Advertisement

Effects of anthropogenic land-use on scorpions (Arachnida: Scorpiones) in Neotropical forests

  • André F. A. LiraEmail author
  • Laís M. Pordeus
  • Renato P. Salomão
  • Raúl Badillo-Montaño
  • Cleide M. R. Albuquerque
Original Research Article

Abstract

Changes in land-cover driven by human activities is one of the main causes of disturbances on natural communities but the impact of this factor on scorpions assemblages remains scarcely know. Here we analyzed the scorpion fauna in five tropical forests and their respective neighboring non-natural matrix (planted forests or crops) in Brazil (n = 4) and Mexico (n = 1), aiming to understand how different species of scorpions respond to land-use changes. Scorpions were actively collected with the help of a UV flashlight. A total of 461 individuals were sampled, belonging to nine species and seven genera distributed in three families Buthidae, Bothriuridae and Diplocentridae. Differences in assemblages between environments were found, with higher gamma diversity in undisturbed environments where species showed the highest abundance. A higher species turnover was found in disturbed environments. Based on these results, we suggest a differential sensitive reaction to habitat alterations amongst scorpions species.

Keywords

Surrounding matrix Native ecosystem Community ecology Arthropods 

Notes

Acknowledgements

We are grateful to ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ (CAPES) for granting a PhD scholarship to A.F.A. Lira. We are also very grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a research productivity funding (Fellowship#307759/2015-6) to C.M.R. Albuquerque. We also thank ‘Consejo Nacional de Ciencias y Tecnología’ (CONACYT) for the PhD scholarships of R. Badillo-Montaño and R.P. Salomão. The material collection in Brazil was partially supported by FACEPE (Fundação de Amparo a Ciência e Tecnologia de Pernambuco- (APQ-0437-2.04/15). We are indebted to Dr. Oscar F. Francke Ballvé, for the identification of Mexican scorpions and comments on the previous version of this manuscript. We also grateful to Eurico Lustosa and Dr. Gilberto G. Rodrigues for their permission to collect samples and to Welton Dionisio-da-Silva, Eder Barbier, Ingrid Tiburcio and Jonathas C. Araújo for their technical assistance during fieldwork.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abensperg-Traun M, Smith GT (1999) How small is too small for small animals? Four terrestrial arthropod species in different sized remnant woodlands in agricultural Western Australia. Biodivers Conserv 8:709–726.  https://doi.org/10.1023/A:1008826114741 CrossRefGoogle Scholar
  2. Araújo PG, Miranda GEC, Kanagawa AI (2008) Repartição espacial da comunidade macrobêntica dos recifes da APA da Barra do Rio Mamanguape, Paraíba, Brasil. Rev Nordest Biol 19:29–50Google Scholar
  3. Ayres M, Ayres Júnior M, Ayres DL, Santos AA (2007) BIOESTAT – aplicações estatísticas nas áreas das ciências biomédicas. ONG Mamirauá, BelémGoogle Scholar
  4. Bibbs CS, Bengston SE, Gouge DH (2014) Activity trends and movement distances in the Arizona bark scorpion (Scorpiones: Buthidae). Environ Entomol 43:1613–1620.  https://doi.org/10.1603/EN14148 CrossRefGoogle Scholar
  5. Bogyó D, Magura T, Nagy DD, Tóthmérész B (2015) Distribution of millipedes (Myriapoda, Diplopoda) along a forest interior – forest edge – grassland habitat complex. Zookeys 510:181–195.  https://doi.org/10.3897/zookeys.510.8657 CrossRefGoogle Scholar
  6. Cagnolo L, Valladares G, Salvo A, Cabido M, Zak M (2009) Habitat fragmentation and species loss across three interacting trophic levels: effects of life-history and food-web traits. Conserv Biol 23:1167–1175.  https://doi.org/10.1111/j.1523-1739.2009.01214.x CrossRefGoogle Scholar
  7. Cala-Riquelme F, Colombo M (2011) Ecology of the scorpion, Microtityus jaumei in sierra de canasta. Cuba J Insect Sci 11:86–95.  https://doi.org/10.1673/031.011.8601 Google Scholar
  8. Campos-Navarrete MJ, Munguía-Rosas MA, Abdala-Roberts L, Quinto J, Parra-Tabla V (2015) Effects of tree genotypic diversity and species diversity on the arthropod community associated with big-leaf mahogany. Biotropica 47:579–587.  https://doi.org/10.1111/btp.12250 CrossRefGoogle Scholar
  9. Chakravarty S, Ghosh SK, Suresh CP, Dey AN, Shukla G (2012) Deforestation: causes, effects and control strategies. In: Okia CA (ed) Global perspectives on sustainable Forest management. InTech, Rijeka, pp 3–28Google Scholar
  10. Climate-data (2017a) Available at <https://pt.climate-data.org/location/43059/>. Accessed 18 Feb 2017
  11. Climate-data (2017b) Available at <https://pt.climate-data.org/location/43066/>. Accessed 18 Feb 2017
  12. Davis ALV, Scholtz CH, Swemmer AS (2012) Effects of land usage on dung beetle assemblage structure: Kruger National Park versus adjacent farmland in South Africa. J Insect Conserv 16:399–411.  https://doi.org/10.1007/s10841-011-9426-3 CrossRefGoogle Scholar
  13. Debruyn LAL (1993) Defining soil macrofauna composition and activity for biopedological studies-a case study on two soils in the Western Australian wheat belt. Soil Res 31:83–95.  https://doi.org/10.1071/SR9930083 CrossRefGoogle Scholar
  14. Dionisio-da-Silva W, Lira AFA, Albuquerque CMR (2018) Distinct edge effects and reproductive periods of sympatric litter-dwelling scorpions (Arachnida: Scorpiones) in a Brazilian Atlantic forest. Zoology 129:17–24.  https://doi.org/10.1016/j.zool.2018.06.001 CrossRefGoogle Scholar
  15. Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167.  https://doi.org/10.1146/annurev.energy.28.050302.105532 CrossRefGoogle Scholar
  16. Durán-García R, García-Contreras G (2010) Distribución espacial de la vegetación. In: Durán-Garcia R, Méndez-González M (eds) Biodiversidad y Desarrollo Humano en Yucatán. Seduma, Yucatán, pp 131–135Google Scholar
  17. Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142.  https://doi.org/10.1017/S1464793105006949 CrossRefGoogle Scholar
  18. Filgueiras BKC, Melo DHA, Leal IR, Tabarelli M, Freitas AVL, Iannuzzi L (2016a) Fruit-feeding butterflies in edge-dominated habitats: community structure, species persistence and cascade effect. J Insect Conserv 20:539–548.  https://doi.org/10.1007/s10841-016-9888-4 CrossRefGoogle Scholar
  19. Filgueiras BKC, Tabarelli M, Leal IR, Vaz-de-Mello FZ, Peres CA, Iannuzzi L (2016b) Spatial replacement of dung beetles in edge-affected habitats: biotic homogenization or divergence in fragmented tropical forest landscapes? Divers Distrib 22:400–409.  https://doi.org/10.1111/ddi.12410 CrossRefGoogle Scholar
  20. Filgueiras BKC, Melo DHA, Andersen AN, Tabarelli M, Leal IR (2019) Cross-taxon congruence in insect responses to fragmentation of Brazilian Atlantic forest. Ecol Indic 98:523–530.  https://doi.org/10.1016/j.ecolind.2018.11.036 CrossRefGoogle Scholar
  21. Guzmán PVM, Ponce-Saavedra J (2014) Actividad superficial de Centruroides ornatus Pocock, 1902 (Scorpiones: Buthidae) en época de lluvias en la cuenca de Cuitzeo. Entomol Mex 1:49–52Google Scholar
  22. Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432.  https://doi.org/10.2307/1934352 CrossRefGoogle Scholar
  23. IBGE (1985) Atlas Nacional do Brasil: Região Nordeste. IBGE, Rio de JaneiroGoogle Scholar
  24. ICMBio (2015) Instituto Chico Mendes de Conservação da Biodiversidade. Available at <http://www.icmbio.gov.br/portal>. Accessed 12 Dec 2015
  25. INEGI (2009) Prontuario de información geográfica municipal de los Estados Unidos Mexicanos Muna, Yucatán. Available at: http://www3.inegi.org.mx/sistemas/mexicocifras/datos-geograficos/31/31053.pdf
  26. Jost L (2006) Entropy and diversity. Oikos 113:363–375.  https://doi.org/10.1111/j.2006.0030-1299.14714.x CrossRefGoogle Scholar
  27. Leal IR, Tabarelli M, Da Silva JMC (2003) Ecologia e conservação da Caatinga. Editora Universitária, RecifeGoogle Scholar
  28. Lewis SL, Lloyd J, Sitch S, Mitchard ETA, Laurance WF (2009) Changing ecology of tropical forests: evidence and drivers. Annu Rev Ecol Evol Syst 40:529–549.  https://doi.org/10.1146/annurev.ecolsys.39.110707.173345 CrossRefGoogle Scholar
  29. Lira AFA, Souza AM, Costa AASS, Albuquerque CMR (2013) Spatio-temporal microhabitat use by two co-occurring species of scorpions in Atlantic rainforest in Brazil. Zoology 116:182–185.  https://doi.org/10.1016/j.zool.2013.01.002 CrossRefGoogle Scholar
  30. Lira AFA, Rego FNAA, Albuquerque CMR (2015) How important are environmental factors for the population structure of co-occurring scorpion species in a tropical forest? Can J Zool 93:15–19.  https://doi.org/10.1139/cjz-2014-0238 CrossRefGoogle Scholar
  31. Lira AFA, Araújo VLN, DeSouza AM, Rego FNAA, Albuquerque CMR (2016) The effect of habitat fragmentation on the scorpion assemblage of a Brazilian Atlantic Forest. J Insect Conserv 20:457–466.  https://doi.org/10.1007/s10841-016-9878-6 CrossRefGoogle Scholar
  32. Lira AFA, Damasceno EM, Silva-Filho AC, Albuquerque CMR (2017a) Linking scorpion (Arachnida: Scorpiones) assemblage with fragment restoration in the Brazilian Atlantic Forest. Stud Neotropical Fauna Environ 53:107–112.  https://doi.org/10.1080/01650521.2017.1413823 CrossRefGoogle Scholar
  33. Lira AFA, Pordeus LM, Barbier E, Rodrigues GG (2017b) Scorpions (Arachnida, Scorpiones) of an Atlantic forest fragment in the coastal northeastern Brazil: Barra of Mamanguape river protected area. Arachnida 13:22–30Google Scholar
  34. Lira AFA, DeSouza AM, Albuquerque CMR (2018) Environmental variation and seasonal changes as determinants of the spatial distribution of scorpions (Arachnida: Scorpiones) in Neotropical forests. Can J Zool 96:963–972.  https://doi.org/10.1139/cjz-2017-0251.
  35. Lisboa EBF, Moura GJB, Melo IVC, Andrade EVE, Figuerêdo Júnior JM (2011) Aspectos ecológicos de Hypsiboas semilineatus (Spix, 1824) (Amphibia, Anura, Hylidae) em fragmento de Mata Atlântica, nordeste do Brasil. Rev Iber Amer Ciênc Amb 2:21–30.  https://doi.org/10.6008/ESS2179-6858.2011.001.0002 Google Scholar
  36. Lôbo D, Leão T, Melo FPL, Santos AMM, Tabarelli M (2011) Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Divers Distrib 17:287–296.  https://doi.org/10.1111/j.1472-4642.2010.00739.x CrossRefGoogle Scholar
  37. Lo-Man-Hung NF, Marichal R, Candiani DF, Carvalho LS, Indicatti RP, Bonaldo AB, Cobo DHR, Feijoo AM, Tselouiko S, Praxedes C, Brown G, Velasquez E, Decaëns T, Oszwald J, Martins M, Lavelle P (2011) Impact of different land management on soil spiders (Arachnida: Araneae) in two Amazonian areas of Brazil and Colombia. J Arachnol 39:296–302.  https://doi.org/10.1636/CP10-89.1 CrossRefGoogle Scholar
  38. Lopes IS, Feliciano ANP, Marangon LC, Alencar AL (2016) Dynamics of natural regeneration in the understory of Pinus caribaea Morelet. Var. caribaea in biological reserve Saltinho. Tamandaré – PE Ciênc Florest 26:95–107.  https://doi.org/10.5902/1980509821094 Google Scholar
  39. Lourenço WR (2002) Scorpions of Brazil. Les Édition de I’lf, ParisGoogle Scholar
  40. Mcreynolds CN (2008) Microhabitat preferences for the errant scorpion, Centruroides vittatus (Scorpiones, Buthidae). J Arachnol 36:557–564.  https://doi.org/10.1636/T07-07.1 CrossRefGoogle Scholar
  41. Medianero E, Castaño-Meneses G, Tishechkin V, Basset Y, Barrios H, Ødegaard F, Cline AR, Bail J (2007) Influence of local illumination and plant composition on the spatial and seasonal distribution of litter dwelling arthropods in a tropical rainforest. Pedobiol 51:131–145.  https://doi.org/10.1016/j.pedobi.2007.03.004 CrossRefGoogle Scholar
  42. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858.  https://doi.org/10.1038/35002501 CrossRefGoogle Scholar
  43. Nime MF, Casanoves F, Mattoni CI (2014) Scorpion diversity in two different habitats in the arid Chaco, Argentina. J Insect Conserv 18:373–384.  https://doi.org/10.1007/s10841-014-9646-4 CrossRefGoogle Scholar
  44. Pardini R, Faria D, Accacio GM, Laps RR, Mariano-Neto E, Paciencia MLB, Dixo J, Baumgarten J (2009) The challenge of maintaining Atlantic forest biodiversity: a multi-taxa conservation assessment of specialist and generalista species in na agro-forestry mosaic in southern Bahia. Biol Conserv 142:1178–1190.  https://doi.org/10.1016/j.biocon.2009.02.010 CrossRefGoogle Scholar
  45. Pereira MS, Alves RRN (2007) Composição Florística de um remanescente de Mata Atlântica na Área de Proteção Ambiental Barra do Rio Mamanguape, Paraíba. Brasil Rev Biol Ciênc Terra 6:357–366Google Scholar
  46. Perry KI, Herms DA (2017) Responses of ground-dwelling invertebrates to gap formation and accumulation of Woody debris from invasive species, wind, and salvage logging. Forests 8:1–13.  https://doi.org/10.3390/f8050174 Google Scholar
  47. Pinkus-Rendón MA, Manrique-Saide P, Delfín-González H (1999) Alacranes sinantrópicos de Mérida, Yucatán, México. Rev Biomed 10:153–158.  https://doi.org/10.32776/revbiomed.v10i3.198 Google Scholar
  48. Polis GA (1990) The biology of scorpions. Stanford University Press, StanfordGoogle Scholar
  49. Ponce-Saavedra J, Francke OF, Suzán H (2013) Actividad superficial y utilización del hábitat por Centruroides balsasensis Ponce y Francke (Scorpiones: Buthidae). Biológicas 8:130–137Google Scholar
  50. Ramírez-Arce D (2015) Uso del hábitat y actividad superficial del escorpión Centruroides margaritatus en el Parque Nacional Palo Verde, Guanacaste, Costa Rica. Cuad Investig 7:279–286Google Scholar
  51. Ranta P, Blom T, Niemela J, Joensuu E, Siitonen M (1998) The fragmented Atlantic rain forest of Brazil: size, shape and distribution of forest fragments. Biodivers Conserv 7:385–403.  https://doi.org/10.1023/A:1008885813543 CrossRefGoogle Scholar
  52. Ribeiro-Neto JD, Arnan X, Tabarelli M, Leal IR (2016) Chronic anthropogenic disturbance causes homogenization of plant and ant communities in the Brazilian Caatinga. Biodivers Conserv 25:943–956.  https://doi.org/10.1007/s10531-016-1099-5 CrossRefGoogle Scholar
  53. Santos BA, Arroyo-Rodríguez V, Moreno CE, Tabarelli M (2010) Edge-related loss of tree phylogenetic diversity in the severely fragmented Brazilian Atlantic Forest. PLoS One 5:e12625.  https://doi.org/10.1371/journal.pone.0012625 CrossRefGoogle Scholar
  54. Santos-Da-Silva ADP, Carvalho LS, Brescovit AD (2017) Two new species of Bothriurus Peters, 1861 (Scorpiones, Bothriuridae) from northeastern Brazil. Zootaxa 4258:238–256.  https://doi.org/10.11646/zootaxa.4258.3.2 CrossRefGoogle Scholar
  55. Silva SO, Ferreira RLC, Silva JAA, Lira MA, Alves Junior FT, Cano MOO, Torres JEL (2012) Advanced natural regeneration in a Caatinga remainder with different descriptions of use in the agreste of Pernambuco. Brazil Rev Árvore 36:441–450.  https://doi.org/10.1590/S0100-67622012000300006 CrossRefGoogle Scholar
  56. Smith GT (1995) Species richness, habitat and conservation of scorpions in the Western Australian wheatbelt. Rec W Austr Mus 52:55–66Google Scholar
  57. Teixeira LJ (2009) Fitossociologia e florística do componente arbóreo em toposseqüência na reserva biológica de Saltinho, Pernambuco. Dissertation, Universidade Federal Rural de PernambucoGoogle Scholar
  58. van der Putten WH, Ruiter PC, Bezemer TM, Harvey JA, Wassen M, Wolters V (2004) Trophic interactions in a changing world. Basic Appl Ecol 5:487–494.  https://doi.org/10.1016/j.baae.2004.09.003 CrossRefGoogle Scholar
  59. Velloso AL, Sampaio EVSB, Pareyn FGC (2002) Ecorregiões propostas para o bioma Caatinga. Associação Plantas do Nordeste, RecifeGoogle Scholar
  60. Wright SJ (2005) Tropical forests in a changing environment. Trends Ecol Evol 20:553–560.  https://doi.org/10.1016/j.tree.2005.07.009 CrossRefGoogle Scholar

Copyright information

© African Association of Insect Scientists 2019

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Biologia Animal, Departamento de ZoologiaUniversidade Federal de Pernambuco – UFPERecifeBrazil
  2. 2.Red de EcoetologíaInstituto de Ecología A.C. Carretera Antigua a Coatepec 351VeracruzMexico
  3. 3.Red de Estudios Moleculares AvanzadosInstituto de Ecología A.C. Carretera Antigua a Coatepec 351VeracruzMexico

Personalised recommendations