Check List 10(6): 1331–1335, 2014 © 2014 Check List and Authors Chec List ISSN 1809-127X (available at www.biotaxa.org/cl) Journal of lists and distribution pecies S

of Diversity of (: Arachnida) in the 1

ists André Felipe de Araujo Lira L Atlantic Forest in Pernambuco, northeastern2 Brazil * and Cleide Maria Ribeiro de Albuquerque

1 Universidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Zoologia, Programa de Pós-Graduação em Biologia . Rua Prof. Moraes Rego S/N, Cidade Universitária, 50570-420. Recife, PE, Brasil. 2 Universidade Federal de Pernambuco,[email protected] Centro de Ciências Biológicas, Departamento de Zoologia. Rua Prof. Moraes Rego S/N, Cidade Universitária, 50570-420. Recife, PE, Brasil. * Corresponding author. E-mail: Abstract:

forest fragments This instudy Sirinhaém was conducted municipality, to measure Pernambuco the State, through of activescorpion searches species at nightin the by remnants using UV of lamps the Brazilianbetween northeastern Atlantic Forest, an important phase center of biodiversity and . Collections were performed in twelve pusillus mauryi Tityus brazilae 19:00h and 21:00h during theTityus new neglectus moon in December 2012 Tityusand January stigmurus 2013. A total of 1,125 specimens from two genera and five species were collected: Pocock,T. 1893; pusillus Lourenço,A. mauryi 1982; Tityus brazilaeEickstedt, T. & neglectus, Lourenço, and 1984; T. stigmurus Mello-Leitão, 1932; and (Thorell, 1876), all belonging to the C.L. Koch, 1837. The most abundant species was (90.7%), followed by (7.1%). together represented less than 3% of the individuals sampled.

DOI: 10.15560/10.6.1331

Introduction Atlantic Forest region, we surveyed the scorpions from twelve fragments of Atlantic Forest in Pernambuco to expand the knowledge of the fauna of this region. distributedThere areworldwide approximately except 1,900in known (Sissom species The study was performed in the fragments belonging to of scorpions (Stockman and Ythier 2010) that are Trapiche Mill as part of the project for the protection of its fragments. The data from the present work provide 1990). Approximately 50% of these species occuret al. in information for the continued maintenance of the Neotropical regions (Lourenço 2002a), including Brazil, remnants of the Atlantic Forest in Pernambuco. ofwhere roughly 130in all species environments are recorded where they (Porto live, the group2010). is Although poorly sampled scorpions and constitute little is known a successful about grouptheir Materials and Methods Study Area Atlantic forest (Dias et al. Field work was conducted in twelve fragments in the Forest,diversity an in important most ecoregions, center of particularlybiodiversity inand the endemism, Brazilian 2006). The Brazilian Atlantic cover and currently has only a few remnant fragments municipality of Sirinhaém (8°35′27″ S, 35°06′58″ W), in ofhas its suffered original aforest. significant These lossfragments of its nativeare isolated vegetation from the state of Pernambuco (Figure 1). Fragments, which are one another and are mostly surrounded by crops or Thesurrounded area is characterized by sugar cane, by rangeda mean annualfrom 6 temperatureto 469 ha and of pasture land (Mittermeier et al. were located at elevations of 20 to 120 m aboveet al.sea level.

et al. 2005). Approximately 25°C and an annual rainfall of 2,400 mm (Silva 2010). secondary83% of the forests remnant with fragments different are levels <50 haof andregeneration only 1% rainforests.We collected According samples during to the the Trapiche dry season. staff, Theremnants Trapiche in (Ribeiroare >100 et ha al (Ribeiro 2009). They are composed of thisMill areaowns have approximately been under 4,000 the landowners’ ha of dense protection ombrophilous over populations and can be food for invertebrates . 2009). Although predators regulate many highlighting scorpion species composition in the remnants Franciscothe last 10 River, years. in This the region states isof located Alagoas, in Pernambuco,the ‘Pernambuco Rio ofand the Atlantic Forest (Polis have 1990), been fewperformed ecological (Dias surveys et al. GrandeEndemism do Norte, Center’ and (PEC), Paraiba. situated north of the São et al. et al et al. et al Data collection 2006;Most studies Yamaguti on andarthropod Pinto dadiversity Rocha in 2006; this Bertanienvironment have2008; been Porto restricted . 2010; to Lirainsects (Santos 2013; etPorto al. . 2013). sampling units in each Trapiche fragment, making a total et al. et al. Six transects that were 20 m apart were used as (Resende et al. 2012; Souza Since 2013), no taxonomical (Melo or ecological 2011), records and harvestmenon scorpion Theof 72 scorpions sampling found units. up Each to 5transect m from was either 30 sidem long of each and 2012a, 2012b). placed randomly at least 200 m from the remnant edge. fauna were available from the Brazilian northeastern transect were collected resulting in a 300 m² sampling 1331 Lira and Albuquerque | Diversity of scorpions in the Atlantic forest

Figure 1.

Map showing the distribution of forest remnants in Trapiche Mill and the position of the 12 studied fragments. area. The scorpions were located by actively searching for them between 19 h and 21 h for one night for each remnant. Each transect was covered twice (round-trip) for 1 h by a pair of collectors equipped with lights (Figure 2). Active searches were made during the new moon phase, from December 2012 to January The2013 specimens (the dry were season). identified Each scorpionaccording collected to Lourenço was individually stored in a vial containing 70% ethanol. the(2002b). Universidade Voucher Federal specimens de (CA-UFPEPernambuco, #601 Recife. to 623) All scorpionswere deposited were collected in the by Arachnological the permission Collection of Instituto of individualsChico Mendes in the de leaf Conservaçãolitter, barks, logs, de and Biodiversidade bromeliads. Specimens(ICMBIO) #36336-1. were either The outside data correspondedor just emerging to activefrom Figure 2. Scorpion individual under ultraviolet radiation. Photo by André F. A. Lira.

Resultsthe refuges, as suggested by McReynolds (2008). exclusively in the leaf litter, while T. brazilae was found A list of species and their occurrences is presented in under bark in cracks, and inside their retreats showing extended and open chela. T. neglectus and T. stigmurus were found in logs and leaf litter. Table 1. A total of 1,125 scorpions were collected. They were Tityusfrom two genera and five T.species, brazilae all belongingLourenço to& theEickstedt, family Discussion ButhidaeT. C.L.pusillus Koch, 1837. Four speciesT. neglectus were from the T. C.L. stigmurus Koch, 1836 ( found. Sixteen species have been recorded in the Atlantic 1984;genus Ananteris Pocock, 1893;A. mauryi Mello-Leitão, In northeastern Brazil, 28 specieset al. of scorpionset areal. 1932;Photographs of the (Thorell,collected 1876) species and are one shown belonged in Figures to the 3 Tityus pusillus Thorell, and A. 1981 mauryi ( were recordedLourenço, in all twelve 1982). inForest Pernambuco. (Lourenço Dias 2002b, et al Dias 2006; Porto species2010). In in thisan urbanstudy, Atlanticone-third Forest of these fragment, species all was of whichfound and 4. were also found in this study.. (2006) found four scorpions followedfragments by (Table A. mauryi 1). The former was the most common Tityus pusillus was the most common species in all species, representing 90.7% of the total collected scorpions, fragments analyzed in the present work. The sedentary collected. The least common, representing species was 7.1%. T. stigmurus, The other which three habit and microhabitat preference of the surface litter wasspecies found together only in one represented fragment. onlyNo single 2.2% fragment of the scorpionshad more of this species are in agreement with Lira et al. and may facilitate sampling by active search, making this Tityus pusillus and Ananteris mauryi were collected species more visible and easier to capture. Tityus pusillus (2013) than three scorpion species (Table 1).

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northeast region and a high ecological plasticity, since they (Porto et al. were recorded from different environments such as rain (Diashas also et al. been recorded in the Atlantic Forest of Bahia forest and dry forest. 2010,et al. Brazil and Porto 2011) and Paraíba Ananteris mauryi, the second most common species 2006), as well as in the Caatinga (Bahia and in the present work, shows an errant habit, inhabiting Piauí) (Porto 2010, Brazil and Porto 2011). These the lower layers of leaf litter, as described previously by findings indicate a wide distribution of this species in the Lira et al. .They also show metasomal (Lira et al (2013) . 2014). This species was originally described from PEC. Later, it was found in the states of Bahia and Sergipe (Lourenço 2002b; Brazil and Porto 2011). Using

Figure 3. Tityus species collected in this study. A. Tityus brazilae Tityus neglectus Tityus pusillus and D. Adriano M. DeSouza and D by André F. A. Lira. B. , C. . Photographs A-C by Table 1.

Number of individuals, species of scorpions, and fragment size (in hectares) of each of the twelve studied fragments. Mata das cobras (MC), Pedra do cão (PC), Tauá (TA), Canto escuro (CE), Ubaca (UB), Canto escuro 2 (CE2), Xanguá (XA), Xanguá 2 (XA2), Franco 1 (FR1), Franco 2 (FR2), São SCORPION SPECIES PedroFRAGMENTS (SP), and BaquinhaAREA (BA). Ananteris mauryi Tityus brazilae Tityus neglectus Tityus pusillus Tityus stigmurus 3 — — 55 FR1 — — — FR2 6.43 4 3 — — — 8.27 16 37 — 5 — BA 10.53 37 — — CE2 18.52 2 86 33.51 1 — — — UB 20.67 2 2 7 1 — — PC 47 — 1 — MC 46.08 9 173 SP — — CE 75.80 6 50 3 — — 120.70 1 0 2 96 TA — — — XA2 197.52 4 177 — 1 — 280.33 9 2 Total 85 8 XA 469.76 20 150 7 920 4 1333 Lira and Albuquerque | Diversity of scorpions in the Atlantic forest a fragment of the Atlantic Forest, Dias et al thatpitfall A. traps mauryi to wassample the scorpionsmost abundant in Mata species. do Buraquinho, Although dominance changes are normal within the. (2006) distribution found of the species, differences in sampling methods may account for the variation observed in these studies because errant behavior may favor capture by pitfall traps. Tityus brazilae was found in four out of the twelve fragments. A previous study reports its presence in the extendedAtlantic Forest pedipalps from andRio deopen Janeiro chela, to which Paraíba corroborated (Brazil and Porto 2011). We observed a sit-and-wait behavior Despite with with the observations of Lira and DeSouza (2014). Therefore,their large it sizeis likely (50–70 that mm)their presence (Lourenço and 2002b), abundance this arebehavior underestimated. makes them difficult to be seen and captured. Tityus neglectus, was found in three out of the twelve fragments. This speciesAnother has largea wide species distribution (54–78 mm),in the northeast, and

et al et al. Itoccurs is associated from the with state bromeliads of Bahia toand Rio soil Grande (Lourenço do Norte and (Lourenço 2002b; Santoset al. . 2003; Dias 2006). of its microhabitat described in the literature, specimens collectedEickstedt in1988; this Santos study were 2003).collected Despite from thethe specificity leaf litter or logs. This suggests that sampling may have occurred Figure 4. Ananteris mauryi during the reproductive period when individuals leave specimen. Photograph by Arthur Costa. more males than females, which supports this hypothesis Acknowledgements: their microhabitats in search of mates. We also collected We are very grateful to Mário Jorge for permission Tityus stigmurus was the least common species and to use areas owned by the Trapiche Mill to collect samples. We thank the (data not shown). Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the MSc. scholarship for the first author. Thanks also to Evânia represent the less conserved. As a synantropic scorpion, valuableFreire, Renato comments Salomão, on previous Laís Pordeus, versions and of Lucas this manuscript. Cavalcanti for technical thisit was species collected may from be the adapted smallest to fragment. a more Whichdisturbed may assistance during the field work, and to two anonymous referees for environment. This species is found in most northeastern Literature Cited et al. Pediatric Epidemiological aspects of and report on Albuquerque,fatal cases C.M.R., due Tityus P.L.S. Neto,stigmurus M.L.P. Amorim and S.C.V. Pires. 2013. higheststates of number Brazil andof scorpion Minas Geraisstings in (De the Souza region, including2009; Journal of the Brazilian Society of Tropical Brazil and Porto 2011). It haset al. been responsible for the Medicine stings (Scorpiones: Buthidae) in Pernambuco, Brazil. Despite the great difference in size of the fragments, Tityus brazilae 64(4): 484–489 (doi: 10.1590/0037-8682-0089-2013). therechild mortalitywere no distribution(Albuquerque patterns 2013). among scorpions. No Bertani, R., R.H. Nagahama and D.R.M. Ortega. 2008. Novos Boletin registros de Lade scorpion species was found only in the larger fragments Sociedad EntomologicaLourenço Aragonesa and Eickstedt, 1984 (Scorpiones, ( Buthidae) para o Brasil e observações sobre o da espécie. and no fragment contained more than three species. Unlike 43: 513–515. http://www.sea- other groups, such as dung and ants, where the entomologia.org/PDF/BSEA43ARACNO/B43513.pdf). fragment size is important for species richness (Filgueiras Biondi-de-Queiroz, I. 1996. Estudo retrospectivo do escorpionismo na Região Metropolitana de Salvador (RMS)—Bahia, Brasil. Sitientibus et al. et al 15: 273–285 (http://www2.uefs.br/sitientibus/pdf/15/estudo_ Os Escorpiões. to be more important for scorpions. However, further retrospectivo_do_escorpionismo.pdf). 2010; Leal . 2012), environmental quality seems Brazil, T.K. and T.J. Porto. 2011. Salvador: EDUFBA. 83 p. Dias,a S.C.,population D.M. Candido of Ananteris and A. mauryiBrescovit. 2006. Scorpions from Mata do RevistaBuraquinho, Brasileira João de Pessoa, Zoologia Paraíba, Brazil, with ecological notes on isstudies an indicator are needed of high to confirm scorpion this. diversity. Therefore, the Lourenço (Scorpiones, Buthidae). fivePolis species (1990) reported suggests in the that Trapiche the presence landscape of six suggests species 23(3): 707–710Habitat (doi: 10.1590/S0101- fragmentation alters81752006000300014 the structure of). dung communities in the Atlantic high scorpion richness in this area. This fact underscores Filgueiras,Forest. B.Biological K., L. Ianuzzi Conservation and I.R. Leal. 2011. the importance of conservation of forest remnants to maintain scorpion fauna. Thus, the results presented 144: 362–369 (doi: 10.1016/j. Effectsbiocon.2010.09.013 of habitat fragmentation). on ant richness and functional here contribute to the knowledge of the diversity of Leal, I.R., B.K.C. Filgueiras, J.P. Gomes, L. IanuzziBiodiversity and A.N. andAndersen. Conservation 2012. scorpions in the Atlantic forest of Pernambuco and can serve as a basis for future research on the impact composition in Brazilian Atlantic forest. 21: 1687–1701 (doi: 10.1007/s10531-012-0271-9). of fragmentation on the population, distribution, and Lira, A.F.A., A.M. Souza, A.A.C. Silva Filho and C.M.R.Zoology Albuquerque.2013. ecology of scorpions. Spatio-temporal microhabitat use by two co-occurring species of scorpions in Atlantic rainforest in Brazil. 116(3): 182–185 (doi: 10.1016/j.zool.2013.01.002).

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Ananteris mauryi Biota Neotropica Lira, A.F.A., N.M.S. Sarinho, Journal A.M. De of SouzaInsect andBehavior C.M.R. Albuquerque. Carlos Botelho, and the Floresta Nacional de Ipanema, São Paulo, 2014. Metasomal autotomy in Lourenço, 1982 Brazil. 112(4): –10 (http://www.biotaneotropica. (Scorpiones: Buthidae). 27(2): 279–282 org.br/v12n4/pt/fullpaper?bn00712042012+en) (doi: 10.1007/s10905-013-9431-3). Ribeiro,forest M.C., distributed? J.P. Metzger, A.C.Implications Martensen, F.for Ponzoni conservation. and M.M. Hirota. Biological 2009. Lira,Revista A.F.A. and Ibérica A.M. de DeSouza. Aracnologia 2014. Microhabitat use by scorpion species BrazilianConservation Atlantic Forest: how much is left and how is the remaining (Arachnida: Scorpiones) in the montane Atlantic Rain Forest, Brazil. Amazonian Arachnida and : 24: 107–108. Identification Keys to All 142: 1141–1153 (doi: 10.1016/j.biocon.2009.02.021Tityus) Lourenço,Classes, W.R.Orders, 2002a. Families, Scorpiones; Some Genera pp. and 399–438, Lists of in:Known J. AdisTerrestrial (ed.). Santos,neglectus R.L., M.G. Almeida, J.V. Nunes, L.D.S. Tinoco and L.Journal B. Martins. of the Species. 2003.Bromeliad Bromeliads Society as a keystone resource for the scorpion Scorpions of Brazil in, A.F. eastern Rio Grande do NorteTorres. state, Brazil. Moscow: Pensoft Publishees. 53: 256–258. Lourenço,de Tityus W.R. 2002b. . Paris: Les Édition de I’lf. 308 pp.T. Santos, M.P.C.J. Carrano-Moreira and J. B. Revista 2012. Brasileira Diversity de Ciências of soil Lourenço,neglectus W.R. and V.R.D. Von Eickstedt. 1988. SinopseRevista dasBrasileira espécies de Agráriasant (Hymenoptera: Formicidae) in dense Atlantic Forest and sugarcane Zoologia do nordeste do Brasil, com a redescrição de plantations in the County of Igarassu-PE. Mello-Leitão (Scorpiones, Buthidae). 7(4): 648–656 (doi: 10.5039/agraria.v7i4a1927). 5: 399–408 (doi: 10.1590/S0101-81751988000300005). Silva, R.K.S., A.L.P. Feliciano, L.P. Marangon and R.B.A Lima.Revista 2010. Brasileira Florística de Lourenço, W.R. and V.R.D. Von Eickstedt. 2003.Animais Escorpiões Peçonhentos de Importância no Brasil: Ciênciase sucessão Agrárias ecológica da vegetação arbórea em área de nascente de Biologia,Médica; pp. Clínica 182–197, e Terapêutica in: J.L.C. dosCardoso, Acidentes F.O.S.. França, F.H. Wen, C.M.S. um fragmento de Mata Atlântica, Pernambuco. Málaque and V. Haddad Jr. (eds). 5(4): 550–559The Biology (doi: of 10.5039/agraria.v5i4a829 Scorpions ). vittatus SãoJournal Paulo: of Sarvier. Sissom,University W.D. 1990.Press. Systematics, Biogeography, and Paleontology; pp McReynolds, C.N. 2008. Microhabitat preferences for the errant scorpion, 31–80, in: G.A. Polis (ed). . Stanford: Stanford (Scorpiones, Buthidae). Tityus stigmurus Zootaxa 36(3): 557–564 (doi: 10.1636/T07-07.1). Souza, C.A.R., D.M. Candido, S.M. Lucas and A.D. Brescovit. 2009. On the Melo, T.S., A.R.S. Andrade,Sitientibus K.R. Benati, M.C.L., Peres and M.A. Dias. 2011. complex (Scorpiones, Buthidae). 1987: Panorama da araneofauna de fragmentos florestais The em Biology Salvador, of 1–38. Bahia,Scorpions Brasil.. Stanford, Stanford11(1): University 37–47. Press. Souza,Atlantic D.G., Forest B.A. Santos, landscape. R. Wirth, Environmental I. R. Leal Entomology and M. Tabarelli. 2013. Polis, G.A. 1990. Ecology, pp. 247–293, in: G.A. Polis (ed.). Community-level patterns of herbivory in a fragmented Check List Scorpions of the World42(3):. 430– Porto, T.J., T.K. Brazil and R.M. Lira da Silva. 2010. Scorpions, state of 437 (doi: 10.1603/EN12273). Bahia, northeast Brasil. 6(2): Evaluating 292–297 forest (http://www. refugial Stockmann, R. and Ythier, E. 2010. Paris:Thestylus NAP checklist.org.br/getpdf?SL021-09). editions.aurantiurus 572 pp. Porto, T.J., A.C. Carnaval and P.L.B. Rocha. 2013.Diversity and Distributions Yamaguti, H.Y.and R. Pinto-da-Rocha. Journal 2006. The of Arachnology ecology of models using species distribution models, model filling and inclusion: of the parque estadual da Serra da Cantareira, São Paulo, a case study with 14 Brazilian species. 19: Brazil (Scorpiones, ). 34: 214– 330–340 (doi: 10.1111/j.1472-4642.2012.00944.x). 220 (doi: 10.1636/T04-37.1). Resende, L.P.A., R. Pinto-da-RochaIheringia and C. Bragagnolo. 2012. Diversity of harvestmen (Arachnida, ) in Parque da Onça Parda, southeastern Brazil. 102(1): 99–105. (doi: 10.1590/S0073- Received: July 2013 47212012000100014). Accepted: October 2014 Ana Lúcia Tourinho Resende, L.P.A., R. Pinto-da-Rocha and C. Bragagnolo. 2012. The Published online: December 2014 harvestmen fauna (Arachnida: Opiliones) of the Parque Estadual Editorial responsibility:

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