Snakes of the Pernambuco Endemism Center, Brazil: diversity, natural history and conservation

Abstract The Atlantic Forest is one of the largest and richest tropical rainforests on the planet, being one of the 25 world priorities for conservation. The Atlantic Forest portion located north of the São Francisco River corresponds to the Pernambuco Endemism Center (PEC). We describe the snake composition of the PEC, providing information about the diversity, natural history and geographical distribution of the species, based on records from five scientific collections and additional information from the literature. A total of 78 species of snakes distributed in eight families was registered in the Pernambuco Endemism Center. The Caatinga is the Brazilian biome that most shares species with the PEC, followed by Cerrado. On the other hand, seven species are considered endemic of this region. Most of the snake species in the PEC have been registered in forest (94.8%), followed by “Brejos Nordestinos” (46.1%), Tabuleiros (43.5%), Restingas (14.1%) and Mangroves (5.1%). The PEC snake fauna includes mainly terrestrial species (60.2%) and cryptozoic and/or fossorial species (21.7%), but also presents a high richness of semi-arboreal and arboreal species (29.5%). Vertebrates are the main food item consumed by the species (78% of species), among the main prey are mammals, lizards, and amphibians. Most species show a strictly nocturnal activity period (50%), followed by strictly diurnal (38%). The PEC is the most degraded and least known region of the Atlantic Forest, yet it has revealed a high richness of snake species, including seven endemic species. It is emphasized that regional conservation efforts need to be intensified, because few forests in the region are formally protected, and the majority consist of small and poorly protected fragments, which means that many species in the region may be in risk of extinction.


Introduction
The Atlantic Forest is considered one of the 25 priority areas for conservation worldwide (Myers et al. 2000). This biome was one of the largest tropical forests in the Americas, originally covering 150 million hectares along the Brazilian coast and parts of Paraguay and Argentina (Silva and Casteleti 2003). Today, the Atlantic Forest has been reduced to less than 12% of its original coverage (Ribeiro et al. 2009). Even having suffered an extensive fragmentation since long time ago, the Atlantic Forest still presents a great biodiversity, housing one of the highest percentages of endemic species in the world (Morellato and Haddad 2000).
Although practically the entire Brazilian coast was occupied by European colonization, it was in the northeast that the Atlantic Forest was more rapidly degraded, due to the economic cycle of brazilwood and sugar cane (Coimbra-Filho and Câmara 1996). This degradation is even more evident in the portion of the Atlantic Forest located north of the São Francisco River, where an important center of endemism is located in South America -The Pernambuco Endemism Center (hereafter PEC) (Prance 1982, Silva andCasteleti 2003). In this region, sugar cane is the main agricultural crop and other anthropic actions, such as animal and plant extractivism, have contributed to the reduction of biodiversity in the PEC (Coimbra-Filho and Câmara 1996, 2006a. In the midst of this scenario, the PEC is considered the most devastated, least known and least protected sector of the Atlantic Forest, being one of the regions on the planet where conservation efforts are most urgent (Coimbra-Filho and Câmara 1996. Among reptiles, snakes are the group that currently presents the most underestimated risks of extinction, due to the scarcity of information on the natural history of most species, mainly because they have long periods of inactivity, are difficult to observe and live in low population densities (Seigel 1993). Although some studies carried out on Atlantic forest remnants of the PEC have provided important information about snakes in this region (e.g. Moura et al. 2011, Pereira Filho and Montingelli 2011, Roberto et al. 2012, 2015, Pereira Filho et al. 2017, Sampaio et al. 2018, Freitas et al. 2019a, the knowledge about the diversity, distribution and natural history of PEC snake species remains scarce and fragmented. In this direction, scientific collections perform a fundamental role in obtaining information that is the basis for the description of new species, biodiversity inventories and identification of endemism areas (Rocha et al. 2014).
Herein, we describe the snake composition at the Pernambuco Endemism Center, providing information about the diversity, natural history and geographical distribution of the species, based on records from scientific collections and additional information from the literature.

Study area
The study area comprises the Atlantic Forest located north of the São Francisco River, which corresponds to the Pernambuco Endemism Center (PEC) (Fig. 1) (Prance 1982, Silva andCasteleti 2003), located between the states of Alagoas and Rio Grande do Norte. This region has a humid tropical climate (Köppen's As'), with autumn-winter rains and rainfall ranging from 750 to 1500 mm per year (Tabarelli et al. 2006a).
The PEC region is composed by different native forest formations and ecosystems associated with the Atlantic Forest domain. A mosaic of ombrophilous and semi-deciduous forests is present in this region (Tabarelli et al. 2006a). Also, PEC comprises the "Brejos de Altitude" or "Brejos Nordestinos", which are "islands" of humid forests established in the semi-arid region, surrounded by Caatinga vegeta- tion (Andrade-Lima 1982). Although the vegetation of the PEC is composed mainly of humid tropical forests, we can also find open physiognomies along the coast, which are called "Restingas", and in the interior, which are called "Tabuleiros". The restingas are formed by strips of beaches and dunes covered by herbaceous and shrubby vegetation (Araujo 1992). The Tabuleiros are considered natural enclaves of savannah, characterized by herbaceous vegetation, with scattered trees and shrubs or grouped in patches that are structurally similar to the coastal restingas, but without the marine influence (Andrade-Lima 1982). On the coast along the PEC, we can also find areas of mangroves, with a diversified aggregation of trees and shrubs that form the dominant plant communities in saline solution of the tides (Tabarelli et al. 2006b).
According to Uchoa Neto and Tabarelli (2002), the PEC presents the largest amount of remaining area of Atlantic Forest in the state of Pernambuco (1,363.23 km²), followed by the states of Alagoas (807.95 km²), Rio Grande do Norte (567.67 km²) and Paraíba (566.09 km²).

Data collection
The data presented here is the result of verification of 3,118 snake specimens deposited in five scientific collections (Coleção Herpetológica da Universidade Federal da Paraíba -UFPB; Coleção do Laboratório de Anfíbios e Répteis da Universidade Federal do Rio Grande do Norte -CLAR; Coleção Herpetológica do Museu de História Natural da Universidade Federal de Alagoas -MUFAL; Coleção Herpetológica da Universidade Federal Rural de Pernambuco -CHUFRPE; Coleção Herpetológica da Universidade Federal de Pernambuco -CHUFPE) and literature data.
The information on the distribution and occurrence of species in each environment were obtained through the records of the scientific collections and literature data, and was subsequently georeferenced. We include records of occurrence of species in the literature only when we were able to confirm the record by direct observation, photo or through museum records or documented vouchers. Information on diet, habitat use, and litter size of the species was obtained from personal data, records of scientific collections and literature data. We categorized the snake size considering the mean body size of each species based on published data as small (< 500mm), moderate (501-1000mm) and large (> 1001mm).
In this work, we have differentiated the habitats of the species into five vegetation physiognomies found in this region: Forests (when the species were found in areas with a typical forest physiognomy, with a large vegetation cover, reaching 35 meters high in the canopy, presenting epiphytes, lianas and bromeliads); Coastal Restingas; Mangroves; Tabuleiros; Brejos Nordestinos (remnants of humid forests scattered in the Caatinga) (Fig. 2); and urban areas. In addition, we compared the snake fauna found in the PEC with these of five other natural ecoregions in Brazil (Amazon, Caatinga, Cerrado, Pampas, and Pantanal). These regions are divided on the basis of geomorphology, climate, and vegetation (IBGE 2004).

Taxonomic considerations
The species Caaeteboia sp. found in the PEC, differs from Caaeteboia amarali (at present the only representative of the genus) mainly because it presents 15 rows of dorsal scales without reduction, while C. amarali presents 17 rows of dorsal scales without reduction. In addition, there is a strong variation between the number of ventral and subcaudal scales between the two species (Pereira Filho et al. 2017). We decided to use the name Micrurus ibiboboca according to Silva Jr (2016). Although Silva Jr (2016) affirms that M. ibiboboca may be a species complex throughout the distribution of the species, the author still maintains the proper name. Thus, the species designated here as M. ibiboboca is the same mentioned in previous works as Micrurus aff. ibiboboca (e.g. França et al. 2012.

Results
We registered a total of 78 species of snakes of eight families, distributed in the PEC (Table 1, Figs 3-7). The most species rich family was Dipsadidae (47 species, 60% of total), followed by Colubridae (12 species, 15.4%), Viperidae (6 species, 7.7%), Boidae and Typhlopidae, both with four species (5.1%), Elapidae (3 species, 3.8 %) and Anomalepididae and Leptotyphlopidae, both with a single species (1.3%).   cies were found in four different habitats and 31 species were found only in one habitat type (Table 1). Of these, 26 species were collected only in forested areas, three species only in the Brejos Nordestinos and one species was found only in restingas (Table 1). The majority of snake species found in the PEC use the soil as substrate, of which 47 species (60.2%) are terrestrial and 17 (21.7%) are cryptozoic and/or fossorial. In addition, 23 species are arboreal or semi-arboreal (29.5%) and 16 (20.5%) are aquatic or semi-aquatic. The diet of PEC snakes consists mainly of vertebrates (61 species, 78.2%), of which 23 species are considered generalists, feeding on three or more types of prey, 21 species feed on two types of prey, 23 species are specialists in amphibians, two species are specialists in snakes and two species are specialists in mammals. Only 14 species feed on invertebrates, of which six species feed on arthropods, three species feed on annelids and five species feed on mollusks ( Table 1). As for the period of activity, 39 (50 %) species are nocturnal, 30 (38.4%) species are diurnal and nine (11.5%) species are diurnal and nocturnal (Table 1).
We present below a commented list of species of snakes that occur in PEC, with notes on natural history and distribution. The "N" corresponds to the number of individuals analyzed in the scientific collections. The species L. trefauti, A. caete, A. potschi, E. cephalomaculata, E. cephalostriata, T. almae, T. hypoconia, and T. phoenix were recorded only by literature data.
Epicrates cenchria (Linnaeus, 1758) -A large semi-arboreal or terrestrial species (average SVL = 1105 mm; N = 6), with nocturnal activity . It has a wide distribution, occurring in the Atlantic Forest, Amazon Forest, Cerrado and Pantanal , 2015, Passos and Fernandes 2008. In the PEC it occurs in the states of Alagoas and Pernambuco (Fig. 8C), being found in Forest areas, but also in urban areas. Epicrates cenchria feeds on mammals, birds, lizards and amphibians Oliveira 1998, Pizzatto et al. 2010). Its litter can range from 8 to 25 hatchlings (Pizzatto and Marques 2007).

Family Colubridae Oppel, 1811
Chironius carinatus (Linnaeus, 1758) -A large terrestrial and arboreal species (average SVL = 1001 mm; N = 15), with diurnal activity . It has a disjunct distribution, occurring in the Amazon Forest and Atlantic Forest (Araújo et al. 2019). In the PEC it occurs in the states of Alagoas, Pernambuco and Paraíba (Fig. 8D), being found in Forest and urban areas when these are close to forests (Araújo et al. 2019). Chironius carinatus feeds on amphibians, birds, lizards and mammals (Dixon et al. 1993, Silva et al. 2010. Its litter can have 5 to 12 eggs (Dixon et al. 1993, Goldberg 2007.
Atractus maculatus (Günther, 1858) -A small-sized fossorial and cryptozoic species (average SVL = 326 mm; N = 5), with nocturnal activity . This species occurs in the Atlantic Forest and Caatinga (Passos et al. 2010, Abegg et al. 2017a). In the PEC it occurs in the states of Alagoas and Pernambuco (Fig. 9B), being found in Forest and urban areas, when close to forests. Atractus maculatus feeds mostly on earthworms (Passos et al. 2010).
Caaeteboia sp. -A small to moderate-sized terrestrial species (average SVL = 411 mm; N = 2), with diurnal activity (personal observation). This species is endemic to the PEC and occurs only in the states of Pernambuco and Paraíba (Fig. 9C), being found in Forest.
Dipsas sazimai Fernandes, Marques & Argôlo, 2010 -A small-sized arboreal and terrestrial species (average SVL = 299 mm; N = 1), with nocturnal activity . This species occurs in the Atlantic Forest and Caatinga ). In the PEC it occurs in the states of Alagoas and Pernambuco (Fig.  9E), being found in Forest. Dipsas sazimai feeds on mollusks .
Dipsas variegata (Duméril, Bibron & Duméril, 1854) -A small to moderate size arboreal and terrestrial species (average SVL = 464 mm; N = 4), with nocturnal activity . This species occurs in the Atlantic Forest and Amazon Forest Nascimento 1993, Marques et al. 2019). In the PEC it occurs only in the state of Alagoas (Fig. 9E), being found in Forest. Dipsas variegata feeds on mollusks .
Echinanthera cephalomaculata Di Bernardo, 1994 -A small to moderate size terrestrial species (average SVL = 297 mm, N = 2), with diurnal activity (Di-Bernardo 1994, Marques et al. 2019). This species is endemic to the PEC and occurs only in the states of Alagoas and Pernambuco (Fig. 9F), being found in Forest , Freitas et al. 2019b. Echinanthera cephalomaculata feeds on amphibians .
Echinanthera cephalostriata Di Bernardo, 1996 -A moderate-sized terrestrial species, with diurnal activity (Di-Bernardo 1996, Marques et al. 2019). This species only occurs in the Atlantic Forest . In the PEC it occurs in the state of Alagoas (Fig. 9F), being found only in the Reserva Biológica de Pedra Talhada . In the report of this species for the PEC Roberto et al. (2015) provide a photo and a voucher (URCA-H 4103). Echinanthera cephalostriata feeds on amphibians ).
Erythrolamprus aesculapii (Linnaeus, 1758) -A moderate-sized terrestrial species (average SVL = 562 mm; N = 7), with diurnal activity . This species occurs in the Atlantic Forest, Amazon forest, Caatinga, Cerrado and Pantanal (Cunha and Nascimento 1993, 2015. In the PEC it occurs in the states of Alagoas and Pernambuco (Fig. 9G), being found in Forest and urban areas. Erythrolamprus aesculapii feeds on snakes and lizards (Marques and Puorto 1992). Its litter can range from 1 to 8 eggs (Marques 1996a).
Erythrolamprus almadensis (Wagler, 1824) -A small-sized semi-aquatic species (average SVL = 298 mm; N = 4), with diurnal activity . This species has a wide distribution, occurring in the Atlantic Forest, Amazon forest, Caatinga, Cerrado, Pantanal and Pampas (Dixon 1989, França et al. 2006). In the PEC it occurs in the states of Paraíba and Rio Grande do Norte (Fig. 9G) Erythrolamprus miliaris (Linnaeus, 1758) -A small-sized semi-aquatic species (average SVL = 382 mm; N = 7), with diurnal and nocturnal activity . This species occurs in the Atlantic Forest, Amazon forest, Caatinga and Cerrado (Cunha and Nascimento 1993, Nogueira et al. 2010, Marques et al. 2017a. In the PEC it occurs in the states of Alagoas, Pernambuco and Paraíba (Fig. 9G), being found in Forest and Brejos Nordestinos. Erythrolamprus miliaris feeds on amphibians and fish . Its litter can range from 1 to 30 eggs (Pizzatto and Marques 2006).
Erythrolamprus poecilogyrus (Wied-Neuwied, 1825) -A small-sized terrestrial species (average SVL = 313 mm; N = 35), with diurnal and nocturnal activity . This species occurs in the Atlantic Forest, Caatinga, Cerrado, Pantanal and Pampas , 2015). In the PEC it occurs in all states (Fig. 9H), being found in Forest, Brejos Nordestinos, Mangroves, Tabuleiros and urban areas , Pereira Filho et al. 2017. Erythrolamprus poecilogyrus feeds on amphibians and lizards (Prieto et al. 2012). Its litter can range from 3 to 17 eggs (Vitt andVangilder 1983, Mesquita et al. 2009). In Figure 4N we show a juvenile that is in the process of changing its coloration to the adult stage. This species has a different color pattern in the region (Pereira Filho et al. 2017) if compared to other populations located more southwards.
Thamnodynastes almae Franco & Ferreira, 2003 -A moderate-sized arboreal and terrestrial, with nocturnal activity Ferreira 2002, Marques et al. 2019). This species occurs in the Atlantic Forest and Caatinga . In the PEC it occurs only in Brejos Nordestinos in the state of Pernambuco (Fig. 10I) (Freitas et al. 2019a). Thamnodynastes almae feeds on amphibians and lizards (Marques et al. 2017a).
Xenodon rabdocephalus (Wied-Neuwied, 1824) -A moderate-sized terrestrial species (average SVL = 630 mm; N = 2), with diurnal activity . This species occurs in the Atlantic Forest, Amazon Forest and Cerrado (Cunha and Nascimento 1993. In the PEC it occurs in the states of Alagoas and Pernambuco (Fig. 11A), being found in Forest. Xenodon rabdocephalus feeds on amphibians (Martins and Oliveira 1998). Its litter can range from 6 to 8 eggs (Martins and Oliveira 1998).
Xenopholis scalaris (Wucherer, 1861) -A small-sized terrestrial species (average SVL = 167 mm; N = 10), with nocturnal activity . This species occurs in the Atlantic Forest and Amazon Forest . In the PEC it occurs in the states of Alagoas and Pernambuco (Fig. 11B), being found in Forest. Xenopholis scalaris feeds on amphibians Oliveira 1998, Bernarde andAbe 2010). Its litter can range from 2 to 3 eggs (Martins and Oliveira 1998).
Amerotyphlops paucisquamus (Dixon, 1979) -A small-sized fossorial species (average SVL = 133 mm; N =153), with nocturnal activity . This species is endemic to the PEC, occurring in all states (Fig. 11F), being found in Forest and Tabuleiros , Pereira Filho et al. 2017. We found four eggs in one female and another individual laid three eggs after being collected.

Discussion
Our results show a broad view of PEC's snake fauna, including distribution data, natural history, and diversity. According to Marques et al. (2019), about 142 species of snakes occur in the Brazilian Atlantic Forest, the 78 species recorded in the PEC represent 51.3% of this total, which we can consider a high richness. In addition, new species are still being discovered in this region, for example, the species D. atlantica (Freire et al. 2010), M. potyguara (Pires et al. 2014), and A. arenensis (Graboski et al. 2015) have been described in the last ten years and at least one new species (Caaeteboia sp.) is being described at the moment (Pereira Filho et al. 2017).
The mixed composition of snake species that inhabit the Atlantic Forest located north of the São Francisco River can be considered a remarkable characteristic of this fauna (Pereira Filho et al. 2017). We can highlight that the main difference between the PEC and other portions of the biome is due to the large number of species of open areas and also of wide distribution that are present in this region. The PEC shares more species with the Caatinga and the Cerrado (74.3% and 56.4% of the shared species, respectively) than with the southern and southeastern regions of the Atlantic Forest (30% of the species are shared). This may be due to the fact that the PEC presents different physiognomic features, such as patches of Tabuleiros, which are natural enclaves of savannah found even in the middle of forests and which may provide adequate conditions for the establishment of populations of species from open areas ). In addition, the proximity to the Caatinga may also have favoured the penetration and establishment of these populations (Pereira Filho et al. 2017). These arguments are supported by historical factors that are based on the expansion and retraction of the boundaries of dry and open habitat ecoregions, due to climatic fluctuations over geological time, which have reached coastal areas of northeastern Brazil (Ab'Saber 1977, Pennington et al. 2006). Thus, species considered previously endemic to the Caatinga, for example, E. borapeliotes and E. assisi , and species considered endemic to the Cerrado, for example C. flavolineatus (Nogueira et al. 2010), are also abundant in the PEC.
Most reptiles are considered habitat specialists, which means that many species can only survive in one or a few distinct environments (Martins and Molina 2008). In the PEC, the great majority of snake species were found in forest areas and 26 species were collected only in this environment. Due to the occupation of the area for agriculture and urbanization, most of the forest in the PEC was lost or reduced to small fragments, mostly smaller than ten hectares, which represent less than 2% of the original coverage of the Center (Ranta et al. 1998, Tabarelli et al. 2005. This is especially worrying because species that do not use the surrounding matrix as part of their area of use or that cannot use these environments to move between the fragments, can become extinct regionally as the populations are becoming isolated, making them unviable in the long term, due to the reduced population size (Nunney and Campbell 1993). On the other hand, some species seem to be generalists in terms of habitat and can be found in different physiognomies of the PEC and even urban areas, as is the case of B. constrictor, P. olfersii, B. leucurus and O. trigeminus.
Most snake species found in the PEC mainly use soil as substrate, as well as snakes in other regions of Brazil, such as the Caatinga , Atlantic Forest (Marques et al. 2017b), Cerrado (França and Braz 2013), Pantanal (Strussmann and Sazima 1993) and Amazon Oliveira 1998, Bernarde andAbe 2006). However, PEC also harbours a great variety of semi-arboreal and arboreal species, which is a characteristic of forest biomes, such as the Atlantic Forest and Amazon (Martins and Oliveira 1998, Argôlo 2004, Marques and Sazima 2004, Bernarde and Abe 2006.
More than half of PEC snakes feed on lizards or amphibians. These types of prey are commonly found in the snake diet, although other vertebrates like mammals, birds, and snakes are also important preys (Bernarde and Abe 2006, Hartmann et al. 2009, Mesquita et al. 2009). Some species of the PEC are generalists, as boids and snakes of the genus Philodryas and Oxyrhopus. Snakes belonging to the genera Apostolepis, Dipsas, and Atractus have specialized diet, feeding on snakes, mollusks and earthworms, respectively, as well as the genera Xenodon and Xenopholis, which are specialists in amphibians. (Vitt and Vangilder 1983, Laporta-Ferreira et al. 1986, Cunha and Nascimento 1993, Martins and Oliveira 1998, Mesquita et al. 2009, Bernarde and Abe 2010, Kokubum and Maciel 2010. It is important to emphasize that the PEC presents at least seven endemic species (A. caete, A. maculatus, B. muriciensis, Caaeteboia sp., D. atlantica, E. cephalomaculata, and M. potyguara) of which basic information on natural history and ecology are scarce. Most of these species have a very restricted distribution, have been little recorded in nature and consequently are poorly represented in scientific collections. For example, B. muriciensis has only nine records and was found only in a single location (Freitas et al. 2012), the E. cephalomaculata has seven known records and was found only in four locations (Freitas et al. 2019b) and Caaeteboia sp., which has only three records and should be a new species for the region (Pereira Filho et al. 2017). Moreover, some species have confused taxonomy, such as M. ibiboboca and D. neuwiedi, being a complex of different taxa. Some of these taxa could figure as endemic species in PEC in the future. Besides the endemic species, other PEC species deserve special attention due to the absence of information on natural history and ecology, for being rare in the region and for presenting a restricted distribution in the PEC, for example, L. trefauti, A. potschi, D. sazimai, D. variegata, E. cephalostriata, and A. arenensis. The conservation status of PEC snake species is still little known. Of the 78 species registered in the region, only 25 species have been evaluated by the IUCN (International Union for Conservation of Nature) to date. On the Brazilian list of threatened species, some PEC species are present, they are: A. amoipira, A. caete, and B. muriciensis as "endangered" and A. paucisquamus and E. cephalomaculata as "vulnerable" (ICMBio 2018). Given the high richness of snake species, the number of endemic species and the fragmented conditions of the region's forests, regional conservation efforts need to be intensified, because few forests north of the São Francisco River are formally protected, and the majority are small, which means that many species in the region may be threatened with extinction (Ranta et al. 1998, Uchoa Neto and Tabarelli 2002, Tabarelli et al. 2006a).
In general, many studies still need to be developed in the PEC region, so that we can better understand the snake fauna of this region. Fauna inventories in areas that are not well sampled, population dynamics studies and distribution patterns are important for better conservation planning of PEC snake species.