Research Article |
Corresponding author: Marco Antonio de Freitas ( philodryas@hotmail.com ) Academic editor: Aaron Bauer
© 2017 Marco Antonio de Freitas, Ruhan Saldanha Vieira, Omar Machado Entiauspe-Neto, Samantha Oliveira e Sousa, Tayse Farias, Alanna Grazieli Sousa, Geraldo Jorge Barbosa de Moura.
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:
Freitas MA, Vieira RS, Entiauspe-Neto OM, Sousa SO, Farias T, Souza AG, Moura GJB (2017) Herpetofauna of the Northwest Amazon forest in the state of Maranhão, Brazil, with remarks on the Gurupi Biological Reserve. ZooKeys 643: 141-155. https://doi.org/10.3897/zookeys.643.8215
|
Understanding the biodiversity of an area is the first step for establishing effective interventions for conservation, especially when it comes to herpetofauna, since 4.1% and 9.2%, respectively, of Brazilian amphibians and reptiles are endangered. The aim of this study is to identify the composition of the herpetofauna occurring in the Northwest Amazonian state of Maranhão, with a focus on the Gurupi Biological Reserve and surrounding areas. Samples were collected between May 2012 and October 2013 (18 months), through pitfall traps, time constrained active search, and opportunistic encounters, and these records were supplemented by specimens collected by third parties and by bibliographic records. A total of 131 species were recorded: 31 species of amphibians and 100 species of reptiles (six testudines, 30 lizards, two amphisbaenas, 60 snakes and two alligators), including some species new to the state of Maranhão and the northeast region of Brazil. This inventory contributes to the knowledge of the herpetofauna for the Belém Endemism Center, the most devastated region of the Brazilian Amazon, and considered poorly sampled.
Amphibians, Belém Center of Endemism, inventory, new records, reptiles
Conservation units in the Amazon (National Parks, ecological stations, extractive reserves, national forests, biological reserves, etc.) are of fundamental importance for the conservation of biodiversity in this biome (
With regard to formulating effective management plans, it is of fundamental importance for biodiversity conservation to know the composition of the fauna and flora. Faunal lists, especially in regions that represent sampling gaps and that refer to groups with a high percentage of endangered species should be emphasized (
In this context, regarding the herpetofauna, there are in Brazil 1080 known species of amphibians and 773 species of reptiles of which 4.1% and 9.2% are endangered, respectively (
Biodiversity inventories enable us to identify the degree of regional endemism, new trigger points, new species and the actual conservation status of the species recorded, besides enriching regional and national scientific collections (
It is noteworthy that species lists are highly important for our understanding of the environmental conservation, since the occurrence of bioindicator species (either opportunistic or vulnerable) can be used to determine the effects of environmental disturbance in the area, and therefore, pave a way to efficient interventions and conservation policies (
The state of Maranhão is known for its rich biodiversity (
Among the indicators of the need for wildlife studies in Maranhão are the articles of the last decades that describe new species in Amazonia, especially in the eastern Amazon (
This study aims to record the composition of amphibians and reptiles of the REBIO Gurupi and adjacent regions of the northwest Amazon of Maranhão state, a conservation unit of utmost importance, composing the largest and last block of continuous forests in the Belém Endemism Center (
Study Area: The Gurupi Biological Reserve (03°58'32"S 46°46'52"W) (Figure
Sampling: Samples were collected between May 2012 and October 2013 (18 months), with pitfall traps, time constrained active search, and opportunistic encounters in the forested areas and access roads to REBIO (road killed individuals). They also included those collected by third parties and bibliographic records.
The pitfall traps were composed of seven lines of five buckets (60 L) connected by a plastic canvas with a length of 10m, totaling 70 meters of intercept lines (Line 1: 03°59'14"S, 46°47'53"W; Line 2: 03°59'11"S, 46°47'50"W; Line 3: 03°59'05 “S, 46°47'27"W; Line 4: 03°59'06"S, 46°47'25 “W; Line 5: 03°59'07"S, 46° 47'15"W; Line 6: 03°59'03"S, 46°47'04"W; Line 7: 03°58'32"S, 46°46'52"W), each line was about 3 km distant from one another. Traps were open around the clock for five days during each sampling campaign. These were concentrated in the rainy season, December 2012, January and May 2013, totaling an effort of 5400 hours/ bucket.
The time-constrained active search was conducted over three campaigns for three nights in December 2012, January and May 2013, by a team made up of five collectors, totaling an effort of 135 man hours according to the methodologies of
The collected amphibians were euthanized by applying lidocaine ointment (lidocaine) on the ventral region and the reptiles through overdosing with ether (
Voucher specimens were deposited in the collection of Herpetology and Paleontology of the Federal Rural University of Pernambuco CHP-UFRPE (tumble numbers in Appendix
Data analysis: In order to evaluate the efficiency of the collection effort in the analyzed fragment, species rarefaction curves were constructed with 1000 randomizations generated based on the data matrix of the relationship between richness and abundance (ICE index) through the statistical program Ecosim version 7.0 (
A total of 131 species composing the local herpetofauna was recorded: 31 species of amphibians (seven families) and 100 species of reptiles, which included six testudines, 30 lizards, two amphisbaenians, 60 snakes and two crocodylians (Figure
Some amphibians and reptiles recorded in the Gurupi Biological Reserve, Maranhão, Brazil. A Adelphobates galactonotus B Phyllomedusa vaillanti C Lithodytes lineatus D Leptodactylus paraensis E Ctenophryne geayi F Platemys platicephala G Paleosuchus trigonatus H Cercosaura argulus. Photo credit of P. trigonatus (G) belong to Eloisa Mendonça and M. A. de Freitas for others.
Some amphibians and reptiles recorded in the Gurupi Biological Reserve, Maranhão, Brazil. A Leposoma percarinatum B Neusticurus bicarinatus C Coleodactylus septentrionalis D Cnemidophorus cryptus E Stenocercus dumerilii F Phrynonax poecilonotus G Rhinobothryum lentiginosum H Sibynomorphus mikanii septentrionalis I Micrurus spixii martiusi J Rhinella gildae. Photo credits of P. poecilonotus (F) belong to Eloisa Mendonça, R. lentiginosum (G) to Saymon Albuquerque and M. A. de Freitas for others.
Of the 131 species recorded for the northwest Amazon in Maranhão, 78 species (62%) were recorded in this study and 53 (38%) included results from previously published data (
The Belém Endemism Center (EC) is the smallest among the eight EC in the Amazon region, and has the largest loss of forest cover, with about 70% of its total area already destroyed (
The diversity of amphibians and reptiles of the Belém Endemism Center is very high, as in other endemic centers, especially those of the eastern Amazon region, such as the ECs Guyana, Xingu and Tapajós: 85 species of snakes further down the Amazon River, in Santarem, state of Pará at EC Tapajós (
The species richness of REBIO Gurupi is second only to the richness sampled in the National Forest of Saracá-Taquera in northern Pará, located in the Guyana Endemism Center, more than 1000 km from REBIO Gurupi (
Regarding sampling efficiency, the collection effort and methods used were not effective, as not all niches were sampled. As a result, the curve implied 33 amphibian species and 78 reptile species at the site. As the curves did not reach an asymptote, we believe that site has potential for species that have not yet been recorded. This is borne out by the additional 58 species not found during the field work but recorded in the literature for the area (
Thinning curves representing the accumulated richness of species of frogs and lizards at REBIO Gurupi. The richness was recorded by passive and active collection between December 2012 and May 2013. The center line is the average (randomizing 1000 times) and the lines on the side represent the associated standard deviation.
Since only 38% of the recorded species included in this inventory were obtained from literature (Table
Herpetofauna recorded between May 2012 and October 2013 in the Gurupi Biological Reserve, Maranhão, Brazil. (Type of record: EO = Opportunistic Encounter; BA = Constrained active search; Pitfalls = pitfall trap, DS = secondary data).
* First occurrence for the state of Maranhão and northeast Brazil.
** Species endemic to the Belém center of endemism.
FAMILY | SPECIES | TYPE OF RECORD |
---|---|---|
Bufonidae | Rhinella gildae Vaz-Silva, Maciel, Bastos & Pombal Jr, 2015** |
EO - DS ( |
Rhinella marina (Linnaeus, 1758) | EO/Pitfalls/BA | |
Craugastoridae | Pristimantis fenestratus (Steindachner, 1864) | BA |
Dendrobatidae | Adelphobates galactonotus (Steindachner, 1864)** | BA |
Hylidae | Dendropsophus marmoratus (Laurenti, 1768) | EO |
Dendropsophus cf. minusculus |
DS ( |
|
Dendropsophus nanus (Boulenger, 1889) |
DS ( |
|
Dendropsophus minutus (Peters, 1872) |
DS ( |
|
Dendropsophus rubicundulus (Reinhardt & Lütken, 1862) |
DS ( |
|
Hypsiboas boans (Linnaeus, 1758) | EO | |
Hypsiboas fasciatus (Günther, 1859 “1858”) |
DS ( |
|
Hypsiboas punctatus (Schneider, 1799) | BA | |
Hypsiboas multifasciatus (Günther, 1859) |
DS ( |
|
Osteocephalus taurinus Steindachner, 1862 | BA | |
Scinax fuscomarginatus (A. Lutz, 1925) |
DS ( |
|
Scinax nebulosus (Spix, 1824) |
DS ( |
|
Scinax ruber (Laurenti, 1768) | EO | |
Sphaenorhynchus lacteus (Daudin, 1800) | DS (Benício et al. 2011) | |
Trachycephalus typhonius (Linnaeus, 1758) | EO | |
Phyllomedusa hypochondrialis (Daudin, 1800) |
DS ( |
|
Phyllomedusa vaillantii Boulenger, 1882 * | BA (Freitas et al. 2014) | |
Leptodactylidae | Adenomera andreae (Müller, 1923) | BA/Pitfalls/EO |
Leptodactylus fuscus (Schneider, 1799) | EO | |
Leptodactylus mystaceus (Spix, 1824) | BA/Pitfalls/EO | |
Leptodactylus rhodomystax Boulenger, 1884 | ( |
|
Leptodactylus paraensis Heyer, 2005 ** - | EO | |
Leptodactylus troglodytes A. Lutz, 1926 | EO | |
Leptodactylus gr latrans |
DS ( |
|
Lithodytes lineatus (Schneider, 1799)* | (Freitas et al. 2014) | |
Leiuperidae | Physalaemus cuvieri Fitzinger, 1826 | BA/Pitfalls |
Microhylidae | Ctenophryne geayi Mocquard, 1904 * | (Freitas et al. 2014) |
Chelidae | Platemys platycephala (Schneider, 1792) * | EO |
Geoemydidae | Rhinoclemmys punctularia (Daudin, 1801) | EO |
Kinosternidae | Kinosternon scorpioides (Linnaeus, 1766) | EO |
Podocnemididae | Podocnemis unifilis Troschel, 1848 | EO |
Testudinidae | Chelonoidis carbonarius (Spix, 1824) | EO |
Chelonoidis denticulatus (Linnaeus, 1766) | EO | |
Alligatoridae | Caiman crocodilus (Linnaeus, 1758) | EO |
Paleosuchus trigonatus (Schneider, 1801) * | EO | |
Dactyloidae | Dactyloa punctata (Daudin, 1802) | BA |
Norops fuscoauratus (D’Orbigny, 1837) | BA/Pitfalls/EO | |
Norops tandai (Ávila-Pires, 1995) |
DS ( |
|
Gekkonidae | Hemidactylus mabouia (Moreau de Jonnès, 1818) | EO |
Gymnophthalmidae | Micrablepharus maximiliani (Reinhardt & Luetken, 1862) | EO |
Cercosaura argulus Peters, 1863 | ( |
|
Cercosaura ocellata Wagler, 1830 |
DS ( |
|
Colobosaura modesta (Reinhardt & Luetken, 1862) |
DS ( |
|
Arthrosaura reticulata (O’Shaughnessy, 1881) |
DS ( |
|
Leposoma percarinatum Muller, 1923 * | Pitfalls | |
Neusticurus bicarinatus (Linnaeus, 1758)** |
DS ( |
|
Iguanidae | Iguana iguana (Linnaeus, 1758) | EO |
Leiosauridae | Enyalius leechii (Boulenger, 1885) |
DS ( |
Mabuyidae | Copeoglossum nigropunctatum (Spix, 1825) | Pitfalls |
Phyllodactylidae | Thecadactylus rapicauda (Houttuyn, 1782) | EO |
Polychrotidae | Polychrus acutirostris Spix, 1825 |
DS ( |
Polychrus marmoratus (Linnaeus, 1758) | EO | |
Sphaerodactylidae | Coleodactylus septentrionalis (Vanzolini, 1980)** | Pitfalls |
Gonatodes humeralis (Guichenot, 1855) | Pitfalls/BA | |
Teiidae | Ameiva ameiva (Linnaeus, 1758) | Pitfalls/EO/BA |
Cnemidophorus cryptus Cole & Dessauer, 1993 * | EO | |
Kentropyx calcarata Spix, 1825 | Pitfalls/BA | |
Salvator merianae (Duméril & Bibron, 1839) | EO/BA | |
Tupinambis teguixin (Linnaeus, 1758) |
DS ( |
|
Dracaena guianensis Daudin, 1801 |
DS ( |
|
Tropiduridae | Plica umbra (Linnaeus, 1758) | Pitfalls |
Stenocercus dumerilii (Steindachner, 1867)** | Pitfalls | |
Tropidurus hispidus (Spix, 1825) | EO/BA | |
Uracentron azureum (Linnaeus, 1758) |
DS ( |
|
Uranoscodon superciliosus (Linnaeus, 1758) | BA | |
Amphisbaenidae | Amphisbaena alba Linnaeus, 1758 |
DS ( |
Amphisbaena amazonica Vanzolini, 1951 | EO | |
Typhlopidae | Amerotyphlops brongersmianus (Vanzolini, 1976) | Pitfalls |
Aniliidae | Anilius scytale (Linnaeus, 1758) | EO |
Boidae | Boa constrictor Linnaeus, 1758 | EO |
Corallus hortulanus (Linnaeus, 1758) | EO | |
Epicrates cenchria (Linnaeus, 1758) | EO | |
Eunectes murinus (Linnaeus, 1758) |
DS ( |
|
Colubridae | Chironius carinatus (Linnaeus, 1758) | EO |
Chironius exoletus (Linnaeus, 1758) | EO | |
Chironius fuscus (Linnaeus, 1758) |
DS ( |
|
Chironius multiventris Schmidt & Walker, 1943 |
DS ( |
|
Chironius scurrulus (Wagler in Spix, 1824) |
DS ( |
|
Drymarchon corais (Boie, 1827) | EO | |
Drymoluber dichrous (Peters, 1863) |
DS ( |
|
Leptophis ahaetulla (Linnaeus, 1758) | EO | |
Mastigodryas bifossatus (Raddi, 1820) |
DS ( |
|
Colubridae | Mastigodryas boddaerti (Sentzen, 1796) | EO |
Oxybelis aeneus (Wagler in Spix, 1824) |
DS ( |
|
Oxybelis fulgidus (Daudin, 1803) | EO | |
Phrynonax poecilonotus (Peters, 1867)* | EO | |
Rhinobothryum lentiginosum (Scopoli, 1785) * | EO | |
Spilotes pullatus (Linnaeus, 1758) | EO | |
Tantilla melanocephala (Linnaeus, 1758) | Pitfalls | |
Dipsadidae | Atractus alphonsehogei Cunha & Nascimento, 1983 |
DS (Cunha and Nascimento 1983) |
Atractus schach (Boie, 1827) |
DS ( |
|
Atractus snethlageae Cunha & Nascimento, 1983 |
DS ( |
|
Dipsas catesbyi (Sentzen, 1796) | EO | |
Dipsas variegata (Duméril, Bibron & Duméril, 1854) |
DS ( |
|
Erythrolamprus aesculapii (Linnaeus, 1766) |
DS ( |
|
Erythrolamprus cobella (Linnaeus, 1758) |
DS ( |
|
Erythrolamprus miliaris chrysostomus (Griffin, 1916) |
DS ( |
|
Erythrolamprus oligolepis (Boulenger, 1905) |
DS ( |
|
Erythrolamprus poecilogyrus (Wied, 1825) | EO | |
Sibon nebulatus (Linnaeus, 1758) |
DS ( |
|
Sibynomorphus mikanii septentrionalis Cunha, Nascimento & Hoge, 1980 ** | EO (Freitas et al. 2014) | |
Imantodes cenchoa (Linnaeus, 1758) |
DS ( |
|
Leptodeira annulata (Linnaeus, 1758) | EO/BA | |
Helicops angulatus (Linnaeus, 1758) |
DS ( |
|
Hydrops martii (Wagler in Spix, 1824) |
DS ( |
|
Pseudoeryx plicatilis (Linnaeus, 1758) |
DS ( |
|
Philodryas olfersii (Liechtenstein, 1823) | EO | |
Philodryas viridissima (Linnaeus, 1758) | EO | |
Clelia plumbea (Wied, 1820) | EO | |
Oxyrhopus melanogenys Cunha & Nascimento, 1983 | BA | |
Oxyrhopus petolarius (Reuss, 1834) | EO | |
Pseudoboa coronata Schneider, 1801 |
DS ( |
|
Pseudoboa neuwiedii (Duméril, Bibron & Duméril, 1854) | EO | |
Pseudoboa nigra (Duméril, Bibron & Duméril, 1854) | EO | |
Siphlophis cervinus (Laurenti, 1768) |
DS ( |
|
Taeniophallus quadriocellatus Santos-Jr, Di-Bernardo & Lema, 2008 |
DS ( |
|
Dipsadidae | Xenodon merremii (Wagler in Spix, 1824) | EO |
Xenodon severus (Linnaeus, 1758) |
DS ( |
|
Elapidae | Micrurus filiformis (Günther, 1859) |
DS ( |
Micrurus hemprichii (Jan, 1858) |
DS ( |
|
Micrurus lemniscatus lemniscatus (Linnaeus, 1758) |
DS ( |
|
Micrurus spixii martiusi Schmidt, 1953 ** | BA | |
Micrurus surinamensis (Cuvier, 1817) |
DS ( |
|
Viperidae | Bothrops atrox (Linnaeus, 1758) | BA/EO |
Bothrops brazili Hoge, 1954 |
DS ( |
|
Bothrops taeniatus Wagler in Spix, 1824 |
DS ( |
|
Lachesis muta (Linnaeus, 1766) |
DS ( |
We thank the colleagues who supported the field activities, particularly the head of the Gurupi Biological Reserve, Evane Alves Lisboa for her support with housing, fuel, and vehicles used in the research. We are also deeply indebted to Anne Taffin d’Heursel Baldisseri for conducting an English grammar revision. We also thank Eloisa Mendonça for a few photographic records and for supporting the team in the field. Saymon Albuquerque is thanked for photographic records and Diego Mendes for building the map. This research was carried out under collecting license SISBIO/ ICMBio 36669-1. We also thank four anonymous reviewers and the editor Aaron Bauer for valuable comments on the manuscript.
Specimens examined
Rhinella marinaCHP-UFRPE 1810 – Rhinella gildaeCHP-UFRPE 1848 Leptodactylus paraensisCHP-UFRPE 1811-1845 – Leptodactylus petersii