The Atlantic Forest is considered one of the richest forests in the world with a high number of endemic species and one of the 25 hotspots in the world (Myers et al., 2000). Originally this forest occurred in Brazil from the state of Rio Grande do Sul to Rio Grande do Norte along the coast as well as in inland regions (Galindo-Leal and Câmara, 2003). Throughout its distribution the Atlantic Forest has different composition of plants and animal species, resulting in biogeographic regions with specific characteristics developed through particular evolutionary and biogeographic processes, called centres of endemism (Silva et al., 2004). One of these centres of endemism is the Pernambuco Endemism Center (PEC), also known as Northern Atlantic Forest, a set of forests located in Alagoas, Pernambuco, Paraíba and Rio Grande do Norte states that are considered the most threatened sector of the entire biome (Tabarelli and Santos, 2004).

The Pernambuco Endemism Center harbours a high number of species with restrict distribution and many

endemic species (Pereira-Filho and Montingelli, 2011). Despite the increasing number of information about the snakes of PEC, many aspects remain unknown and unexplored and even basic data such as geographic distribution of many species are not known so far. At least three snake species are threatened of extinction in PEC, such as: Amerotyphlops amoipira (Rodrigues and Juncá, 2002), Atractus caete Passos, Fernandes, Bérnils and Moura-Leite, 2010, and Bothrops muriciensis Ferrarezzi and Freire, 2001; two others are considered vulnerable: Amerotyphlops paucisquamus (Dixon and Hendricks, 1979) and Echinanthera cephalomaculata Di-Bernardo, 1994 (Freitas et al., 2019).

One of the snake species inhabiting the PEC is Lachesis muta (Linnaeus, 1766) commonly known as Surucucu, Surucucu Pico de Jaca, Siri Pico de Jaca or Siri de Fogo and South American Bushmaster or even Mute Rattlesnake in other countries. The genus Lachesis Daudin, 1803 comprises four species: Lachesis acrochorda (Garcia, 1896) distributed in Panama, Colombia and Ecuador; Lachesis melanocephala Solorzano and Cerdas, 1986, found in Costa Rica and Panama; Lachesis stenophrys Cope, 1875 found in Nicaragua, Costa Rica and Panama and finally Lachesis muta (Linnaeus, 1766) with a wide distribution in Colombia, Venezuela, Trinidad, Guyana, French Guyana, Suriname and Brazil. In Brazil there are two disjunct populations, one in the Amazon Forest and one in the Atlantic Forest (Cambpell and Lamar, 2004). The population of the Atlantic Forest is distributed from Rio de Janeiro until Paraíba state with some relictual populations in inland forests of Ceará (Rodrigues et al., 2013).

The populations of Lachesis muta inhabiting the forests of PEC are poorly documented and only few specimens are known in herpetological collections (Fernandes and Franco, 2004; Rodrigues et al., 2013). However, there was an increase of specimens found in forest fragments along the PEC in the last few years (Fig. 1). The aim of

Herpetology Notes, volume 13: 565-569 (2020) (published online on 26 July 2020)

The Distribution of Lachesis muta (Linnaeus, 1766) in the Atlantic Forest of the Pernambuco Endemism Center,

Northeastern Brazil

Gentil Alves Pereira Filho1,*, Silvaney de Medeiros Sousa2, Abimael Guedes Figueiredo de Sousa2,3, Abraão Ribeiro Barbosa4, Frederico Gustavo Rodrigues França1, and Marco Antônio de Freitas5

1 Universidade Federal da Paraíba, Centro de Ciências Aplicadas e Educação, Departamento de Engenharia e Meio Ambiente, Núcleo de Ecologia de Serpentes, 58297- 000, Rio Tinto, PB, Brazil.

2 Museu Vivo Répteis da Caatinga, Rua Paulo Américo Paiva s/n, 58115-000, Puxinanã, PB, Brazil.

3 Universidade Estadual da Paraíba, Departamento de Biologia. Av. Das Baraúnas 35, 58429-500, Campina Grande, Paraíba, Brazil.

4 Universidade Federal da Paraíba, Centro de Ciências Agrárias, Departamento de Ciências Veterinárias, Brazil.

5 Instituto Chico Mendes de Conservação da Biosdiversidade (ICMbio), Estação Ecológica de Murici, Rua Marino Vieira de Araújo 32, Cidade Alta, Murici, Alagoas, 57820-000, Brazil.

* Corresponding author. E-mail: gentilfilho@yahoo.com

Gentil Alves Pereira Filho et al.566

Figure 1. Specimens of Lachesis muta recorded at the Pernambuco Endemism Center with respective precedence. (A) Recife, Pernambuco; (B) Mata do Buraquinho, João Pessoa, Paraíba; (C) Mata do Pau Ferro, Areia, Paraíba; (D) Rio Tinto, Paraíba. Photo by Willianilson Pessoa; (E) Areia, Paraíba. Record from 1929; (F) Serra do Urubu, Lagoa do Gatos, Pernambuco. Photo by Igor Joventino; (G) Serra Grande, Alagoas. Photo by Gabriel Skuk.

this work is to present an updated distribution of L. muta in the forest fragments of PEC, as well as emphasize the conservation status of the species in the most threatened region of the Atlantic Forest.

We gathered our data from four herpetological collections: Museu de Zoologia da Universidade de São Paulo (MZUSP), Instituto Butantan (IB), Instituto Vital Brazil (IVB) and Universidade Federal da Paraiba (CHUFPB), unpublished information from the authors and literature records.

Evaluating the records, it is also clear that Lachesis muta is a typical forest species that occurs only in forested areas and absent in dry areas like the Caatinga that surrounds many inland forests. Nowadays the species is confined to the remaining forest patches of PEC. The record closer to the coast is the one of João

Pessoa, Paraiba (seven kilometres far from the sea) in a dense ombrophilous forest, while the most inland is the one of Pedra Talhada Biological Reserve in Alagoas/Pernambuco states (120 kilometers far from the sea), in a montane forest over 500 meters above sea level (Table 1, Fig. 2). Lachesis muta can be found even in urban fragments of large cities like Recife and João Pessoa, such as Dois Irmãos and Mata do Buraquinho forest respectively.

The oldest record of Lachesis muta in PEC is from Areia (Mata do Pau Ferro Forest) and dates from 1929. The municipality of Areia nowadays presents small fragments of Atlantic Forest called “Brejos de Altitude” and most of the reduction of the natural forest began in 1930 with the sugar cane industry, responsible for the economy of the city during a long time. Even though

Table 1. Records of Lachesis muta in the Pernambuco Endemism Center.

Records Size of the areas (hectares)

Geographical Coordinates Numbers of records

Paraiba State

João Pessoa (Mata do Buraquinho Forest) 515 7 08’49.4”S \ 34 51'38.57’’W 3

Cruz do Espírito Santo (Usina São João Forest) 731,5 7 08’47.50’’S \ 35 05’21.71’’W 1

Santa Rita (RPPN Gargau, Usina Miriri forest) Gargau 1.436 Miriri forest 1.911

7 01’’03.74’’ S \ 34 57’’ 10. 73’’W 7 00’’.41.3’' S \ 35 05’ 31.76’’W

1 for each place

Areia (Mata do Pau Ferro Forest) 600 6 58’29.06’’S \ 35 43’28.21’’W 2

Rio Tinto unavailable data 6 55’22.19’’S \ 35 03’27. 81’W 1

Pernambuco State

Goiana unavailable data 7 36’02. 41’’S\ 34 59’25. 26’’W 1

Timbaúba (Àgua Azul Forest) 2.110 7 36’38.41’’S\ 35 22’59.97’’W 1

Bonito 1.508 8 31’13.72’’S\ 35 42’ 40. 32’’W

Lagoa dos Gatos/Jaqueira (RPPN Pedra D`Anta\ RPPN Frei Caneca)

1.550 8 41’35.1’’ S \ 35 51'27.’’W 8 41’47.4’’S \ 35 51’17. 3’’W

3

Camaragibe (Aldeia) 1.211 7 58’48. 88’’S \ 34 57’03. 38’’W 1

Agrestina/ Serra dos Cavalos Forest 785 8 22’13. 44’’S\ 36 01’51.78’’W 1

Nazaré da Mata unavailable data 7 50’43.62’’S\ 35 05’11. 72’’W 1

Recife/Dois Irmãos Forest 1.584 7 58’30. 09’’S\ 34 57’01. 00”W unprecise number, more than one

Barreiros 562 8 43’27. 26’’S\ 35 10’53. 87’’W 1

Jaboatão dos Guararapes unavailable data 8 12’36. 67’’W\ 34 58’21. 58’’W 1

Alagoas State

Muriçi (Muriçi Ecological Station) 6.131 9 12’17.80’’S \ 35 52’16. 86’’W many records

Chã Preta unknown 9 16’33. 37’’S\ 36 14’ 03. 26’’W 1

Pedra Talhada Biological Reserve 4.469 9 13’57.56’’S\ 36 25’39. 03’W 5

Rio Largo unavailable data 9 33’14. 45’’S\ 35 48’05. 15’’W 1

São José da Lage (Serra Grande Forest) unavailable data 8 56’12.22’’S\ 35 59’35.75’’W 3

Rio Largo (Utinga Leão Forest) 900 9 31’23. 27’’S\ 35 54’36. 32’’W 2

São Miguel dos Campos unavailable data 9 44’83.33”S\ 35 85’33.33”W 1

Table 1. Records of Lachesis muta in the Pernambuco Endemism Center.

The Distribution of Lachesis muta in the Atlantic Forest, Northeastern Brazil 567

the presence of a second specimen of L. muta in the area was not expected due to the habitat fragmentation of the region, there was a recent record from 2019. This record evidences that even relatively small forests fragments can provide suitable habitat for sensitive species such as Lachesis muta

Another important finding is the lack of recent or historical records in the state of Rio Grande do Norte. According to Campbell and Lamar (2004), L. muta occurs in this state, but we were not able to find any record for that region. The type of vegetation can be a limiting factor to the presence of L. muta; the Atlantic Forest found in the Rio Grande do Norte is dryer and presents a smaller arboreal size than the ones of Paraiba, Pernambuco and Alagoas. Most of the remnants of that state are Restinga forests, a coastal savannah-like formation characterized by sandy soils and small trees (Thomas and Barbosa, 2008), which could explain the absence of the species. Overall, the forest fragments of Rio Grande do Norte remains poorly surveyed and no list of snake species is available.

Undoubtedly, the habitat destruction and consequent habitat fragmentation is the main threat to L. muta, but another factor must be mentioned. Hunting activities are very common in Brazil and have great impacts on populations of game species, mainly mammals and birds, notably species weighing more than 500 grams (Fernandes-Ferreira and Alves, 2017), leading to regional extinctions of common vertebrates such as rodents (Dasyprocta sp. and Cuniculus paca), armadillos (Dasypus sp. and Euphractus sexinctus) and birds. In northeastern Brazil hunting activities have strong cultural attributions that are deeply rooted in the population, no longer by the necessity of animal protein, but merely by sporting activity itself. During hunting activities, the encounter of a large snake such as Lachesis muta (which is usually about 2 meters in size) (Campbell and Lamar, 2004) commonly ends with the snake being shot in order to avoid new encounters. This environmental problem has caused regional extinction in several fragments of forests still intact, many of them without records of this species in several years,

Figure 2. Distribution map of Lachesis muta in the Pernambuco Endemism Center.

Gentil Alves Pereira Filho et al.568

as stated by rural populations who live in many areas. This fact shows clearly that conserved forests with good physical structure (vegetation structure) are not always a guarantee of maintaining wild animal populations (Pereira-Filho et al., 2017).

Another factor related to illegal hunting which can affect the L. muta population indirectly is that this snake commonly uses burrows of armadillos, agoutis and pacas to lay eggs and even mating, as stated by Antônio Argôlo, personal communication from the region of Ilhéus, Bahia, Northeastern Brazil (Atlantic Forest), and Marco Freitas, personal communication from Roraima, Pacaraima, Northern Brazil (Amazon Forest), (Campbell and Lamar, 2004). With the reduction of such mammals the burrows that once were abundant are no longer available for the snakes, thus interfering in the reproduction habits of the species.

The records gathered herein show that L. muta may have small and isolated populations throughout PEC and probably was extinct in many areas once the northeast Atlantic Forest was destroyed in its majority. There is an urgent necessity to maintain these isolated forests remnants that harbour the last populations of L. muta in the region. In our view, the populations of L. muta are threatened in the Atlantic Forest. Unfortunately, the criteria used by IUCN to compose the red list of endangered species does not encompass Lachesis muta in any category due to its large distribution. An option to protect this species is the elaboration of lists of endangered fauna of the states of PEC as well as reintroduction and monitoring programs and natural corridors connecting the fragments. Without these procedures the extinction of L. muta in PEC is a matter of time, once that the populations will be affected by habitat destruction that increases every day and the ignorance of human populations responsible for killing this species.

Acknowledgments. The authors are grateful to Arthur Abegg for providing the map.

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Accepted by Anamarija Zagar

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