Herpetofauna of the Northwest Amazon forest in the state of Maranhão, Brazil, with remarks on the Gurupi Biological Reserve.

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.

Introduction

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 (Peres 2005; Silva 2005).

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 (Peres 2005).

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 (Costa and Bérnils 2015; Segalla et al. 2016).

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 (Moura et al. 2014).

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 (Brown and Freitas 2002).

The state of Maranhão is known for its rich biodiversity (Martins and Oliveira 2011), lack of researchers and extensive sampling gaps, especially regarding the herpetofauna in the Amazon biome of northwestern Maranhão.

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 (Caramaschi 2010; Vaz-Silva et al. 2015), as well as the few publications, concentrated mainly on snakes (Cunha and Nascimento 1993; Freitas et al. 2014), lizards (Avila-Pires and Vitt 1998; Avila-Pires 1995; Freitas et al. 2013) and anurans (Andrade et al. 2003; Rodrigues et al. 2003; Andrade et al. 2011; Barreto et al. 2011; Miranda et al. 2012; Miranda et al. 2013; Matavelli et al. 2013; Freitas et al. 2014b, c, d; Vaz-Silva et al. 2015).

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 (Martins and Oliveira 2011).

Materials and methods

Study Area: The Gurupi Biological Reserve () (Figure 1), was created by Law 95 614 1988 and occupies an original area of 341,650 hectares in the municipalities of Bom Jardim, Centro Novo do Maranhão and São João do Caru, in the state of Maranhão (IBAMA 2006). The climate is humid type B2, with moderate water deficit in the summer, average annual rainfall exceeding 2,000 and average temperature greater than 24°C, with the soil type being argisoil (Martins and Oliveira 2011). This work was performed and focused only in Gurupi and the adjacent rainforests of the State of Maranhão, northwest Amazon.

Figure 1.

Map with the location of the study area, in the Gurupi Biological Reserve, Maranhão, Brazil.

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: ; Line 2: ; Line 3: ; Line 4: ; Line 5: ; Line 6: ; Line 7: ), 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 Martins and Oliveira (1998), and Bernarde and Abe (2006). The search was concentrated in the area adjacent to aquatic environments near the southern tip of REBIO Gurupi ().

The collected amphibians were euthanized by applying lidocaine ointment (lidocaine) on the ventral region and the reptiles through overdosing with ether (Callefo 2002; Franco and Salomão 2002). All specimens were fixed with 10% formalin and then preserved in 70% ethanol.

Voucher specimens were deposited in the collection of (tumble numbers in Appendix 1) and the (tumble numbers in Appendix 1). Important bibliographic databases added to this work were Cunha and Nascimento (1993) for snakes, Avila-Pires (1995) for lizards and Barreto et al. (2011) for amphibians and reptiles.

Herpetology and Paleontology of the Federal Rural University of Pernambuco

University of São Paulo Museum of Zoology

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 (Gotelli and Enstminger 2003).

Results

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 3, 4).

Figure 3.

Some amphibians and reptiles recorded in the Gurupi Biological Reserve, Maranhão, Brazil. A B C D E F G H . Photo credit of (G) belong to Eloisa Mendonça and M. A. de Freitas for others.

Figure 4.

Some amphibians and reptiles recorded in the Gurupi Biological Reserve, Maranhão, Brazil. A B C D E F G H I J . Photo credits of (F) belong to Eloisa Mendonça, (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 (Cunha and Nascimento 1993; Avila-Pires 1995; Barreto et al. 2011).

Discussion

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 (Silva et al. 2005; Fearnside 2006).

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 (Frota et al. 2005); 62 species of amphibians and reptiles in the Biological Reserve Tapirape, also at Pará, in the EC Xingu (Bernardo et al. 2012); 71 species of amphibians in the National Forest of Carajás, also at the EC Xingu (Pinheiro et al. 2012); 175 species of amphibians and reptiles in the National Forest of Saracá-Taquera, in theEC Guiana at Pará (Morato et al. 2014.); 53 species of snakes for the National Forest of Caxiuanã (at the EC Xingu (Santos-Costa et al. 2015); 78 species of amphibians and reptiles in the northern part of the state of PageBreakPageBreakPageBreakPageBreakPageBreakPageBreakMaranhão (Barreto et al. 2011). It is noteworthy that the last of these studies includes species of open areas, which are present due to the strong influence of Cerrado vegetation in northern Maranhão, as seen in the inventory of Miranda et al. (2012), which lists 42 species of reptiles for the coastal region of Maranhão, which is characterized by open vegetation and the predominance of coastal dunes.

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 (Morato et al. 2014).

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 (Cunha and Nascimento 1993; Avila-Pires 1995; Barreto et al. 2011) (Figure 2). Regarding collection methods, pitfall traps yielded only 33 species of the 78 found in the field, chiefly amphibians, frogs, and fossorial lizards.

Figure 2.

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.

Conclusion

Since only 38% of the recorded species included in this inventory were obtained from literature (Table 1), it is possible to ascertain that our sampling reflects a great share of the total herpetofauna from Northwestern Maranhão. With this richness, the Gurupi Biological Reserve stands out as a biodiversity hotspot in the Amazon, reinforcing the need for its protection, and its position as the most important restricted use conservation unit of the Belém Endemism Center.

Table 1.

Herpetofauna recorded between May 2012 and October 2013 in the Gurupi Biological Reserve, Maranhão, Brazil. (Type of record: EO; BA; Pitfalls, DS).

= Opportunistic Encounter

= Constrained active search

= pitfall trap

= 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 (Vaz-Silva et al. 2015)
	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 (Barreto et al. 2011)
	Dendropsophus nanus (Boulenger, 1889)	DS (Barreto et al. 2011)
	Dendropsophus minutus (Peters, 1872)	DS (Barreto et al. 2011)
	Dendropsophus rubicundulus (Reinhardt & Lütken, 1862)	DS (Barreto et al. 2011)
	Hypsiboas boans (Linnaeus, 1758)	EO
	Hypsiboas fasciatus (Günther, 1859 “1858”)	DS (Barreto et al. 2011)
	Hypsiboas punctatus (Schneider, 1799)	BA
	Hypsiboas multifasciatus (Günther, 1859)	DS (Barreto et al. 2011)
	Osteocephalus taurinus Steindachner, 1862	BA
	Scinax fuscomarginatus (A. Lutz, 1925)	DS (Barreto et al. 2011)
	Scinax nebulosus (Spix, 1824)	DS (Barreto et al. 2011)
	Scinax ruber (Laurenti, 1768)	EO
	Sphaenorhynchus lacteus (Daudin, 1800)	DS (Benício et al. 2011)
	Trachycephalus typhonius (Linnaeus, 1758)	EO
	Phyllomedusa hypochondrialis (Daudin, 1800)	DS (Barreto et al. 2011)
	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	(Sá et al. 2014)
	Leptodactylus paraensis Heyer, 2005 ** -	EO
	Leptodactylus troglodytes A. Lutz, 1926	EO
	Leptodactylus gr latrans	DS (Barreto et al. 2011)
	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 (Ávila-Pires 1995)
Gekkonidae	Hemidactylus mabouia (Moreau de Jonnès, 1818)	EO
Gymnophthalmidae	Micrablepharus maximiliani (Reinhardt & Luetken, 1862)	EO
	Cercosaura argulus Peters, 1863	(Freitas et al. 2013)
	Cercosaura ocellata Wagler, 1830	DS (Ávila-Pires 1995)
	Colobosaura modesta (Reinhardt & Luetken, 1862)	DS (Ávila-Pires 1995)
	Arthrosaura reticulata (O’Shaughnessy, 1881)	DS (Ávila-Pires 1995)
	Leposoma percarinatum Muller, 1923 *	Pitfalls
	Neusticurus bicarinatus (Linnaeus, 1758)**	DS (Ávila-Pires 1995)
Iguanidae	Iguana iguana (Linnaeus, 1758)	EO
Leiosauridae	Enyalius leechii (Boulenger, 1885)	DS (Ávila-Pires 1995)
Mabuyidae	Copeoglossum nigropunctatum (Spix, 1825)	Pitfalls
Phyllodactylidae	Thecadactylus rapicauda (Houttuyn, 1782)	EO
Polychrotidae	Polychrus acutirostris Spix, 1825	DS (Ávila-Pires 1995)
	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 (Ávila-Pires 1995)
	Dracaena guianensis Daudin, 1801	DS (Ávila-Pires 1995)
Tropiduridae	Plica umbra (Linnaeus, 1758)	Pitfalls
	Stenocercus dumerilii (Steindachner, 1867)**	Pitfalls
	Tropidurus hispidus (Spix, 1825)	EO/BA
	Uracentron azureum (Linnaeus, 1758)	DS (Ávila-Pires 1995)
	Uranoscodon superciliosus (Linnaeus, 1758)	BA
Amphisbaenidae	Amphisbaena alba Linnaeus, 1758	DS (Barreto et al. 2011)
	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 (Cunha and Nascimento 1993)
Colubridae	Chironius carinatus (Linnaeus, 1758)	EO
	Chironius exoletus (Linnaeus, 1758)	EO
	Chironius fuscus (Linnaeus, 1758)	DS (Cunha and Nascimento 1993)
	Chironius multiventris Schmidt & Walker, 1943	DS (Cunha and Nascimento 1993)
	Chironius scurrulus (Wagler in Spix, 1824)	DS (Cunha and Nascimento 1993)
	Drymarchon corais (Boie, 1827)	EO
	Drymoluber dichrous (Peters, 1863)	DS (Cunha and Nascimento 1993)
	Leptophis ahaetulla (Linnaeus, 1758)	EO
	Mastigodryas bifossatus (Raddi, 1820)	DS (Cunha and Nascimento 1993)
Colubridae	Mastigodryas boddaerti (Sentzen, 1796)	EO
	Oxybelis aeneus (Wagler in Spix, 1824)	DS (Barreto et al. 2011)
	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 (Cunha and Nascimento 1993)
	Atractus snethlageae Cunha & Nascimento, 1983	DS (Cunha and Nascimento 1993)
	Dipsas catesbyi (Sentzen, 1796)	EO
	Dipsas variegata (Duméril, Bibron & Duméril, 1854)	DS (Cunha and Nascimento 1993)
	Erythrolamprus aesculapii (Linnaeus, 1766)	DS (Cunha and Nascimento 1993)
	Erythrolamprus cobella (Linnaeus, 1758)	DS (Cunha and Nascimento 1993)
	Erythrolamprus miliaris chrysostomus (Griffin, 1916)	DS (Cunha and Nascimento 1993)
	Erythrolamprus oligolepis (Boulenger, 1905)	DS (Cunha and Nascimento 1993)
	Erythrolamprus poecilogyrus (Wied, 1825)	EO
	Sibon nebulatus (Linnaeus, 1758)	DS (Cunha and Nascimento 1993)
	Sibynomorphus mikanii septentrionalis Cunha, Nascimento & Hoge, 1980 **	EO (Freitas et al. 2014)
	Imantodes cenchoa (Linnaeus, 1758)	DS (Cunha and Nascimento 1993)
	Leptodeira annulata (Linnaeus, 1758)	EO/BA
	Helicops angulatus (Linnaeus, 1758)	DS (Barreto et al. 2011)
	Hydrops martii (Wagler in Spix, 1824)	DS (Cunha and Nascimento 1993)
	Pseudoeryx plicatilis (Linnaeus, 1758)	DS (Cunha and Nascimento 1993)
	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 (Cunha and Nascimento 1993)
	Pseudoboa neuwiedii (Duméril, Bibron & Duméril, 1854)	EO
	Pseudoboa nigra (Duméril, Bibron & Duméril, 1854)	EO
	Siphlophis cervinus (Laurenti, 1768)	DS (Cunha and Nascimento 1993)
	Taeniophallus quadriocellatus Santos-Jr, Di-Bernardo & Lema, 2008	DS (Cunha and Nascimento 1993)
Dipsadidae	Xenodon merremii (Wagler in Spix, 1824)	EO
	Xenodon severus (Linnaeus, 1758)	DS (Cunha and Nascimento 1993)
Elapidae	Micrurus filiformis (Günther, 1859)	DS (Cunha and Nascimento 1993)
	Micrurus hemprichii (Jan, 1858)	DS (Cunha and Nascimento 1993)
	Micrurus lemniscatus lemniscatus (Linnaeus, 1758)	DS (Cunha and Nascimento 1993)
	Micrurus spixii martiusi Schmidt, 1953 **	BA
	Micrurus surinamensis (Cuvier, 1817)	DS (Cunha and Nascimento 1993)
Viperidae	Bothrops atrox (Linnaeus, 1758)	BA/EO
	Bothrops brazili Hoge, 1954	DS (Cunha and Nascimento 1993)
	Bothrops taeniatus Wagler in Spix, 1824	DS (Cunha and Nascimento 1993)
	Lachesis muta (Linnaeus, 1766)	DS (Cunha and Nascimento 1993)