Research Article |
Corresponding author: Frederico G. R. França ( fredericogrf@gmail.com ) Academic editor: Robert Jadin
© 2018 Ivan L. R. Sampaio, Claudileide P. Santos, Rafaela C. França, Isabella M. M. C. Pedrosa, Mirco Solé, Frederico G. R. França.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Sampaio ILR, Santos CP, França RC, Pedrosa IMMC, Solé M, França FGR (2018) Ecological diversity of a snake assemblage from the Atlantic Forest at the south coast of Paraíba, northeast Brazil. ZooKeys 787: 107-125. https://doi.org/10.3897/zookeys.787.26946
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Despite an increase in studies focusing on snake ecology and composition in the northeastern Atlantic Forest, several poorly studied sites and environments remain. The aim of this study was to assess species richness and natural history attributes of the snakes of an assemblage in the Restinga, Tabuleiro and Forest environments of the Atlantic Forest of the south coast of Paraíba, northeastern Brazil. A total of 151 individuals of 27 species, 23 genera, and six families of snakes were found. The most effective sampling methods were time-constrained searches and incidental encounters. Species sampled most frequently were the blindsnake Epictia borapeliotes, the Boa Constrictor Boa constrictor, the Brown Vinesnake Oxybelis aeneus, and the Brazilian False Coral Snake Oxyrhopus trigeminus. The snake fauna is characterized mainly by terrestrial species found in open-area environments of Restinga and Tabuleiro, and with most species feeding on amphibians and small mammals. The rarefaction curve did not reach the asymptote and new species should be recorded for south coast of Paraíba in future studies. Despite the richness and composition of snakes of the south coast being similar to other areas in the state, there is a lack of some species typically linked to forests, and this is probably because of the high level of deforestation that the south area of the state has suffered.
inventory, natural history, open formations, restinga, Serpentes , species richness
Biological surveys are the foundation for our knowledge on biodiversity. They also provide the groundwork for ecological studies and provide an outline for implementing conservation strategies (
The Atlantic Forest is the most threatened biome in Brazil, and it has been suffering from intense deforestation and fragmentation since the time of European colonization. Even though less than six percent of the original vegetation remains, the Atlantic Forest still harbors high levels of biodiversity with more than 8,000 endemic species of vascular plants, amphibians, reptiles, birds and mammals (
In the Atlantic Forest of the four states (Rio Grande do Norte, Paraíba, Pernambuco and Alagoas) that comprise the PEC, the four main vegetation physiognomies in the region are: (a) Mangroves, saline-adapted tropical vegetation on the coast; (b) Coastal Restingas, low forest that grows on coastal sand dunes; (c) Semi-deciduous Forests, also known as Lowland Tabuleiro Forests, that are evergreen forests with natural savanna enclaves (called tabuleiros) that occur over faster-draining sand soils, and (d) Highland Stationary Forests, that are humid forest remnants scattered throughout Caatinga Highlands, known as Brejos de Altitude (
The snake fauna of the Atlantic Forest of Paraíba State, in Northeast Brazil, has been studied previously, in the central and north portions, but the south of the State remains unknown (
The study was conducted in Barra de Gramame, located in the south of the municipality of João Pessoa at the South Coast of Paraíba State, Northeast Brazil (Figure
The Barra de Gramame area covers approximately 843 ha (Figure
Variation of temperature, maximum (line with square) and minimum (line with triangle), precipitation as bars. Data from January 2012 and December 2013 (Source: INMET, http://www.inmet.gov.br/portal/index.php?r=bdmep/bdmep).
For the fieldwork conducted in Barra de Gramame, we employed the following snake survey methods: time-constrained search, incidental encounters, and specimens donated by local people. Snake specimens were obtained from January 2012 to December 2013 predominantly through 2520 man-hours of time-constrained search (see
For each specimen found in Barra de Gramame, we recorded information on location (with GPS), time, habitat use and microhabitat, and morphology. Snakes were collected under ICMBio collecting permit (SISBIO license 37318-1), preserved in 10% formalin and deposited in Coleção Herpetológica da Universidade Federal da Paraíba (Appendix). Some individuals of the most common species were released after we marked them by clipping ventral scales to identify them as previously captured. No recapture was obtained in this study. We categorized the snake size considering the mean body size of each species based on published data (França and Araújo 2006,
We constructed the species accumulation curves for the snakes of the South Coast using the individual-based rarefaction method (with the nonparametric Mao Tau estimator) to evaluate the relationship between collection effort and species saturation in the assemblage (
We recorded 151 individuals of 27 species, 23 genera, and six families (Boidae, Colubridae, Elapidae, Leptotyphlopidae, Typhlopidae, and Viperidae) (Table
Summary of the Information of Natural History of the Snakes in Barra de Gramame. Abbreviations of Municipalities are: AL = Alhandra; CA = Caaporã; CO = Conde; JP = João Pessoa (Barra de Gramame), PF = Pedras de Fogo, PI = Pitimbu. Habits are: AB = arboreal, AQ = aquatic, CR = cryptozoic, FO = fossorial, TE = terrestrial, SAB = semi-arboreal. Habitats are: T = tabuleiro, F = forest, R = restinga, * = Data from Herpetological Collection. Diet are: am = amphibians, an = anfisbaenas, ar = arthropods, bi = birds, fi = fishes, li = lizards, ma = mammals, sl = snails, sn = snakes. Capture Methods are: TCS = time-constrained search, DO = donated, IE = incidental encounters; – = No data available (see methods).
Family / Species (number of species) | N | Municipality | Habits | Habitats | Diet | Capture method |
---|---|---|---|---|---|---|
Boidae (3) | ||||||
Boa constrictor Linnaeus, 1758 | 16 | JP | SAB | T, F, R | ma, bi | TCS, DO, IE |
Corallus hortulanus (Linnaeus, 1758) | 1 | JP | AB | T | ma, bi | DO |
Epicrates assisi Machado, 1945 | 10 | AL, CO, JP, PI | TE, SAB | T, F | ma, bi, li | TCS, DO |
Colubridae; Colubrinae (5) | ||||||
Chironius flavolineatus Jan, 1863 | 1 | AL | SAB | F* | am | – |
Oxybelis aeneus (Wagler, 1824) | 14 | JP | AB | T | li | TCS, DO, IE |
Mastigodryas bifossatus (Raddi, 1820) | 1 | CO | TE | T* | ma | – |
Spilotes pullatus (Linnaeus, 1758) | 1 | PF | SAB | F* | ma, bi | – |
Tantilla melanocephala (Linnaeus, 1758) | 5 | AL, JP | FO | T, R | ar | TCS, IE |
Colubridae; Dipsadinae (13) | ||||||
Erythrolamprus taeniogaster (Jan, 1863) | 1 | JP | TE, AQ | R | fi, am | IE |
Helicops angulatus (Linnaeus, 1758) | 3 | CA, JP | AQ | R | fi, am | TCS |
Hydrodynastes gigas (Duméril, Bibron & Duméril, 1854) | 5 | JP | AQ | R | fi, am, sn, ma | TCS, IE |
Oxyrhopus petolarius Reuss, 1834 | 1 | JP | TE | T | ma, li | TCS |
Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 | 16 | CA, CO, JP | TE | T, F | ma, li | TCS, DO, IE |
Philodryas nattereri Steindachner, 1870 | 8 | AL, JP | TE | T | ma, bi, li, an | TCS, DO, IE |
Philodryas olfersii (Lichtenstein, 1823) | 10 | JP, PI | TE, SAB | T | ma, bi, li, an | TCS, DO, IE |
Philodryas patagoniensis (Girard, 1858) | 11 | JP | TE | T, R | ma, bi, li, an | TCS, DO, IE |
Phimophis guerini (Duméril, Bibron & Duméril, 1854) | 3 | CO, JP | CR, TE | T | li | IE |
Sibon nebulatus (Linnaeus, 1758) | 1 | PF | AB | F | sl | – |
Sibynomorphus mikanii (Schlegel, 1837) | 10 | AL, CA, JP | TE | T | sl | DO |
Taeniophallus occipitalis (Jan, 1863) | 7 | AL, CA, JP | TE | T | am | TCS, DO, IE |
Xenodon merremii (Wagler, 1824) | 1 | CO | TE | F* | am | – |
Elapidae (2) | ||||||
Micrurus ibiboboca (Merrem, 1820) | 1 | AL | CR, TE | T* | an, sn | – |
Micrurus potyguara Pires, Silva, Feitosa, Prudente, Pereira Filho & Zaher, 2014 | 3 | JP | CR, TE | T | an, sn | TCS, DO |
Leptotyphlopidae (1) | ||||||
Epictia borapeliotes (Vanzolini, 1996) | 16 | JP | FO | T | ar | TCS, DO, IE |
Typhlopidae (1) | ||||||
Amerotyphlops brongersmianus (Vanzolini, 1976) | 1 | CA | FO | T* | ar | – |
Viperidae (2) | ||||||
Bothrops leucurus Wagler, 1824 | 2 | AL, CA | TE | F* | ma, li, an | – |
Crotalus durissus Linnaeus, 1758 | 2 | CO | TE | R* | ma | – |
Species from the Atlantic Forest in south coast of Paraíba. A Boa constrictor B Epicrates assisi C Corallus hortulanus D Chironius flavolineatus E Oxybelis aeneus F Mastigodryas bifossatus G Spilotes pullatus H Tantilla melanocephala I Erythrolamprus taeniogaster J Helicops angulatus K Hydrodynastes gigas L Oxyrhopus petolarius M Oxyrhopus trigeminus N Philodryas nattereri O Philodryas olfersii. Photograph credits: Ivan L. Sampaio (A, B, C, E, K, L, M, N, O), Frederico G. França (D, H, I, J), Mayara Morais (F), Willianilson Pessoa (G).
Species from the Atlantic Forest in south coast of Paraíba: A Philodryas patagoniensis B Phimophis guerini C Sibon nebulatus D Sibynomorphus mikanii E Taeniophallus occipitalis F Xenodon merremii G Micrurus ibiboboca H Micrurus potyguara I Epictia borapeliotes J Amerotyphlops brongersmianus K Bothrops leucurus L Crotalus durissus. Photograph credits: Ivan L. Sampaio (A, B, D, E, H, I), Frederico G. França (F, G, J, L), Pedro T. S. Moura (C) Rafaela C. França (K).
The individual-based rarefaction curves didn’t reach stability (Figure
Richness estimators of snake assemblages for the south coast of Paraíba.
Richness Estimators | Mean ± Std Deviation |
---|---|
Observed Richness | 27 |
ACE | 40.59 ± 1.16 |
CHAO 1 | 51.83 ± 24.08 |
CHAO 2 | 51.83 ± 32.04 |
ICE | 40.21 ± 1.13 |
JACKNIFE 1 | 36.93 ± 3.05 |
JACKNIFE 2 | 44.84 ± 0.91 |
BOOTSTRAP | 31.09 ± 0.35 |
The snakes showed a diversity of habits and food preferences (Table
Below we present information on morphology, habitat use, and activity of all snake species found on the south coast of Paraíba. We include data on diet, habitat, and habits from published literature.
BOIDAE: Boa constrictor – A large terrestrial species (average SVL = 904.25 mm; range from 400 to 2000 mm; N = 16). Second most common species in the study area. Six individuals were found active during the day between 10:40 and 17:30, despite literature records indicating nocturnal activity for the species (
COLUBRIDAE: COLUBRINAE: Chironius flavolineatus – A moderate-sized semi-arboreal species (SVL = 598 mm; N = 1). No data of habitat use for the south coast is available. This species eats primarily amphibians (
COLUBRIDAE: DIPSADINAE: Erythrolamprus taeniogaster – A moderate-sized semi-aquatic species (SVL = 385 mm; N = 1). One individual was found resting in the water at 9:00. This species eats anurans (
ELAPIDAE: Micrurus ibiboboca – A moderate-sized cryptozoic species (SVL = 525 mm; N = 1). No data of habitat use for the south coast is available. This species eats amphisbaenians and snakes (
LEPTOTYPHLOPIDAE: Epictia borapeliotes – A small-sized fossorial species (average SVL = 110 mm; range from 70 to 136 mm; N = 16). This was the most common species in Gramame and it was very adapted to anthropic areas. All individuals were found active moving on sand, on grass and on unpaved and paved roads, during the day and twilight (from 8:45 to 17:30). Many individuals stung with tail points when handled. The representatives of this family eat ants and larvae, but there is no information on the diet of this species.
TYPHLOPIDAE: Amerotyphlops brongersmianus – A small-sized fossorial species (SVL = 212 mm; N = 1). No data of habitat use for the south coast is available. This species eats ant larvae (
VIPERIDAE: Bothrops leucurus – A large terrestrial species (SVL = 587 mm; N = 1). This species frequently is found in the urban area and in preserved forest patches. No data of habitat use for the south coast is available. This species eats frogs (juveniles) and small mammals (adults) (
The snake fauna of Barra de Gramame presents similar richness and composition compared with other snake assemblages from central and north coast of Paraíba State (
Despite the savanna enclaves extending along all the Northeast Atlantic Forest, this physiognomy is poorly known and highly threatened because of agriculture and pastures (
Although the reptiles of costal Restingas have been commonly studied in the Southeast and Central Atlantic Forest (
Two species are typical of forest environments (Sibon nebulatus and Bothrops leucurus), and six are habitat generalist, occurring also in open areas. This richness of forest snake species for the south coast is low if compared with assemblages studied for the north and central coasts (
Despite the presence of open area of Restinga and Tabuleiros, there is a lack of large forest patches in the south coast that are present in other areas of Paraíba State (
It is important to emphasize that there are large gaps in the conservation status of snake species in the PEC region; of the 27 species of snakes reported in this study, only two species (Corallus hortulanus and Crotalus durissus) were evaluated by the IUCN. In addition, some species are still being discovered in the PEC region, and have little information available, such as Micrurus potyguara (described in 2014) (
Finally, comparing with other snake assemblages in Paraíba, the fauna of south coast shows some peculiarities. The most common species was a blindsnake, the same as the North Coast (
We thank Julie Ray and an anonymous reviewer for review contributions. RCF thanks FAPESB for a PhD scholarship (BOL0353/2016) and CNPq for Doutorado Sanduíche no Exterior (SWE) scholarship (208442/2017-0). FGRF thanks the financial support from CNPq (Universal grant 404671/2016-0). MS thanks CNPq for a research scholarship (304999/2015-6) and Alexander von Humboldt Foundation/CAPES for a grant (BEX 0585/16-5)
Snake species collected at the Paraíba state’s south coast, northeast Brazil, and housed at the Coleção Herpetológica da Universidade Federal da Paraíba
João Pessoa – Barra de Gramame: Boa constrictor (CHUPB 12252/RT 419, RT 603, RT 661, RT 790), Corallus hortulanus (BG 40), Epicrates assisi (RT 792), Epictia borapeliotes (RT 531, RT 645, RT 646, RT 705, RT 825, RT 864, RT 887, RT 890), Erythrolamprus taeniogaster (RF 106), Helicops angulatus (RT 847), Hydrodynastes gigas (BG 26), Micrurus potyguara (RT 860), Oxybelis aeneus (RT 606, RT 700, RT 747, RT 861, RT 862, RT 889), Oxyrhopus petola (RT 701), Oxyrhopus trigeminus (RT 703, RT 765, RT 793, RT 859, RT 891, RT 892), Philodryas nattereri (CHUFPB 7669/RT 166, RT 763), Philodryas olfersii (RT 072, RT 702, RT 748, RT 888), Philodryas patagoniensis (RT 223, RT 604, RT 605, RT 706, RT 750, RT 791), Taeniophallus occipitalis (RT 704, RT 749), Tantilla melanocephala (RT 766, RT 893); Alhandra: Bothrops leucurus (UFPB 12963); Chironius flavolineatus (UFPB 9374); Epicrates assisi (UFPB 13163), Micrurus ibiboboca (UFPB 13636); Philodryas nattereri (UFPB 13642); Sibynomorphus neuwiedi (UFPB 12643); Taeniophallus occipitalis (UFPB 9390); Tantilla melanocephala (UFPB 9389); Caaporã: Amerotyphlops brongersmianus (CHUFPB 15704); Bothrops leucurus (UFPB 12961); Helicops angulatus (CHUFPB 15670, 15715); Oxyrhopus trigeminus (CHUFPB 15806); Sibynomorphus mikanii (UFPB 12948-53); Taeniophallus occipitalis (CHUFPB 15837); Conde: Crotalus durissus (UFPB 5053, 5803); Epicrates assisi (UFPB 13163), Mastigodryas bifossatus (UFPB 4825); Oxyrhopus trigeminus (UFPB 13157-8); Phimophis guerini (UFPB 13976-7); Xenodon merremii (UFPB 13974); Pitimbu: Epicrates assisi (UFPB 13164, 13179, 13199), Philodryas olfersii (UFPB 13650); Pedras de Fogo: Spilotes pullatus (UFPB 13981).