Advertisement

Journal of Insect Conservation

, Volume 22, Issue 3–4, pp 627–633 | Cite as

Challenges to the conservation of stingless bees in Atlantic Forest patches: old approaches, new applications

  • Mariana Victorino Nicolosi Arena
  • Fábio Camacho Destéfani
  • Tiago Nunes da Silva
  • Júlio César da Silva Mascotti
  • Elaine Cristina Mathias da Silva-ZacarinEmail author
  • Rogério Hartung ToppaEmail author
ORIGINAL PAPER
  • 154 Downloads

Abstract

Fragmentation is one of the many threats that leads to the decline in the population of bees, and stingless bees compose the most abundant pollinator group in the neotropical rain forests. Considering the importance of forested areas to the presence of bees that forage above the ground and nest in trees, this study aimed to discuss the effectiveness of artificial bee shelters as a strategy for the conservation of stingless bees in fragmented habitats. Artificial bee shelters (n = 72) were installed in Atlantic Forest patches and were monitored for 8 months. Four (5.5%) artificial shelters were successfully colonized by Scaptotrigona postica (Latreille, 1807) and 23 (32%) shelters contained signs of initial colonization or traces of dead stingless bees. Difficulties faced by the bees in colonizing the artificial bee shelters included water accumulation, predation, and occupation by other species. The occurrence of Scaptotrigona bees may be related to the group’s need to nest in the hollows of living trees. The artificial shelters supported the swarming of Scaptotrigona bees by providing nesting sites that assisted in their self-maintenance in highly fragmented forest patches with scarce adequate nesting sites. The use of artificial bee shelters can be a strategy for studying stingless bees in their natural environment and for evaluating conservation strategies.

Keywords

Trap-nests Meliponini Scaptotrigona Artificial bee shelters Fragmentation Bee’s swarming 

Notes

Acknowledgements

We are thankful to SISBIO which authorized the collection of bees; to Dr. Favízia Freitas de Oliveira (Institute of Biology, Federal University of Bahia) for identifying the bees and to Dr. Cláudia Inês da Silva (Institute of Biology, University of São Paulo) for all the assistance provided; to all the land owners who cordially authorized the survey to be taken in their properties; to the farm caretakers who kindly received us; to Roberto from Meliponário Itu, who graciously provided us with a wealth of information; to Maria Virginia Urso Guimaraes and to Denise de Araujo Alves for the valuable notes to the article.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10841_2018_90_MOESM1_ESM.doc (2.5 mb)
Supplementary material 1 (DOC 2510 KB). Study area.
10841_2018_90_MOESM2_ESM.kml (270 kb)
Supplementary material 2 (KML 270 KB). Study patches.
10841_2018_90_MOESM3_ESM.doc (12.8 mb)
Supplementary material 3 (DOC 13118 KB). Artificial shelters.

Supplementary material 4 (MP4 42257 KB). Colonized artificial shelter.

References

  1. Aleixo KP, Menezes C, Imperatriz Fonseca VL, da Silva CI (2016) Seasonal availability of floral resources and ambient temperature shape stingless bee foraging behavior (Scaptotrigona aff. depilis). Apidologie 48:117–127.  https://doi.org/10.1007/s13592-016-0456-4 CrossRefGoogle Scholar
  2. Arena MVN, Martines MR, da Silva TN. Destéfani FC, Mascotti JCS, Silva-Zacarin ECM, Toppa RH (2018) Multiple-scale approach for evaluating the occupation of stingless bees in Atlantic forest patches. For Ecol Manage 430:509–516.  https://doi.org/10.1016/j.foreco.2018.08.038 CrossRefGoogle Scholar
  3. Batista MA, Ramalho M, Soares AEE (2003) Nesting sites and abundance of Meliponini (Hymenoptera: Apidae) in heterogeneous habitats of the Atlantic Rain Forest. Bahia Brazil Lundiana 4:19–23Google Scholar
  4. Baum K, Haynes KJ, Dillemuth FP, Cronin JT (2004) The matrix enhances the effectiveness of corridors and stepping stones. Ecology 85:2671–2676.  https://doi.org/10.1890/04-0500 CrossRefGoogle Scholar
  5. Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annu Rev Ecol Syst 21:399–422.  https://doi.org/10.1146/annurev.ecolsys.21.1.399 CrossRefGoogle Scholar
  6. Boscolo D, Candia-Gallardo C, Awade M, Metzger JP (2008) Importance of interhabitat gaps and stepping-stones for lesser woodcreepers (Xiphorhynchus fuscus) in the Atlantic Forest, Brazil. Biotropica 40:273–276.  https://doi.org/10.1111/j.1744-7429.2008.00409.x CrossRefGoogle Scholar
  7. Brosi BJ (2009) The complex responses of social stingless bees (Apidae: Meliponini) to tropical deforestation. For Ecol Manage 258:1830–1837.  https://doi.org/10.1016/j.foreco.2009.02.025 CrossRefGoogle Scholar
  8. Brown JC, Albrecht C (2001) The effect of tropical deforestation on stingless bees of the genus Melipona (Insecta: Hymenoptera: Apidae: Meliponini) in central Rondonia. Brazil J Biogeogr 28:623–634.  https://doi.org/10.1046/j.1365-2699.2001.00583.x CrossRefGoogle Scholar
  9. Centro de Pesquisas Meteorológicas e Climáticas Aplicadas a Agricultura - CEPAGRI (2017) Clima dos Municípios Paulistas. Centro de Pesquisas Meteorológicas e Climáticas aplicadas a Agricultura. http://www.cpa.unicamp.br/outras-informacoes/clima_muni_511.html. Accessed 05 June 2017
  10. Eltz T, Brühl CA, Imiyabir Z, Linsenmair KE (2003) Nesting and nest trees of stingless bees (Apidae: Meliponini) in lowland dipterocarp forests in Sabah, Malaysia, with implications for forest management. For Ecol Manag 172:301–313.  https://doi.org/10.1016/S0378-1127(01)00792-7 CrossRefGoogle Scholar
  11. Engels W (1990) Social insects: an evolutionary approach to castes and reproduction. Springer, New York, 265 ppCrossRefGoogle Scholar
  12. Engels W, Rosenkranz P, Engels E (1995) Thermoregulation in the nest of the Neotropical Stingless bee Scaptotrigona postica and a hypothesis on the evolution of temperature homeostasis in highly Eusocial bees. Stud Neotrop Fauna Environ 39:193–205.  https://doi.org/10.1080/01650529509360958 CrossRefGoogle Scholar
  13. Ferreira PA, Boscolo D, Carvalheiro LG, Biesmeijer JC, Rocha PLB, Viana BF (2015) Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic Rainforest. Landsc Ecol 30:2067–2078.  https://doi.org/10.1007/s10980-015-0231-3 CrossRefGoogle Scholar
  14. Gillies CS, Beyer HL, St. Clair CC (2011) Fine-scale movement decisions of tropical forest birds in a fragmented landscape. Ecol Appl 21:944–954.  https://doi.org/10.1890/09-2090.1 CrossRefPubMedGoogle Scholar
  15. Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957.  https://doi.org/10.1126/science.1255957 CrossRefPubMedGoogle Scholar
  16. Haddad NM (2000) Corridor length and patch colonization by a butterfly, Junonia coenia. Conserv Biol 14:738–745.  https://doi.org/10.1046/j.1523-1739.2000.99041.x CrossRefGoogle Scholar
  17. Instituto Nacional de Meteorologia—INMET (2017) Consulta Dados da Estação Automática: Sorocaba (SP). http://www.inmet.gov.br/portal/index.php?r=estacoes/estacoesAutomaticas. Accessed on 27 July 2017
  18. Kerr WE, Nascimento VA, Carvalho GA (1999) Preservation of native Brazilian bees: a question of historical and ecological conscience. Ciência e cultura 51:390–393Google Scholar
  19. Klein AM, Steffan-Dewenter I, Buchori D, Tscharntke T (2002) Effects of land-use intensity in tropical agroforestry systems on coffee flower-visiting and trap-nesting bees and wasps. Conserv Biol 16:1003–1014.  https://doi.org/10.1046/j.1523-1739.2002.00499.x CrossRefGoogle Scholar
  20. Macieira OJD, Proni EA (2004) Capacidade de resistência a altas e baixas temperaturas em operárias de Scaptotrigona postica (Latreille) (Hymenoptera, Apidae) durante os períodos de verão e inverno. Rev Bras Zool 21:893–896.  https://doi.org/10.1590/S0101-81752004000400025 CrossRefGoogle Scholar
  21. Mandujano S, Escobedo-Morales LA, Palacios-Silva R (2004) Movements of Alouatta palliata among forest fragments in Los Tuxtlas, Mexico. Neotrop Primates 12:126–131.  https://doi.org/10.1896/1413-4705.12.3.126 CrossRefGoogle Scholar
  22. Matlack GR (1993) Sociological edge effects: spatial distribution of human impact in suburban forest fragments. Environ Manage 17:829–835.  https://doi.org/10.1007/BF02393903 CrossRefGoogle Scholar
  23. Matos MCB, Sousa-Souto L, Almeida RS, Teodoro AV (2012) Contrasting patterns of species richness and composition of solitary wasps and bees (Insecta: Hymenoptera) According to Land-use. Biotropica 0:1–7Google Scholar
  24. Michener CD (2007) The bees of the world. JHU Press, Baltimor, p 963Google Scholar
  25. Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62.  https://doi.org/10.1016/S0169-5347(00)88977-6 CrossRefGoogle Scholar
  26. Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858.  https://doi.org/10.1038/35002501 CrossRefGoogle Scholar
  27. Nogueira-Neto P (1997) Vida e Criação de Abelhas Indígenas Sem Ferrão. Nogueirapis, São Paulo, p 445Google Scholar
  28. Oliveira RC, Menezes C, Soares AEE, Fonseca VLI (2013) Trap-nests for stingless bees (Hymenoptera, Meliponini). Apidologie 44:29–37.  https://doi.org/10.1007/s13592-012-0152-y CrossRefGoogle Scholar
  29. Pires VR, de Garcia MA, Martines MR, Toppa RH (2016a) Land use and occupation mapping as support to environmental planning. Ambiência 12:899–908.  https://doi.org/10.5935/ambiencia.2016.Especial.15 CrossRefGoogle Scholar
  30. Pires VR, de Garcia MA, Martines MR, Toppa RH (2016b) Landscape structure analysis for the establishment of conservation strategies in Atlantic Forest patches. Ambiência 12:765–774.  https://doi.org/10.5935/ambiencia.2016.Especial.01 CrossRefGoogle Scholar
  31. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353.  https://doi.org/10.1016/j.tree.2010.01.007 CrossRefGoogle Scholar
  32. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153.  https://doi.org/10.1016/j.biocon.2009.02.021 CrossRefGoogle Scholar
  33. Roberts HP, King DI, Milam J (2017) Factors affecting bee communities in forest openings and adjacent mature forest. For Ecol Manage 394:111–122.  https://doi.org/10.1016/j.foreco.2017.03.027 CrossRefGoogle Scholar
  34. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New YorkCrossRefGoogle Scholar
  35. Saura S, Bodin Ö, Fortin MJ (2014) Stepping stones are crucial for species’ long-distance dispersal and range expansion through habitat networks. J Appl Ecol 51:171–182.  https://doi.org/10.1111/1365-2664.12179 CrossRefGoogle Scholar
  36. Silva MD, Ramalho M, Monteiro D (2014) Communities of Social Bees (Apidae: Meliponini) in Trap-Nests: the spatial dynamics of reproduction in an area of Atlantic forest. Neotrop Entomol 43:307–313.  https://doi.org/10.1007/s13744-014-0219-8 CrossRefPubMedGoogle Scholar
  37. Siqueira ENL, Bartelli BF, Nascimento ART, Nogueira-Ferreira FH (2012) Diversity and nesting substrates of stingless bees (Hymenoptera, Meliponina) in a forest remnant. Psyche (New York) 2012:1–9.  https://doi.org/10.1155/2012/370895 CrossRefGoogle Scholar
  38. Slaa EJ (2006) Population dynamics of a stingless bee community in the seasonal dry lowlands of Costa Rica. Insects Soc 53:70–79.  https://doi.org/10.1007/s00040-005-0837-6 CrossRefGoogle Scholar
  39. Stangler ES, Hanson PE, Steffan-Dewenter I (2016) Vertical diversity patterns and biotic interactions of trap-nesting bees along a fragmentation gradient of small secondary rainforest remnants. Apidologie 47:527–538.  https://doi.org/10.1007/s13592-015-0397-3 CrossRefGoogle Scholar
  40. Storck-Tonon D, Peres CA (2017) Forest patch isolation drives local extinctions of Amazonian orchid bees in a 26 years old archipelago. Biol Conserv 214:270–277.  https://doi.org/10.1016/j.biocon.2017.07.018 CrossRefGoogle Scholar
  41. Van Rossum F, Ludwig T (2012) Stepping-stone populations in linear landscape elements increase pollen dispersal between urban forest fragments. Plant Ecol Evol 145:332–340.  https://doi.org/10.5091/plecevo.2012.737 CrossRefGoogle Scholar
  42. Vollet-Neto A, Koffler S, dos Santos CF, Menezes C, Nunes FMF, Hartfelder K, Imperatriz-Fonseca VL, Alves DA (2018) Recent advances in reproductive biology of stingless bees. Insectes Soc 65:201–212.  https://doi.org/10.1007/s00040-018-0607-x CrossRefGoogle Scholar
  43. Winfree R (2010) The conservation and restoration of wild bees. Ann NY Acad Sci 1195:169–197.  https://doi.org/10.1111/j.1749-6632.2010.05449.x CrossRefPubMedGoogle Scholar
  44. Zheng Q, Matis JH (1993) Some applications, properties and conjectures for higher order cumulants of a markovian stepping-stone model. Commun Stat Theory Methods 22:3305–3319.  https://doi.org/10.1080/03610929308831217 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Sustentabilidade na Gestão AmbientalUniversidade Federal de São CarlosSorocabaBrazil
  2. 2.Bacharelado em Ciências BiológicasUniversidade Federal de São CarlosSorocabaBrazil
  3. 3.Departamento de BiologiaUniversidade Federal de São CarlosSorocabaBrazil
  4. 4.Departamento de Ciências AmbientaisUniversidade Federal de São CarlosSorocabaBrazil
  5. 5.Universidade Federal de São Carlos, Rodovia João Leme dos Santos (SP-264)SorocabaBrazil

Personalised recommendations