP). This result was also confirmed by the species that were found exclusively in areas of Cerrado (19 species), Caatinga (14) and Cerrado-Caatinga ecotone (12), as apparent from the symbols in Table 2.

DISCUSSION

The reptile assemblage in the Middle Gurguéia

Although this study was based on a collection of reptiles that lacks information about the collection effort, we consider that no data should be discarded or neglected. This assertion is supported by the finding of a specimen of Helicops leopardinus, the first record of this species for Piauí. Helicops is a genus of semi-aquatic and very specialized snakes (Cisneros-Heredia, 2006), so we suggest that more-thorough collections should be carried out in the Parnaíba River Basin, especially near water bodies.

The list of reptile species found in MG indicates an affinity with the Cerrado-Caatinga ecotone (e.g., Gymnodactylus geckoides; Hemidactylus agrius; Vanzosaura rubricauda) in concordance with results from other studies (Colli et al., 2002; Rodrigues, 2003; Sawaya et al., 2008), although some species (e.g., Boa constrictor, Spilotes pullatus, Philodryas nattereri, Iguana iguana, Ameiva ameiva and Salvator merianae) were found in areas outside these habitats (Henderson et al., 1995; Bérnils et al., 2001; Cicchi et al., 2007; Vaz-Silva et al., 2007). In addition, the fauna of MG was similar only to the inventories carried out in Picos (Benício et al., 2015a), Barras (Benício et al., 2015b) and Batalha (Silva et al., 2015), all areas of Cerrado-Caatinga ecotone (Figs. 3-5), reinforcing the evidence that the composition of the fauna in MG is not associated with the Cerrado or Caatinga biomes separately.

Comparison between species composition in Middle Gurguéia with inventoried areas of eastern Parnaíba River Basin (PRB)

The finding of the largest number of individuals and the highest reptile richness in the inventories conducted in the Parque Nacional Serra da Capivara (CA) and Parque Nacional Serra das Confusões (CO) may result from a higher collection effort in these studies compared to surveys in other localities in the PRB (Rocha & Prudente, 2010; Rodrigues & Prudente, 2011; Cavalcante et al., 2014; Benício et al., 2015a, b; Silva et al., 2015). The CO inventory discovered and described five new species (see Table 2), which was attributed to the collection effort (Dal Vechio et al., 2016).

The dendrograms of similarity among the nine study areas of the PRB, including MG (Figs. 3-5), showed that the species composition is correlated with the Cerrado, Caatinga or ecotone areas (transitions between these biomes). Species found predominantly in one of these environments may have a narrower niche compared to species found at virtually all sites in the PRB. This argument is supported by studies that demonstrate the association of reptile species with the structure of the environment (Garden et al., 2007; Stumpel & Werf, 2012). Pelegrin et al. (2017) described differences in microhabitat preferences in the Caatinga among Tropidurus hispidus, T. helenae and T. semitaeniatus, three sympatric species found in the Parque Nacional Serra da Capivara. Drymoluber brazili, Micrablepharus maximiliani and Tupinambis quadrilineatus, which were also found in other areas of Piauí, were recorded in areas with a predominance of Caatinga, Cerrado-Caatinga ecotone and Cerrado vegetation, respectively (Moura et al., 2010; Freitas et al., 2012; Silva et al., 2013).

Further studies of the degree of interaction of reptile species within the vegetation composition and physical structure in the Cerrado, Caatinga and/or ecotone areas should be conducted to confirm the species-environment association, in order to explain the reptile diversity and composition in the PRB. Understanding the distribution, composition and determining factors for the presence of each reptile species in each environment is fundamentally important for species conservation and management, especially for species that are considered vulnerable, as observed in this study.

CONCLUSIONS

Our examination of this collection revealed a new record for the state of Piauí, the snake Helicops leopardinus (Schlegel, 1837). The cluster analysis showed that the reptile fauna in the eastern Parnaíba River Basin is closely identified with Cerrado, Caatinga or ecotonal areas individually.

Because of the rapid landscape transformation in northeastern Brazil, changing Cerrado and Caatinga vegetation complexes (including ecotonal areas) into agricultural areas, it is imperative to understand the diversity of species and their environmental relationships in order to inform the development of conservation strategies, especially in unprotected areas such as the Middle Gurguéia.

ACKNOWLEDGEMENTS

We are grateful to Valdir J. Germano for the taxonomic identifications, and Dr. Francisco Franco for accepting specimens to be deposited in the Laboratório Especial de Coleções Zoológicas (LECZ), Instituto Butantan. We also thank Brisa G. Costa for help in laboratory work, and Mr. Luis Casado Filho for his comments and language corrections. Janet W. Reid edited the English text.

REFERENCES

BENÍCIO, R.A.; LIMA, D.C. & FONSECA, M.G. 2015a. Species richness of reptiles in a Caatinga area in northeastern Brazil. Gaia Scientia, 9(1):89-94. [ Links ]

BENÍCIO, R.A.; DE MESQUITA, P.C.M.D.; CAVALCANTE, V.H.G.L. & FONSECA, M.G. 2015b. Répteis de uma região de ecótono no estado do Piauí, Nordeste do Brasil. Gaia Scientia, 9(1):95-100. [ Links ]

BÉRNILS, R.S.; BATISTA, M.A. & BERTELLI, P.W. 2001. Cobras e lagartos do Vale: levantamento das espécies de Squamata (Reptilia, Lepidosauria) da Bacia do Rio Itajai, Santa Catarina, Brasil. Revista de Estudos Ambientais, Blumenau, 3:69-79. [ Links ]

CAVALCANTE, L.B.Q.; COSTA, T.B.; COLLI, G.R.; COSTA, G.C.; FRANÇA, F.G.R.; MESQUITA, D.O.; PALMEIRA, C.N.S.; PELEGRIN, N.; SOARES, A.H.B.; TUCKER, D.B. & GARDA, A.A. 2014. Reptiles of protected areas in the Caatinga II: Serra da Capivara National Park, Piauí, Brazil. Check List, 10:18-27. [ Links ]

CICCHI, P.J.P.; SENA, M.A.; PECCININI-SEALE, D.M. & DUARTE, M.R. 2007. Snakes from coastal islands of state of São Paulo, southeastern Brazil. Biota Neotropica, 7(2):227-240. [ Links ]

CISNEROS-HEREDIA, D.F. 2006. Reptilia, Colubridae, Helicops angulatus and Helicops leopardinus: Distribution extension, new country record. Check List, 2(1):36-37. [ Links ]

CITES. 2016. Convention on International Trade in Endangered Species of Wild Fauna and Flora (2016). “Appendices I, II and III”. Available at: Available at: https://cites.org/eng/app/appendices.php . Accessed on: 06/06/2017. [ Links ]

COLLI, G.R.; BASTOS, R.P. & ARAÚJO, A.B. 2002. The character and dynamics of the Cerrado Reptiles. In: Oliveira, P.S. & Marques, R.J. (Eds.). The Cerrados of Brazil. Ecology and natural history of a neotropical savanna. New York,Columbia University Press, [ Links ]

COSTA, H. & BÉRNILS, R.S. 2015. Répteis brasileiros: Lista de espécies. Herpetologia Brasileira, 4:75-93. [ Links ]

DAL VECHIO, F.; RECODER, R.; RODRIGUES, M.T. & ZAHER, H. 2013. The reptiles of the Estação Ecológica de Uruçuí-Una, State of Piauí, Brazil. Papéis Avulsos de Zoologia, 53:225-243. [ Links ]

DAL VECHIO, F.; TEIXEIRA JR., M.; RECODER, R.S.; RODRIGUES, M.T. & ZAHER, H. 2016. The herpetofauna of Parque Nacional da Serra das Confusões, state of Piauí, Brazil, with a regional species list from an ecotonal area of Cerrado and Caatinga. Biota Neotropica, 16:1-19. [ Links ]

FREITAS, M.A.; FRANÇA, D.P.F. & VERÍSSIMO, D. 2012. Distribution extension of Drymoluber brazili (Gomes, 1918) (Serpentes: Colubridae) for the state of Piauí, Brazil. Check List, 8(1):168-169. [ Links ]

GARDEN, J.G.; MCALPINE, C.A.; POSSINGHAM, H.P. & JONES, D.N. 2007. Habitat structure is more important than vegetation composition for local-level management of native terrestrial reptile and small mammal species living in urban remnants: A case study from Brisbane, Australia. Austral Ecology, 32(6):669-685. [ Links ]

GUEDES, T.B.; NOGUEIRA, C. & MARQUES, O.A.V. 2014. Diversity, natural history, and geographic distribution of snakes in the Caatinga, Northeastern Brazil. Zootaxa, 3863:1-93. [ Links ]

HARVEY, M.B.; UGUETO, G.N. & GUTBERLET JR., R.L. 2012. Review of Teiid morphology with a revised taxonomy and phylogeny of the Teiidae (Lepidosauria: Squamata). Zootaxa, 3459:1-156. [ Links ]

HENDERSON, R.W.; MICUCCI, T.W.P.; PUORTO, G. & BOURGEOIS, R.W. 1995. Ecological correlates and patterns in the distribution of Neotropical Boines (Serpentes: Boidae): A preliminary assessment. Herpetological Natural History, 3:15-27. [ Links ]

MAGURRAN, A.E. 2013. Measuring biological diversity. Wiley-Blackwell, New York. [ Links ]

MOURA, M.; DAYRELL, J.S. & SAN-PEDRO, V.A. 2010. Reptilia, Gymnophtalmidae, Micrablepharus maximiliani (Reinhardt and Lutken, 1861): Distribution extension, new state record and geographic distribution map. Check List, 6(3):419-426. [ Links ]

OKSANEN, J.; BLANCHET, F.G.; KINDT, R.; LEGENDRE, P.; MINCHIN, P.R.; O’HARA, R.B.; SIMPSON, G.L.; SOLYMOS, P.; STEVENS, M.H.M. & WAGNER, H. 2016. Package ‘vegan’: Community Ecology Package. Available at: Available at: http://cran.r-project.org/web/packages/vegan/index.html . Accessed on: 03/05/2016. [ Links ]

PASSOS, D.C.; MESQUITA, P.C.M.D. & BORGES-NOJOSA, D.M. 2016. Diversity and seasonal dynamic of a lizard assemblage in a Neotropical semiarid habitat. Studies on Neotropical Fauna and Environment, 51(1):19-28. [ Links ]

PELEGRIN, N.; MESQUITA, D.O.; ALBINATI, P.; CALDAS, F.L.S.; DE QUEIROGA CAVALCANTI, L.B.; COSTA, T.B.; FALICO, D.A.; GALDINO, J.Y.; TUCKER, D.B. & GARDA, A.A. 2017. Extreme specialization to rocky habitats in Tropidurus lizards from Brazil: Trade-offs between a fitted ecomorph and autoecology in a harsh environment. Austral Ecology, 12486:1-13. [ Links ]

R CORE TEAM. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: Available at: www.R-project.org . Accessed on: 10/01/2015. [ Links ]

REYDON, B.P. & MONTEIRO, M.S.L. 2006. A ocupação do Cerrado piauiense: Um processo de valorização fundiária. In: Reydon, B.P. & Cornélio, A. (Eds.). Mercados de Terras no Brasil - Estrutura e Dinâmica. Brasília, Ministério do Desenvolvimento Agrário. [ Links ]

ROCHA, W.A. & PRUDENTE, A.L.C. 2010. The snake assemblage of Parque Nacional de Sete Cidades, State of Piauí, Brazil. South American Journal of Herpetology, 5:132-142. [ Links ]

RODRIGUES, F.S. & PRUDENTE, A.L.C. 2011. The snake assemblage (Squamata: Serpentes) of a Cerrado-Caatinga transition area in Castelo do Piauí, state of Piauí, Brazil. Zoologia, 28:440-448. [ Links ]

RODRIGUES, M.T. 2003. Herpetofauna da Caatinga. In: Leal, I.R.; Tabarelli, M. & Silva, J.M.C. (Eds.). Ecologia e Conservação da Caatinga. Recife, Universidade Federal de Pernambuco. p. 181-236. [ Links ]

RODRIGUES, M.T. 2005a. A biodiversidade dos cerrados: conhecimento atual e perspectivas, com uma hipótese sobre o papel das matas galerias na troca faunística durante ciclos climáticos. In: Scariot, A.; Sousa-Silva, J.C. & Felfili, J.M. (Eds.). Cerrado: Ecologia, Biodiversidade e Conservação. Brasília, Ministério do Meio Ambiente. p. 235-246. [ Links ]

RODRIGUES, M.T. 2005b. Conservação dos répteis brasileiros: os desafios de um país megadiverso. Megadiversidade, 1:87-94. [ Links ]

SAWAYA, R.J.; MARQUES, O.A.V. & MARTINS, M. 2008. Composition and natural history of a Cerrado snake assemblage at Itirapina, São Paulo state, southeastern Brazil. Biota Neotropica, 8:127-149. [ Links ]

SILVA, M.B.; CARVALHO, L.S. & RODRIGUES, V. 2015. Reptiles in an ecotonal area in northern state of Piauí, Brazil. Boletim do Museu de Biologia Mello Leitão, 37:437-455. [ Links ]

SILVA, M.B.; LIMA-FILHO, G.R.; CRONEMBERGER, A.A.; CARVALHO, L.S; MANZANI, P.R. & VIEIRA, J.B. 2013. Description of the hemipenial morphology of Tupinambis quadrilineatus Manzani and Abe, 1997 (Squamata, Teiidae) and new records from Piauí, Brazil. Zookeys, 361:61-72. [ Links ]

STUMPEL, A.H. & WERF, D.C. 2012. Reptile habitat preference in heathland: implications for heathland management. The Herpetological Journal, 22(3):179-182. [ Links ]

VANZOLINI, P.E. 1976. On the lizards of a Cerrado-Caatinga contact: evolutionary and zoogeographical implications (Sauria). Papéis Avulsos de Zoologia, 29:111-119. [ Links ]

VAZ-SILVA, W.; GUEDES, A.G.; AZEVEDO-SILVA, P.L.; GONTIJO, F.F.; BARBOSA, R.S.; ALOÍSIO, G.R. & OLIVEIRA, F.C.G. 2007. Herpetofauna, Espora Hydroeletric Power Plant, State of Goiás, Brazil. Check List, 3:338-345. [ Links ]

WÜSTER, W. & BÉRNILS, R.S. 2011. On the generic classification of the rattlesnakes, with special reference to Neotropical Crotalus durissus complex (Squamata: Viperidae). Zoologia, 28(4):417-419. [ Links ]

ZAHER, H.; GRAZZIOTIN, F.G.; CADLE, J.E.; MURPHY, R.W.; MOURA-LEITE, J.C.D.; & BONATTO, S.L. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia, São Paulo, 49(11):115-153. [ Links ]

1Editor Responsável: Marcelo Duarte

Publicado com o apoio financeiro do Programa de Apoio às Publicações Científicas Periódicas da USP

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Appendix 1

List of the specimens used in this study, followed by the collection site and collection number, housed at the Instituto Butantan, IBSP: Instituto Butantan São Paulo; CRIB: Collection of Reptiles of Instituto Butantan.

Ameiva ameiva (Linnaeus, 1758), Palmeira do Piauí, PI, IBSP.CRIB.0380;

Amphisbaena vermicularis Wagler, 1824, Bom Jesus, PI, IBSP.CRIB.0403; IBSP.CRIB.0404; IBSP.CRIB.0405; IBSP.CRIB.0406; Cristino Castro, PI, IBSP.CRIB.0402;

Apostolepis cearensis Gomes, 1915, Redenção do Gurguéia, PI, IBSP-80.942;

Boa constrictor Linnaeus, 1758, Bom Jesus (Colégio Agrícola UFPI), PI, IBSP-81.301;

Chironius flavolineatus (Boettger, 1885), Palmeira do Piauí, PI, IBSP-80.935;

Crotalus durissus Linnaeus, 1758, PI, IBSP-81.316;

Epicrates assisi Machado, 1945, Bom Jesus, PI, IBSP-81.304; Canto do Buriti (6 km ao sul da cidade, BR135, km 170), PI, IBSP-81.317; Palmeira do Piauí, PI, IBSP-80.933;

Erythrolamprus poecilogyrus (Wied, 1825), Bom Jesus, PI, IBSP-81.302; IBSP-81.303;

Gymnodactylus geckoides Spix, 1825, Bom Jesus, PI, IBSP.CRIB.0394;

Helicops leopardinus (Schlegel, 1837), Bom Jesus, PI, IBSP-80.937;

Hemidactylu smabuia (Moreau de Jonnès, 1818), Bom Jesus, PI, IBSP.CRIB.0395; IBSP.CRIB.0396; Cristino Castro, PI;

Iguana iguana (Linnaeus, 1758), Bom Jesus, PI, IBSP.CRIB.0391;

Leptodeira annulata (Linnaeus, 1758), Redenção do Gurguéia, PI, IBSP-80.943;

Mabuya heathi (Schmidt & Inger, 1951), Palmeira do Piauí, PI, IBSP.CRIB.0393; IBSP.CRIB.0397;

Mesoclemmys tuberculata (Luederwaldt, 1926), Bom Jesus, PI, IBSP.CRIB.0334;

Micrablepharus maximiliani (Reinhardt & Lütken, 1862), Cristino Castro, PI, IBSP.CRIB.0398; IBSP.CRIB.0399; IBSP.CRIB.0400; IBSP.CRIB.0401;

Oxybelis aeneus (Wagler, 1824), Palmeira do Piauí, PI, IBSP-80.936;

Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854, Bom Jesus, PI, IBSP-80.938; IBSP-80.939; IBSP-80.840; Palmeira do Piauí, PI, IBSP-81.310; IBSP-81.311;

Philodryas nattereri Steindachner, 1870, Alvorada do Gurguéia, PI, IBSP-81.313; Bom Jesus (UFPI), PI, IBSP-81.307; IBSP-81.308; IBSP-81.309; Palmeira do Piauí, PI, IBSP-81.312; IBSP-80.934;

Phrynops geoffroanus (Schweigger, 1812), Bom Jesus, PI, IBSP.CRIB.0335;

Psomophis joberti (Sauvage, 1884), Bom Jesus, PI, IBSP-80.941;

Spilotes pullatus (Linnaeus, 1758), BR135, Km 367, PI, Monte Alegre do Piauí, IBSP-81.314;

Tropidurus hispidus (Spix, 1825), Bom Jesus, PI, IBSP.CRIB.0392; Cristino Castro, PI, IBSP.CRIB.0390; Palmeira do Piauí, PI, IBSP.CRIB.0381; IBSP.CRIB.0382; IBSP.CRIB.0383; IBSP.CRIB.0384; IBSP.CRIB.0385; IBSP.CRIB.0386; IBSP.CRIB.0387; IBSP.CRIB.0388; IBSP.CRIB.0389;

Tropidurus semitaeniatus (Spix, 1825), Palmeira do Piauí, PI, IBSP.CRIB.0373; IBSP.CRIB.0374; IBSP.CRIB.0375; IBSP.CRIB.0376; IBSP.CRIB.0377; IBSP.CRIB.0378; IBSP.CRIB.0379;

Xenodon merremii (Wagler, 1824), Bom Jesus, PI, IBSP-81.305; IBSP-81.306.

Received: July 17, 2017; Accepted: September 15, 2017

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