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Home , Bothrops, Lachesis (genus), Lachesis acrochorda, Lachesis melanocephala, Lachesis muta, Lachesis stenophrys

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

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

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

The Atlantic Forest is considered one of the richest endemic (Pereira-Filho and Montingelli, 2011). forests in the world with a high number of endemic Despite the increasing number of information about species and one of the 25 hotspots in the world (Myers et the of PEC, many aspects remain unknown and al., 2000). Originally this forest occurred in Brazil from unexplored and even basic data such as geographic the state of to distribution of many species are not known so far. At along the coast as well as in inland regions (Galindo- least three species are threatened of extinction in Leal and Câmara, 2003). Throughout its distribution the PEC, such as: Amerotyphlops amoipira (Rodrigues and Atlantic Forest has different composition of plants and Juncá, 2002), Atractus caete Passos, Fernandes, Bérnils species, resulting in biogeographic regions with and Moura-Leite, 2010, and muriciensis specific characteristics developed through particular Ferrarezzi and Freire, 2001; two others are considered evolutionary and biogeographic processes, called vulnerable: Amerotyphlops paucisquamus (Dixon and centres of endemism (Silva et al., 2004). One of these Hendricks, 1979) and Echinanthera cephalomaculata centres of endemism is the Pernambuco Endemism Di-Bernardo, 1994 (Freitas et al., 2019). Center (PEC), also known as Northern Atlantic Forest, One of the snake species inhabiting the PEC is Lachesis a set of forests located in , Pernambuco, Paraíba muta (Linnaeus, 1766) commonly known as Surucucu, and Rio Grande do Norte states that are considered the Surucucu Pico de Jaca, Siri Pico de Jaca or Siri de Fogo and most threatened sector of the entire biome (Tabarelli South American Bushmaster or even Mute and Santos, 2004). in other countries. The Lachesis Daudin, 1803 The Pernambuco Endemism Center harbours a high comprises four species: (Garcia, number of species with restrict distribution and many 1896) distributed in , and ; Solorzano and Cerdas, 1986, found in and Panama; Cope, 1875 found in , Costa Rica and Panama and finally (Linnaeus, 1766) with a wide 1 Universidade Federal da Paraíba, Centro de Ciências distribution in Colombia, , Trinidad, , Aplicadas e Educação, Departamento de Engenharia e Meio French Guyana, and Brazil. In Brazil there are Ambiente, Núcleo de Ecologia de Serpentes, 58297- 000, two disjunct populations, one in the Amazon Forest and Rio Tinto, PB, Brazil. one in the Atlantic Forest (Cambpell and Lamar, 2004). 2 Museu Vivo Répteis da Caatinga, Rua Paulo Américo Paiva s/n, 58115-000, Puxinanã, PB, Brazil. The population of the Atlantic Forest is distributed from 3 Universidade Estadual da Paraíba, Departamento de Biologia. until Paraíba state with some relictual Av. Das Baraúnas 35, 58429-500, Campina Grande, Paraíba, populations in inland forests of Ceará (Rodrigues et al., Brazil. 2013). 4 Universidade Federal da Paraíba, Centro de Ciências Agrárias, The populations of Lachesis muta inhabiting the forests Departamento de Ciências Veterinárias, Brazil. of PEC are poorly documented and only few specimens 5 Instituto Chico Mendes de Conservação da Biosdiversidade are known in herpetological collections (Fernandes and (ICMbio), Estação Ecológica de Murici, Rua Marino Vieira de Araújo 32, Cidade Alta, Murici, Alagoas, 57820-000, Franco, 2004; Rodrigues et al., 2013). However, there Brazil. was an increase of specimens found in forest fragments * Corresponding author. E-mail: [email protected] along the PEC in the last few years (Fig. 1). The aim of 566 Gentil Alves Pereira Filho et al.

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. The Distribution of Lachesis muta in the Atlantic Forest, Northeastern Brazil 567 this work is to present an updated distribution of L. muta Pessoa, Paraiba (seven kilometres far from the sea) in in the forest fragments of PEC, as well as emphasize the a dense ombrophilous forest, while the most inland is conservation status of the species in the most threatened the one of Pedra Talhada Biological Reserve in Alagoas/ region of the Atlantic Forest. Pernambuco states (120 kilometers far from the sea), in We gathered our data from four herpetological a montane forest over 500 meters above sea level (Table collections: Museu de Zoologia da Universidade de 1, Fig. 2). Lachesis muta can be found even in urban São Paulo (MZUSP), Instituto Butantan (IB), Instituto fragments of large cities like Recife and João Pessoa, (IVB) and Universidade Federal da Paraiba such as Dois Irmãos and Mata do Buraquinho forest (CHUFPB), unpublished information from the authors respectively. and literature records. The oldest record of Lachesis muta in PEC is from Evaluating the records, it is also clear that Lachesis Areia (Mata do Pau Ferro Forest) and dates from 1929. muta is a typical forest species that occurs only in The municipality of Areia nowadays presents small forested areas and absent in dry areas like the Caatinga fragments of Atlantic Forest called “Brejos de Altitude” that surrounds many inland forests. Nowadays the and most of the reduction of the natural forest began in species is confined to the remaining forest patches of 1930 with the sugar cane industry, responsible for the PEC. The record closer to the coast is the one of João economy of the city during a long time. Even though

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

Records Size of the areas Geographical Coordinates Numbers of (hectares) 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 7 01’’03.74’’ S \ 34 57’’ 10. 73’’W 1 for each place forest 1.911 7 00’’.41.3’' S \ 35 05’ 31.76’’W 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 1.550 8 41’35.1’’ S \ 35 51'27.’’W 3 D`Anta\ RPPN Frei Caneca) 8 41’47.4’’S \ 35 51’17. 3’’W 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

568 Gentil Alves Pereira Filho et al.

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

the presence of a second specimen of L. muta in the area Undoubtedly, the habitat destruction and consequent was not expected due to the habitat fragmentation of the habitat fragmentation is the main threat to L. muta, but region, there was a recent record from 2019. This record another factor must be mentioned. Hunting activities evidences that even relatively small forests fragments are very common in Brazil and have great impacts can provide suitable habitat for sensitive species such on populations of game species, mainly mammals as Lachesis muta and birds, notably species weighing more than 500 Another important finding is the lack of recent or grams (Fernandes-Ferreira and Alves, 2017), leading historical records in the state of Rio Grande do Norte. to regional extinctions of common vertebrates such According to Campbell and Lamar (2004), L. muta as rodents (Dasyprocta sp. and Cuniculus paca), occurs in this state, but we were not able to find any armadillos (Dasypus sp. and Euphractus sexinctus) record for that region. The of vegetation can be a and birds. In northeastern Brazil hunting activities limiting factor to the presence of L. muta; the Atlantic have strong cultural attributions that are deeply rooted Forest found in the Rio Grande do Norte is dryer and in the population, no longer by the necessity of animal presents a smaller arboreal size than the ones of Paraiba, protein, but merely by sporting activity itself. During Pernambuco and Alagoas. Most of the remnants of hunting activities, the encounter of a large snake such as that state are Restinga forests, a coastal savannah-like Lachesis muta (which is usually about 2 meters in size) formation characterized by sandy soils and small trees (Campbell and Lamar, 2004) commonly ends with the (Thomas and Barbosa, 2008), which could explain the snake being shot in order to avoid new encounters. This absence of the species. Overall, the forest fragments of environmental problem has caused regional extinction Rio Grande do Norte remains poorly surveyed and no in several fragments of forests still intact, many of list of snake species is available. them without records of this species in several years, The Distribution of Lachesis muta in the Atlantic Forest, Northeastern Brazil 569 as stated by rural populations who live in many areas. Freitas, M.A., Barbosa, G.G., Bernardino, K.P., Pinheiro Filho, This fact shows clearly that conserved forests with good J.D., Abbeg, A.D. (2019): First records of the rare snake physical structure (vegetation structure) are not always Echinanthera cephalomaculata Di-Bernardo, 1994 in the state of Pernambuco, Brazil (Serpentes: Dipsadidae). Herpetology a guarantee of maintaining wild animal populations Notes 12: 1005–1009. (Pereira-Filho et al., 2017). Galindo-Leal, C., Câmara, I.G. (2003): Atlantic Forest hotspots Another factor related to illegal hunting which can status: an overview. In: The Atlantic Forest of : affect the L. muta population indirectly is that this snake biodiversity status, threats, and outlook, p. 1–13. Galindo-Leal, commonly uses burrows of armadillos, agoutis and C., Câmara, I.G., Eds. Washington, D.C., Center for Applied pacas to lay eggs and even mating, as stated by Antônio Biodiversity Science and Island Press. Argôlo, personal communication from the region of Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., Kent, J. (2000): Biodiversity hotspots for conservation priorities. Ilhéus, , Northeastern Brazil (Atlantic Forest), Nature 403: 853–858. and Marco Freitas, personal communication from Pereira-Filho, G.A., Vieira, W.L., Montingelli, G.G., Rodrigues, Roraima, Pacaraima, Northern Brazil (Amazon Forest), J.B., Alves, R.R.N., França, F.G.R. (2017): Diversidade. In: (Campbell and Lamar, 2004). With the reduction of Pereira-Filho, G.A, Vieira, W.L.S, Alves, R.R.N, França. F.G.R., such mammals the burrows that once were abundant are Eds. Serpentes da Paraíba. João Pessoa, p. 55–269. no longer available for the snakes, thus interfering in the Pereira Filho, G.A., Montingelli, G.G. (2011): Check list of snakes reproduction habits of the species. from the brejos de altitude of Paraíba and Pernambuco, Brazil. Biota Neotropica 11: 1–7. The records gathered herein show that L. muta may Rodrigues, R., Albuquerque, R.L., Santana, D.J., Laranjeiras, D.O., have small and isolated populations throughout PEC and Protazio, A.S., França, F.G.R., Mesquita, D.O. (2013): Record probably was extinct in many areas once the northeast of the occurrence of Lachesis muta (Serpentes, ) in an Atlantic Forest was destroyed in its majority. There is Atlantic Forest fragment in Paraíba, Brazil, with comments on an urgent necessity to maintain these isolated forests the species’ preservation status. Biotemas 26: 283–286. remnants that harbour the last populations of L. muta Silva, J.M.C., Sousa, M.C., Casteleti, C.H.M. (2004): Areas of in the region. In our view, the populations of L. muta endemism for passerine birds in the Atlantic forest, South America. Global Ecology and Biogeography 13: 85–92. are threatened in the Atlantic Forest. Unfortunately, Tabarelli, M., Santos, A.M.M. (2004): Uma breve descrição sobre a the criteria used by IUCN to compose the red list of história natural dos brejos nordestinos. In: Brejos de altitude em endangered species does not encompass Lachesis Pernambuco e Paraíba: história natural, ecologia e conservação, muta in any category due to its large distribution. An p. 17–24. Pôrto, K.C., Cabral, J.J.P., Tabarelli, M., Eds., Brasília, option to protect this species is the elaboration of lists Brazil, Ministério do Meio Ambiente. of endangered fauna of the states of PEC as well as Thomas, W.W., Barbosa, M.R. (2008): Natural Vegetation Types reintroduction and monitoring programs and natural in the Brazilian Atlantic Coastal Forest North of the Rio Doce. Memoirs of the New York Botanical Garden 100: 6–20. 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.

References

Campbell, J.A., Lamar, W.L. (2004): The venomous of the . New York, USA, Cornell University Press. Fernandes-Ferreira, H., Alves, R.R.N. (2017): The researches on the hunting in Brazil: a brief overview. Ethnobiology and Conservation 6: 1–6. Fernandes, D.S., Franco, F.L., Fernandes, R. (2004): Systematic revision of the genus Lachesis Daudin, 1803 (Serpentes, Accepted by Anamarija Zagar Viperidae). Herpetologica 60: 245–260.