Biology and conservation status of Piraja’s Lancehead Snake Bothrops pirajai Amaral, 1923 (Serpentes: Viperidae), Brazil
Marco Antonio de Freitas 1, Antonio Jorge Suzart Argôlo 2,
Catherine Gonner 3 & Diogo Veríssimo 4
1,2 Programa de pós-graduação em Zoologia, Universidade Estadual de Santa Cruz - UESC, Rod.
Ilhéus-Itabuna, km 16, CEP 45662-900, Ilhéus, BA, Brasil
3,4 Durrell Institute of Conservation and Ecology (DICE), School of Anthropology and Conservation,
University of Kent, CT2 7NR, Canterbury, Kent, UK
1 firstname.lastname@example.org (corresponding author), 2 email@example.com,
3 C.Gonner@kent.ac.uk, 4 firstname.lastname@example.org
Abstract: The venomous snake Bothrops pirajai (Amaral, 1923) is endemic to Brazil. Despite being described almost a century ago, very little is known about this species, which has never been studied in situ. Here, we present new data on the biology and natural history of B. pirajai based on a review of existing museum specimens and a field study (1504 man hours) carried out throughout the species range. The distribution of B. pirajai was found to be restricted to the eastern Atlantic forest of the state of Bahia, Brazil, between Todosos Santos Bay, Itabuna and Ilhéus (12050’S–14050’S, 88–835 m). We recommend the species be uplisted to Endangered in the International Union for the Conservation of Nature’s global Red List of Threatened Species as its estimated extent of occurrence is under 5000km2. The effective conservation of B. pirajai will rely on addressing two key issues: improving our knowledge of the species and successfully mitigating habitat loss and fragmentation.
Keywords: Assessment, conservation status, Reptilia, South America, Squamata, threatened species, viper.
Portuguese Abstract: A serpente venenosa Bothrops pirajai (Amaral, 1923) é endémica do Brasil. Apesar de ter sido descrita há mais de um século, pouco é sabido acerca desta espécie, que nunca foi estudada em estado selvagem. Neste trabalho, apresentamos novos dados biológicos sobre B. pirajai baseados não só numa revisão de espécimes de museu, mas também em amostragens (total cerca de 1700 horas/pessoa) realizadas na área de distribuição da espécie. Os nossos resultados indicam que a distribuição geográfica está apenas confinada ao sudeste da Mata Atlântica do estado da Bahia, Brasil, entre a Baia de Todos os Santos, Itabuna e Ilhéus (12050’S–14050’S, 88–835 m). Neste sentido, recomendamos que a espécie seja elevada ao estatuto de “Em perigo” na Lista Vermelha da União Internacional para a Conservação da Natureza, dado que a sua extensão de ocorrência é menos de 5000km2. Uma estratégia de conservação efectiva para esta espécie deverá centrar-se na melhoria do conhecimento existente sobre a história natural e biologia da espécie e na mitigação do impacto da perda e fragmentação do habitat.
We examined specimens from the following herpetological collections: Coleção Herpetológica “Alphonse Richard Hoge” (IBSP) of the Instituto Butantan, São Paulo, the Coleção Zoológica Gregório Bondar (CZGB) of the Comissão Executiva do Plano da Lavoura Cacaueira (CEPLAC) and Museu de Zoologia da UniversidadeEstadual de Santa Cruz (MZUESC), both in Ilhéus, Bahia, Brazil. For each specimen, total length, sex and locality were recorded. Where GPS coordinates were unavailable, other information on the collection locality (e.g., name of estates or other geographical features) was used to infer an approximate location. Information on coloration and patterning of preserved individuals was also collected as far as preservation conditions allowed.
We conducted ecological field surveys along the southeastern region of Bahia, Brazil, between January 2005 and February 2008. The surveys first focused on the localities where specimens of B. pirajai were previously found (Amaral 1923; Freitas 1999; Argôlo 2004) and then moved on to neighbouring regions. Surveys were conducted with one to five observers (most commonly two), throughout the day, but were concentrated between 18:00 and 22:00 hr as this is the time when species of the viper family tend to be most active (Campbell & Lamar 2004). Search effort was calculated as man/hours by summing the total number of survey hours by all surveyors involved. When encountering individuals of B. pirajai, we registered time, date, GPS coordinates, type of habitat in which it was found, straight-line distance to nearest water course and behaviour (see Oliveira & Martins 2001). Unfortunately, the variation in survey effort per site and lack of repeated visits to the different field sites did not allow us to estimate species detectability. Lastly, all specimens were photographed to provide information on color and patterning.
We also interviewed local residents about the occurrence of Piraja’s Lancehead. We focused our sampling on current or ex-hunters (i.e., adult males), as these tend to be the group with the most in-depth knowledge of the local fauna and flora. After a few initial questions concerning the most common snakes in the region, we showed the interviewees photos of Piraja’s Lancehead and other morphologically similar snakes, including B. leucurus Wagler, 1824, Bothrops jararaca (Wied, 1824) and Xenodon rabdocephalus (Wied, 1824). We then asked local residents which of those species they had seen before. We used the mention of the species’ local names, jaracuçu-tapete or tapete (rug or carpet), as well as the species’ body length and species’ behaviour (e.g., propensity to flatten itself on the ground when threatened) to determine if they had successfully identified the snake.
Considering the small amount of available data on this species, the most viable method to assess the conservation status of B. pirajai is to estimate the species extent of occurrence (IUCN Standards and Petitions Subcommittee 2014), “the area contained within the shortest continuous imaginary boundary which can be drawn to encompass all the known, inferred or projected sites of present occurrence of a taxon, excluding cases of vagrancy”. To calculate this area we used 27 of the existing 32 records for this species. We decided to exclude the single record for Monte Santo, which is most likely inaccurate (the locality was only added 54 years after the specimen was collected and the habitat has historically been ecologically different from any location where the species was found) and the records for the municipalities of Ilhéus and Itabuna, which are more than 50 years old and which recent surveys did not corroborate. We also did not take into account two records for the municipality of Igrapiuna (for which eight additional records exist) as it was not possible to estimate their GPS coordinates.
The ecological survey effort was just over 1700 man-hours, distributed across 18 municipalities of the state of Bahia. Only five individuals were found (four juveniles and one adult) (Image 1B–E and G). However, another five anecdotal records registered by other researchers in subsequent studies and verified through high-resolution photographs, are also included in the present analysis (e.g., Image 1A, F and H). A total of 310 interviews were conducted across 43 municipalities in the state of Bahia. Only in about 7% of the interviews did the respondents successfully identify B. pirajai.
All B. pirajai specimens were found in the eastern Atlantic Forest biome, more specifically Ombrophilous forest, between 12050’S and 14050’S (Fig. 1), in altitudes ranging from 88–835 m. In terms of geographic distribution, the present study significantly widens the potential distribution of B. pirajai, providing evidence from interviews that B. pirajai may be distributed across 14 municipalities for which there are no biological records (Fig. 1).
The largest recorded individual of B. pirajai was a female measuring 1130mm in length (IB 3008), with 50% of the 22 females in herpetological collections being more than 800 mm in length. The largest recorded male of B. pirajai measured 820mm (MZUESC 5104). Although records for two other male specimen exist (one of which is the holotype), these specimens appear now to have been lost.
In terms of coloration, most specimens have a reddish-brown back with dark brown dorsal markings. There is marked sexual dichromatism in adult snakes. Males have disruptive coloration, with less defined and fragmented dorsal spots. Interspaces usually have dark spots in both the vertebral region and on the flanks. It should be noted that when preserved in alcohol, the reddish-brown coloration fades and males become similar to some B. leucurus specimens. Unlike males, females have well defined and complete dorsal marks, forming a V or an inverted Y. The vertebral line has interspaces with a dark region and usually with two dark, irregular, opposite and alternate spots (Image 1G and H). On the sides, interspaces are clear and often without spots, thus sharply contrasting with the dorsal spots, which are much more conspicuous than those found on males.
Considering habitat use for all newly recorded individuals were found on the ground, nine of which in a thick layer of leaf litter and one female in a burrow. Individuals were found to be active during evenings between 20:00 and 22:00 hours and mostly inactive or potentially thermoregulating during the morning. When disturbed, individuals flattened dorso-ventrally and vibrated their tail. Although this species might hunt near water, only half of the specimens found were within 50m of a water source. In relation to diet, a juvenile female housed at the Coleção Zoológica Gregório Bondar (CZGB 9509) was anecdotally found to have a Teiid Lizard in its stomach. Three juvenile females, kept in in situ terrariums for between 48–72 hours, consumed frogs (e.g., Eleutherodactylus bilineata and Haddadus binotatus). Finally, in terms, of conservation status, the estimated area of extent of occurrence for B. pirajai was 4222km2. However, it should be noted that the municipalities where the species occurs have a total of only 858km2 of forest cover.
Much of the published information on the distribution of B. pirajai is misleading (Argôlo 2008). The present study highlights a further potential inconsistency around the locality of Monte Santo, where the holotype for this species was allegedly collected. Ecological surveys conducted in this locality not only failed to find any specimens of this species but have also uncovered that the habitat types in this region are different from those where all other records of B. pirajai have been obtained. Furthermore, historical data on the snake species collected in that region shows the presence of species from much more arid habitats than those where B. pirajai have been recorded. Lastly, it should also be considered that detailed information on the locality was added only 54 years after the specimen was collected (see Amaral 1923, 1977). Based on verified records, B. pirajai is likely to be restricted to the dense ombrophilous Atlantic Forest of the state of Bahia, between 12030’S & 15000’S (Argôlo 2008). While most of this is lowland, some records, such as the Serra do Timbó in Ubaíra, or the Serra da Jibóia in ElísioMedrado, indicate that B. pirajai can be found at higher elevations (up to 880m).
As it is the case with other species in the Bothrops genus, B. pirajai is terrestrial and primarily nocturnal, although it may thermoregulate in the early morning hours in forest clearings (Martins et al. 2002; Oliveira & Martins 2002; Sasa-Marín et al. 2009). Despite the few male specimens available, sexual dimorphism is likely to occur in B. pirajai, with males being generally smaller than females, as is the case in many snake species (e.g., Shine 1994). In addition, there seems to be clear sexual dichromatism (Amaral 1923; Amaral 1977) in line with other related species, such as B. jararacussu (Marques & Sazima 2003). Juveniles of B. pirajai have a yellow tail tip, a characteristic shared with other Bothrops species, which is likely to be used to attract prey such as lizards and frogs. This behaviour is known as caudal luring and has been reported for other Bothrops species (Sazima 1991, 2006).
Regarding diet, the only previous records showed remains of rodents in two individuals of B. pirajai, (Argôlo 2004). We found a teiid lizard in the stomach of one juvenile museum specimen (CZGB 9509) and three individuals ate amphibians shortly after they were caught and kept in short-term captivity. As is common with other snake species of the genus Bothrops (Greene 1988), individuals of B. pirajai were seen to flatten their body dorso-ventrally and vibrate their tail when confronted with a perceived threat, perhaps in an effort to seem larger (Greene 1988). According to residents from Igrapiúna and Camamu, this behaviour explains the common names of the snake: Jaracuçu-tapeteor simply Tapete, which means carpet or rug in Portuguese.
As is the case for most of the reptiles in Brazil, the most important threat to B. pirajai is habitat loss (Rodrigues 2005; Argôlo 2008), with the state of Bahia having lost about 4% of its Atlantic forest in the last decade (SOSMA/INPE 2013). Human persecution may also play a role, with local residents reporting killing the species on sight when entering the forest to extract resources such as firewood (Freitas 2008). Nonetheless, only one case of human envenomation has ever been reported (Argôlo et al. 1999).
Bothrops pirajai is currently classified as Endangered B1ab(iii) in the Red Book of Brazilian Reptiles (Argôlo 2008), after not appearing in the Brazilian RedList assessments of 1968, 1972 or 1989. Globally, the species is classified as Vulnerable A1c, having been included in the global RedList of Threatened Species (Argôlo 2000), for the first time in 2000. The latter assessment is, however, now more than a decade old and is in need of an update (see Argôlo 2000). We believe the data gathered in this study could inform this revision.
Both national and global species assessments emphasize the decrease in available habitat, severe habitat fragmentation and the species’ restricted distribution. This highlights not only the key conservation threats to the species but also that geographical distribution is one of the few parameters for which there is enough information on which to base a conservation assessment. A similar situation has been found with other poorly known members of the genus Bothrops (de Freitas et al. 2012). The estimated extent of occurrence for B. pirajai is 4222km2, placing the species under the 5000km2 threshold required for the Endangered category (IUCN Standards and Petitions Subcommittee 2014). The species should thus be uplisted to Endangered under criteria B1ab(iii). This stems from the species’ highly fragmented habitat (the municipalities with confirmed biological records of B. pirajai have only 858km2 of forest; Fig. 2) and suspected continued decline based on the decrease of area and quality of habitat (SOSMA/INPE 2013). This is the same status and underlying criteria currently used to determine the status of the species in the Red Book of Brazilian Reptiles.
We purposefully restricted our estimate of the extent of occurrence to the confirmed biological records, although the results of the interviews conducted make it likely that the species could be distributed across a wider area. We adopt this precautionary approach, as the species is expected to occur at very low densities and habitat fragmentation and loss are ongoing (IESB 2007). Further studies are needed to corroborate with biological evidence the records obtained through interviews and thus allow for an eventual recalculation of the species’ extent of occurrence. It should also be noted that the only records of B. pirajai for a protected area were obtained via interviews of local residents near the Wenceslau Guimarães Ecological Station. Records for the Boa Esperança Muncipal Park and Area de Protecção Ambiental Baia de Camamu have recently been discredited. The former due to the 80 years that have elapsed since the collection of the information combined with the lack of corroboration by recent surveys and the latter due to an error in naming the locality where the specimen was found (Freitas 2008). This means that B. pirajai is poorly represented in Brazil’s protected area network, making the species even more vulnerable to further habitat loss and fragmentation.
The effective conservation of B. pirajai relies on addressing two key issues: improving our knowledge of the species, namely through the study of population density, genetics and dynamics, and successfully mitigating habitat loss and fragmentation. The first will depend on the implementation a species action plan (Argôlo 2008) identifying the priority geographical areas for the species as well as key knowledge gaps, such as understanding the species ecological requirements or its sensitivity to habitat disturbance. The second resolves around ensuring adequate management of existing protected areas, especially those that allow sustainable use, in the face of growing demand for natural resources. As with many other reptiles in Brazil, the future of B. pirajai relies on improving the links between livelihoods and biodiversity through an adequate mix of knowledge, management and community-based conservation.
Amaral, A. (1923). New genera and species of snakes. Proceedings New England and Zoological Club 8: 85–105.
Amaral, A. (1977). Serpentes do Brasil, Iconografia colorida. São Paulo, Edições Melhoramentos/EDUSP.
Argôlo, A.J.S. (1989). Nota sobre Bothrops pirajai Amaral, 1923 (Serpentes, Viperidae). Anais do XVI Congresso Brasileiro de Zoologia. Sociedade Brasileira de Zoologia, Rio de Janeiro, Brazil: Sociedade Brasileira de Zoologia, Rio de Janeiro, Brazil, 81pp.
Argôlo, A.J.S. (2000). Bothrops pirajai. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. <www.iucnredlist.org>. Downloaded on 02 April 2014.
Argôlo, A.J.S. (2004). As serpentes dos cacauais do Sudeste da Bahia. Editus, Ilhéus, Brazil, 260pp.
Argôlo, A.J.S. (2007). Bothrops pirajai Amaral, 1923 (Serpentes, Viperidae): cópula e gestação em cativeiro. 3º Congresso Brasileiro de Herpetologia, 2007, Belém, Brazil
Argôlo, A.J.S. (2008). Bothrops pirajai, pp. 354–355. In: Machado, A.B., G.M. Drummond & A.P. Paglia (eds.). Livro Vermelho da Fauna Brasileira Ameaçada de Extinção, Volume 2. Répteis. Ministério do Meio Ambiente, Brasília; Fundação Biodiversitas, Belo Horizonte.
Argôlo, A.J.S., E.P.F. Moraes & M.A. Freitas (1999). Primeiro caso documentado de acidente humano por Bothrops pirajai Amaral, 1923 (Serpentes, Viperidae). Anais do XII Encontro de Zoologia do Nordeste. Feira de Santana, Sociedade Nordestina de Zoologia, 423pp.
Câmara, I.G. (2005). Breve história da conservação da Mata Atlântica. Mata Atlântica: biodiversidade, ameaças e perspectivas. Fundação SOS Mata Atlântica, São Paulo & Conservation International, Belo Horizonte, Brazil: 31–42.
Campbell, J.A., & W. Lamar (2004). The Venomous Reptiles of the Western Hemisphere. Comstock Publishing Associates, Cornell University Press, Ithaca, New York, USA.
da Silva, J.M.C. & C. Casteleti (2003). Status of the biodiversity of the Atlantic Forest of Brazil, pp. 43–59. In: Leal, C.G. & I.G. Câmara (eds.). The Atlantic Forest of South America: Biodiversity Status, Threats, and Outlook. Island Press, Washington DC, USA, 408pp.
de Freitas, M.A., F. de França, D. Pereira, R. Graboski, V. Uhlig & D. Veríssimo (2012). Notes on the conservation status, geographic distribution and ecology of Bothrops muriciensis Ferrarezzi & Freire, 2001 (Serpentes, Viperidae). North-Western Journal of Zoology 8(2): 338–343.
Freitas, M.A. (1999). Serpentes da Bahia e do Brasil. Dall, Feira de Santana, Brazil, 78pp.
Freitas, M.A. (2008). Distribuição geográfica, história natural e avaliação do status de conservação da jaracuçu-tapete Bothrops pirajai Amaral, 1923. MSc Thesis, Universidade Estadual de Santa Cruz, Ilhéus, Brazil.
Greene, H.W. (1988). Antipredator mechanisms in reptiles, pp. 1–152. In: Gans, C. & R.B. Huey (eds.). Biology of the Reptilia. New York, USA.
IESB (Instituto de Estudos Socioambientais do Sul da Bahia)(2007). Levantamento da Cobertura Vegetal Nativa do Bioma Mata Atlântica. Instituto de Estudos Socioambientais do Sul da Bahia (IESB). Rio de Janeiro, Brazil.
IUCN Standards and Petitions Subcommittee (2014). Guidelines for Using the IUCN Red List Categories and Criteria. Version 11. Prepared by the Standards and Petitions Subcommittee of the IUCN Species Survival Commission. Downloadable from www.iucnredlist.org/documents/RedListGuidelines.pdf.
Marques, O. & I. Sazima (2003). Bothrops jararacussu (Jararacussu). Sexual Dichromatism. Herpetological Review 34: 62.
Martins, M., O.A.V. Marques & I. Sazima (2002). Ecological and phylogenetic correlates of feeding habits in Neotropical pitvipers of the genus Bothrops. Biology of the Vipers, pp. 307–328. In: Schuett, G.W., M.E. Douglas, M. Höggren & H.W. Greene (eds.). Biology of the Vipers. Eagle Mountain Publishing, Eagle Mountain, UT, 508pp.
Menaldo, D.L., C.P. Bernardes, N.A. Santos-Filho, L.A. Moura, A.L. Fuly, E.C. Arantes & S.V. Sampaio (2012). Biochemical characterization and comparative analysis of two distinct serine proteases from Bothrops pirajai snake venom. Biochimie 94: 2545–2558; http://dx.doi.org/10.1016/j.biochi.2012.07.007
Myers, N., R.A. Mittermeier, C.G. Mittermeier, G.A. da Fonseca & J. Kent (2000). Biodiversity hotspots for conservation priorities. Nature 403: 853–858; http://dx.doi.org/10.1038/35002501
Oliveira, M.E. & M. Martins (2001). When and where to find a pitviper: activity patterns and habitat use of the lancehead, Bothrops atrox, in central Amazonia, Brazil. Herpetological Natural History 8: 101–110.
Oliveira, M.E. & M. Martins (2002). When and where to find a pitviper: activity patterns and habitat use of the lancehead, Bothrops atrox, in central Amazonia, Brazil. Herpetological Natural History 8: 101–110.
Pimm, S.L., C.N. Jenkins, L.N. Joppa, D.L. Roberts & G.J. Russell (2010). How many endangered species remain to be discovered in Brazil. Natureza & Conservação 8: 71–77; http://dx.doi.org/10.4322/natcon.00801011
Ribeiro, M.C., J.P. Metzger, A.C. Martensen, F.J. Ponzoni & M.M. Hirota (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological conservation 142: 1141–1153; http://dx.doi.org/10.1016/j.biocon.2009.02.021
Rodrigues, M.T. (2005). The conservation of Brazilian reptiles: challenges for a megadiverse country. Conservation Biology 19: 659–664; http://dx.doi.org/10.1111/j.1523-1739.2005.00690.x
Sasa-Marín, M., D.K. Wasko, & W.W. Lamar (2009). Natural history of the terciopelo Bothrops asper (Serpentes: Viperidae) in Costa Rica. Toxicon 54(7): 904–922; http://dx.doi.org/10.1016/j.toxicon.2009.06.024
Sazima, I. (1991). Caudal luring in two Neotropical Pitvipers, Bothrops jararaca and B. jararacussu. Copeia 1: 245–248; http://dx.doi.org/10.2307/1446274
Sazima, I. (2006). Theatrical frogs and crafty snakes: predation of visually-signalling frogs by tail-luring and ambushing pitvipers. Aqua 11: 117–124.
Shine, R. (1994). Allometric patterns in the ecology of Australian snakes. Copeia 1994: 851–867; http://dx.doi.org/10.2307/1446709
SOSMA (SOS Mata Atlântica) /INPE (Instituto Nacional de Pesquisas Espaciais) (2013). Atlas dos remanescentes florestais da Mata Atlântica periodo 2011–2012. Fundação SOS Mata Atlântica/Instituto Nacional de Pesquisas Espaciais. São Paulo, Brazil.
Teixeira, S.S., L.B. Silveira, F.M. da Silva, D.P. Marchi-Salvador, F.P. Silva Jr, L.F.M. Izidoro, A.L. Fuly, M.A. Juliano, C.R. dos Santos & M.T. Murakami (2011). Molecular characterization of an acidic phospholipase A2 from Bothrops pirajai snake venom: synthetic C-terminal peptide identifies its antiplatelet region. Archives of toxicology 85: 1219–1233; http://dx.doi.org/10.1007/s00204-011-0665-6