Surveys of the bee (Hymenoptera: Apiformes) community in a Neotropical savanna using pan traps

Authors

  • Thaís Andrade Viana Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM), Faculdade de Ciências Biológicas e da Saúde (FCBS), Departamento de Ciências Biológicas (DCBIO) - Diamantina, MG, Brasil; Universidade Federal de Viçosa (UFV), Departamento de Entomologia (DDE) - Viçosa, MG, Brasil. Author http://orcid.org/0000-0001-8794-9275
  • Anete Pedro Lourenço Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM), Faculdade de Ciências Biológicas e da Saúde (FCBS), Departamento de Ciências Biológicas (DCBIO) - Diamantina, MG, Brasil. Author http://orcid.org/0000-0001-6929-7277

DOI:

https://doi.org/10.11606/1807-0205/2020.60.31

Keywords:

Callonychium, Dialictus, Wild bees, Cerrado, South America

Abstract

Bee populations are declining because of various synergistic threats, and therefore bee survey and monitoring programs are needed. Several techniques have been developed to survey bees, but the most cost-effective and suitable methods to sample bees in several sites at the same time are passive approaches, such as methods involving colored pan traps (also known as Moericke or bowl traps). Several bee surveys using pan traps have been conducted in North America, Europe, and Australia, but only a few such surveys have been done in tropical regions. We used colored pan traps (blue, yellow, and white) to assess the bee community in the Brazilian savanna ecosystem in Rio Preto State Park. Sampling was conducted in October 2013 and March 2014 along permanent trails. We also characterized the local habitat of each trail, and then we compared bee abundance with habitat complexity. In total, 187 individual bees (n = 15 species) were collected, mainly using blue and white traps. Although we were not able to sample most species that were previously recorded in this park, the pan trap method can be used to survey and monitor bee assemblages in combination with another sampling method. Habitat complexity also affected the numbers of bees sampled using the pan traps, and more bees were collected at open sites.

Downloads

Download data is not yet available.

Author Biographies

  • Thaís Andrade Viana, Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM), Faculdade de Ciências Biológicas e da Saúde (FCBS), Departamento de Ciências Biológicas (DCBIO) - Diamantina, MG, Brasil; Universidade Federal de Viçosa (UFV), Departamento de Entomologia (DDE) - Viçosa, MG, Brasil.

    Campus JK, Rodovia MGT 367, km 583, 5.000, Alto da Jacuba, CEP 39100-000, Diamantina, MG, Brasil.
    Avenida Peter Henry Rolfs, s/nº, Campus Universitário, CEP 36570-900, Viçosa, MG, Brasil.

  • Anete Pedro Lourenço, Universidade Federal dos Vales do Jequitinhonha e Mucuri (UFVJM), Faculdade de Ciências Biológicas e da Saúde (FCBS), Departamento de Ciências Biológicas (DCBIO) - Diamantina, MG, Brasil.

    Campus JK, Rodovia MGT 367, km 583, 5.000, Alto da Jacuba, CEP 39100-000, Diamantina, MG, Brasil.

References

Andena, S.R.; Nascimento, F.S.; Bispo, P.C.; Mechi, M.R.; Mateus, S. & Bego, L.R. 2009. Bee communities (Hymenoptera: Anthophila) of the “Cerrado” ecosystem in São Paulo State, Brazil. Genetics and Molecular Research, 8(2): 766-774. http://doi.org/10.4238/vol8-2kerr009

Antonini, Y.; Silveira, R.A.; Oliveira, M.L.; Martins, C. & Oliveira, R. 2016. Orchid bee fauna responds to habitat complexity on a savanna area (Cerrado) in Brazil. Sociobiology, 63(2): 819-825. http://doi.org/10.13102/sociobiology.v63i2.1038

Ayres, M.; Ayres Junior, M.; Ayres, D.L. & Santos, A.A. 2007. Bioestat-5.0: Aplicações estatísticas nas áreas das ciências bio-médicas. Belém, PA, Sociedade Civil Mamirauá/MCT-CNPQ. 364p. 1 CD-ROM

Azevedo, A.; Silveira, F.; Aguiar, C. & Pereira, V. 2008. Fauna de abelhas (Hymenoptera, Apoidea) nos campos rupestres da Cadeia do Espinhaço (Minas Gerais e Bahia, Brasil): riqueza de espécies, padrões. Megadiversidade, 4(1-2): 154-181.

Batalha, M.A.; Aragaki, S. & Mantovani, W. 1997. Variações fenológicas das espécies do cerrado em Emas (Pirassununga, SP). Acta Botanica Brasilica, 11: 61-78.

Baum, K.A. & Wallen, K.E. 2011. Potential bias in pan trapping as a function of floral abundance. Journal of the Kansas Entomological Society, 84(2): 155-159. http://doi.org/10.2317/JKES100629.1

Bawa, K.S. 1990. Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology, Evolution, and Systematics, 21: 399-422. http://doi.org/10.1146/annurev.es.21.110190.002151

Boiteau, G. 1983. The arthropod community of potato fields in New Brunswick, 1979-1981. The Canadian Entomologist, 115(7): 847-853. http://doi.org/10.4039/Ent115847-7

Buri, P.; Humbert, J.Y. & Arlettaz, R. 2014. Promoting pollinating insects in intensive agricultural matrices: Field-scale experimental manipulation of hay-meadow mowing regimes and its effects on bees. PLoS ONE, 9(1): 1-8, e85635. http://doi.org/10.1371/journal.pone.0085635

Button, L. & Elle, E. 2014. Wild bumble bees reduce pollination deficits in a crop mostly visited by managed honey bees. Agriculture, Ecosystems & Environment, 197: 255-263. http://doi.org/10.1016/j.agee.2014.08.004

Campbell, J.W. & Hanula, J.L. 2007. Efficiency of Malaise traps and colored pan traps for collecting flower visiting insects from three forested ecosystems. Journal of Insect Conservation, 11: 399-408. http://doi.org/10.1007/s10841-006-9055-4

Cane, J.H.; Minckley, R.L. & Kervin, L.J. 2000. Sampling Bees (Hymenoptera: Apiformes) for Pollinator Community Studies: Pitfalls of Pan-Trapping. Journal of the Kansas Entomological Society, 73: 225-231. Available at: http://www.jstor.org/stable/25085973.

Chao, A.; Colwell, R.K.; Lin, C.W. & Gotelli, N.J. 2009. Sufficient sampling for asymptotic minimum species richness estimators. Ecology, 90(4): 1125-1133. http://doi.org/10.1890/07-2147.1

Colwell, R.K. 2013. EstimateS, Version 9.1: Statistical Estimation of Species Richness and Shared Species from Samples (Software and User’s Guide). Available at: http://viceroy.eeb.uconn.edu/estimates.

Coops, N.C. & Catling, P.C. 1997. Predicting the complexity of habitat in forests from airborne videography for wildlife management. International Journal of Remote Sensing, 18(12): 2677-2682. http://doi.org/10.1080/014311697217530

Cordeiro, M.; Garraffoni, A.R.S. & Lourenço, A.P. 2019. Rapid assessment of the orchid bee fauna (Hymenoptera: Apidae: Euglossini) in the vicinity of an urban Atlantic Forest remnant in São Paulo, Brazil, Brazilian Journal of Biology, 79: 149-151. http://doi.org/10.1590/1519-6984.171286

Dafni, A.; Kevan, P.G. & Husband, B.C. 2005. Practical pollination biology. Canada, Enviroquest Ltda. 590p.

Devigne, C. & De Biseau, J.C. 2014. Urban ecology: comparison of the effectiveness of five traps commonly used to study the biodiversity of flying insects. Biodiversity, 5: 165-174.

Dirrigl, F.J. 2012. Effectiveness of Pan Trapping as a Rapid Bioinventory Method of Freshwater Shoreline Insects of Subtropical Texas. Southwestern Entomologist, 37: 133-139. http://doi.org/10.3958/059.037.0205

Droege, S.; Tepedino, V.J.; LeBuhn, G.; Link, W.; Minckley, R.L.; Chen, Q. & Conrad, C. 2010. Spatial patterns of bee captures in North American bowl trapping surveys. Insect Conservation and Diversity, 3(1): 15-23. http://doi.org/10.1111/j.1752-4598.2009.00074.x

Eiten, G. 1972. The cerrado vegetation of Brazil. The Botanical Review, 38: 201-341. http://doi.org/10.1007/BF02859158

Evans, D.A. & Medler, J.T. 1967. Flight activity of the corn leaf aphid in Wisconsin as determined by yellow pan trap collections. Journal of Economic Entomology, 60(4): 1088-1091. http://doi.org/10.1093/jee/60.4.1088

Fortel, L.; Henry, M.; Guilbaud, L.; Guirao, A.L.; Kuhlmann, M.; Mouret, H.; Rollin, O. & Vaissière, B.E. 2014. Decreasing abundance, increasing diversity and changing structure of the wild bee community (Hymenoptera: Anthophila) along an urbanization gradient. PLoS ONE, 9(8): e104679. http://doi.org/10.1371/journal.pone.0104679

Geroff, R.K.; Gibbs, J. & McCravy, K.W. 2014. Assessing bee (Hymenoptera: Apoidea) diversity of an Illinois restored tallgrass prairie: methodology and conservation considerations. Journal of Insect Conservation, 18(5): 951-964. http://doi.org/10.1007/s10841-014-9703-z

Gollan, J.R.; Ashcroft, M.B. & Batley, M. 2011. Comparison of yellow and white pan traps in surveys of bee fauna in New South Wales, Australia (Hymenoptera: Apoidea: Anthophila). Austral Entomology, 50: 174-178. http://doi.org/10.1111/j.1440-6055.2010.00797.x

Gonçalves, R.B. & Oliveira, P.S. 2013. Preliminary results of bowl trapping bees (Hymenoptera, Apoidea) in a southern Brazil forest fragment. Journal of Insect Biodiversity, 1(2): 1-9. http://doi.org/10.12976/jib/2013.1.2

Gonçalves, R.B.; Melo, G.A. & Aguiar, A.J. 2009. A assembléia de abelhas (Hymenoptera, Apidae) de uma área restrita de campos naturais do Parque Estadual de Vila Velha, Paraná e comparações com áreas de campos e cerrado. Papéis Avulsos de Zoologia, São Paulo, 49(14): 163-181. http://doi.org/10.1590/S0031-10492009001400001

Hall, M. 2018. Blue and yellow vane traps differ in their sampling effectiveness for wild bees in both open and wooded habitats. Agricultural and Forest Entomology, 1: 1-9. http://doi.org/10.1111/afe.12281

Hammer, Ø.; Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4: 1-9.

Heneberg, P. & Bogusch, P. 2014. To enrich or not to enrich? Are there any benefits of using multiple colors of pan traps when sampling aculeate Hymenoptera? Journal of Insect Conservation, 18(6): 1123-1136. http://doi.org/10.1007/s10841-014-9723-8

Imperatriz-Fonseca, V.; Saraiva, A.M. & Gonçalves, L.A. 2007. Iniciativa brasileira de polinizadores e os avanços para a compreensão do papel dos polinizadores como produtores de serviços ambientais. Bioscience Journal, 23: 100-106.

Instituto Estadual de Florestas (IEF). 2004. Plano de Manejo do Parque Estadual do Rio Preto. Belo Horizonte, IEF. 24p.

Joshi, N.K.; Leslie, T.; Rajotte, E.G.; Kammerer, M.A.; Otieno, M. & Biddinger, D.J. 2015. Comparative trapping efficiency to characterize bee abundance, diversity, and community composition in apple orchards. Annals of the Entomological Society of America, 108(5): 785-799. http://doi.org/10.1093/aesa/sav057

Klink, C.A. & Machado, R.B. 2005. A conservação do Cerrado brasileiro. Megadiversidade, 1: 147-155.

Kremen, C.; Colwell, R.K.; Erwin, T.L.; Murphy, D.D.; Noss, R.A. & Sanjayan, M.A. 1993. Terrestrial arthropod assemblages: their use in conservation planning. Conservation Biology, 7(4): 796-808. http://www.jstor.org/stable/2386811

Krug, C. & Alves-dos-Santos, I. 2008. O uso de diferentes métodos para amostragem da fauna de abelhas (Hymenoptera: Apoidea), um estudo em floresta ombrófila mista em Santa Catarina. Neotropical Entomology, 37(3): 265-278. http://doi.org/10.1590/S1519-566X2008000300005

Landaverde‐González, P.; Quezada‐Euán, J.J.G.; Theodorou, P.; Murray, T.E.; Husemann, M.; Ayala, R.; Moo-Valle, H.; Vandame, R. & Paxton, R.J. 2017. Sweat bees on hot chillies: provision of pollination services by native bees in traditional slash‐and‐burn agriculture in the Yucatán Peninsula of tropical Mexico. Journal of Applied Ecology, 54(6): 1814-1824. https://besjournals.onlinelibrary.wiley.com/doi/pdfdirect/10.1111/1365-2664.12860

Larsen, N.J.; Minor, M.A.; Cruickshank, R.H. & Robertson, A.W. 2014. Optimising methods for collecting Hymenoptera, including parasitoids and Halictidae bees, in New Zealand apple orchards. Journal of Asia-Pacific Entomology, 17(3): 375-381. http://doi.org/10.1016/j.aspen.2014.03.004

Lassau, S.A. & Hochuli, D.F. 2004. Effects of habitat complexity on ant assemblages. Ecography, 27(2): 157-164. http://doi.org/10.1111/j.0906-7590.2004.03675.x

Lassau, S.A. & Hochuli, D.F. 2005. Wasp community responses to habitat complexity in Sydney sandstone forests. Austral Ecology, 30: 179-187. http://doi.org/10.1111/j.1442-9993.2005.01435.x

Lassau, S.A. & Hochuli, D.F. 2007. Associations between wasp communities and forest structure: do strong local patterns hold across landscapes? Austral Ecology, 32(6): 656-662. http://doi.org/10.1111/j.1442-9993.2007.01751.x

Lassau, S.A.; Hochuli, D.F.; Cassis, G. & Reid, C.A.M. 2005. Effects of habitat complexity on forest beetle diversity: do functional groups respond consistently? Diversity and Distributions, 11: 73-82. http://doi.org/10.1111/j.1366-9516.2005.00124.x

Leong, J. & Thorp, R.W. 1999. Colour‐coded sampling: the pan trap colour preferences of oligolectic and nonoligolectic bees associated with a vernal pool plant. Ecological Entomology, 24(3): 329-335. http://doi.org/10.1046/j.1365-2311.1999.00196.x

Lourenço, A.P.; Santos, A.P.M.; Checon, H.H.; Costa, M.R.; & Assis Júnior, S.L. 2020. Cavity-nesting bee communities in areas with different levels of vegetation disturbance. Studies on Neotropical Fauna and Environment, 1-13. http://doi.org/10.1080/01650521.2019.1710334

Mayer, C. 2005. Does grazing influence bee diversity: molecules, organisms, ecosystems. In: International Symposium on Tropical Biology, 5º. Proceedings. Boston, MA, Springer. p. 173-179. http://doi.org/10.1007/0-387-24320-8_14

McCravy, K.W. & Ruholl, J.D. 2017. Bee (Hymenoptera: Apoidea) diversity and sampling methodology in a Midwestern USA Deciduous Forest. Insects, 8(3): 81. http://doi.org/10.3390/insects8030081

McCravy, K.W.; Geroff, R.K. & Gibbs, J. 2016. Tallgrass Prairie Malaise trap sampling efficiency for bees (Hymenoptera: Apoidea) in a restored tallgrass prairie, Florida Entomologist, 99: 321-323. http://doi.org/10.1653/024.099.0230

Milet-Pinheiro, P.; de Andrade Penante, D.C. & Schlindwein, C. 2013. Low legitimate pollen flow in distylic Turnera hermannioides (Passifloraceae) and its consequences on fruit and seed set. Flora-Morphology, Distribution, Functional Ecology of Plants, 208(10-12): 570-578. http://doi.org/10.1016/j.flora.2013.09.005

Missa, O.; Basset, Y.; Alonso, A.; Miller, S.E.; Curletti, G.; De Meyer, M.; Eardley, N.; Mansell, M.W. & Wagner, T. 2009. Monitoring arthropods in a tropical landscape: relative effects of sampling methods and habitat types on trap catches. Journal of Insect Conservation, 13(1): 103-118. http://doi.org/10.1016/j.flora.2013.09.005

Morandin, L.A. & Kremen, C. 2013. Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecological Applications, 23(4): 829-839. http://doi.org/10.1890/12-1051

Moreira, E.F.; Santos, R.L.S.; Penna, U.L.; Angel-Coca, C.; de Oliveira, F.F. & Viana, B.F. 2016. Are pan traps colors complementary to sample community of potential pollinator insects? Journal of Insect Conservation, 20: 583-596. http://doi.org/10.1007/s10841-016-9890-x

Moure, J.S.; Urban, D. & Melo, G.A.R. 2012. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region – online version. Available at: http://www.moure.cria.org.br/catalogue. Access in: 31/07/2017.

Myers, N.; Mittermeier, R.A. & Mittermeier, C.G. 2000. Biodiversity hotspots for conservation priorities. Nature, 403: 853-858. http://doi.org/10.1038/35002501

Neves, S.C.N.; Abreu, P.A.A. & Fraga, L.M.S. 2005. Fisiografia. In: Silva, A.C.; Pedreira, L.C.V.S.F. & Abreu, P.A.A. (Eds.). Serra do Espinhaço Meridional: Paisagens e ambientes. Belo Horizonte, O Lutador. p. 47-58.

Nicolson, S.W. 2009. Water homeostasis in bees, with the emphasis on sociality. Journal of Experimental Biology, 212(3): 429-434. http://doi.org/10.1242/jeb.022343

Popic, T.J.; Davila, Y.C. & Wardle, G.M. 2013. Evaluation of common methods for sampling invertebrate pollinator assemblages: net sampling out-perform pan traps. PLoS ONE, 8(6): e66665. http://doi.org/10.1371/journal.pone.0066665

Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O. & Kunin, W.E. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25: 345-353. http://doi.org/10.1016/j.tree.2010.01.007

Prado, S.G.; Ngo, H.T.; Florez, J.A. & Colazzo, J.A. 2017. Sampling bees in tropical forests and agroecosystems: a review. Journal of Insect Conservation, 21: 753. http://doi.org/10.1007/s10841-017-0018-8

Roulston, T.A.H.; Smith, S.A. & Brewster, A.L. 2007. A comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. Journal of the Kansas Entomological Society, 80: 179-181. http://doi.org/10.2317/0022-8567(2007)80[179:ACOPTA]2.0.CO;2

Rubene, D.; Schroeder, M. & Ranius, T. 2015. Diversity patterns of wild bees and wasps in managed boreal forests: effects of spatial structure, local habitat and surrounding landscape. Biological Conservation, 184: 201-208. http://doi.org/10.1016/j.biocon.2015.01.029

Saunders, M.E. & Luck, G.W. 2013. Pan trap catches of pollinator insects vary with habitat. Australian Journal of Entomology, 52(2): 106-113. http://doi.org/10.1111/aen.12008

Shapiro, L.H.; Tepedino, V.J. & Minckley, R.L. 2014. Bowling for bees: optimal sample number for “bee bowl” sampling transects. Journal of insect conservation, 18(6): 1105-1113. http://doi.org/10.1007/s10841-014-9720-y

Silveira, F.A.; Melo, G.A.R. & Almeida, E.A.B. 2002. Abelhas brasileiras: sistemática e identificação. Belo Horizonte: F.A. Almeida. 253p.

Stephen, W.P. & Rao, S. 2005. Unscented Color Traps for Non-Apis Bees (Hymenoptera: Apiformes). Journal of the Kansas Entomological Society, 78: 373-380. http://doi.org/10.2317/0410.03.1

Torné-Noguera, A.; Rodrigo, A.; Arnan, X.; Osorio, S.; Barril-Graells, H.; da Rocha-Filho, L.C. & Bosch, J. 2014. Determinants of spatial distribution in a bee community: nesting resources, flower resources, and body size. PLoS ONE, 9: e97255. http://doi.org/10.1371/journal.pone.0097255

Tuell, J.K. & Isaacs, R. 2009. Elevated pan traps to monitor bees in flowering crop canopies. Entomologia Experimentalis et Applicata, 131(1): 93-98. http://doi.org/10.1111/j.1570-7458.2009.00826.x

Viotti, M.A.; Moura, F.R. & Lourenço, A.P. 2013. Species Diversity and Temporal Variation of the Orchid-Bee Fauna (Hymenoptera, Apidae) in a Conservation Gradient of a Rocky Field Area in the Espinhaço Range, State of Minas Gerais, Southeastern Brazil. Neotropical Entomology, 42: 565-575. http://doi.org/10.1007/s13744-013-0164-y

Vrdoljak, S.M. & Samways, M.J. 2012. Optimising coloured pan traps to survey flower visiting insects. Journal of Insect Conservation, 16(3): 345-354. http://doi.org/10.1007/s10841-011-9420-9

Westphal, C.; Bommarco, R.; Carré, G.; Lamborn, E.; Morison, N.; Petanidou, T.; Potts, S.G.; Roberts, S.P.M.; Szentgyorgyi, H.; Tscheulin, T.; Vaissière, B.E.; Woyciechowski, M.; Biesmeijer, J.C.; Kenin, W.E.; Sttele, J. & Steffan-Dewenter, I. 2008. Measuring bee diversity in different European habitats and biogeographical regions. Ecological Monographs, 78(4): 653-671. http://doi.org/10.1890/07-1292.1

Wilson, J.S.; Griswold, T. & Messinger, O.J. 2008. Sampling bee communities (Hymenoptera: Apiformes) in a desert landscape: are pan traps sufficient? Journal of the Kansas Entomological Society, 81: 288-300. http://doi.org/10.2317/JKES-802.06.1

Wittmann, D.; Radtke, R.; Cure, J.R. & Schifino‐Wittmann, M.T. 1990. Coevolved reproductive strategies in the oligolectic bee Callonychium petuniae (Apoidea, Andrenidae) and three purple flowered Petunia species (Solanaceae) in southern Brazil. Journal of Zoological Systematics and Evolutionary Research, 28(3): 157-165. http://doi.org/10.1111/j.1439-0469.1990.tb00373.x

Downloads

Published

2020-07-16

Issue

Section

Original Article

How to Cite

Viana, T. A., & Lourenço, A. P. (2020). Surveys of the bee (Hymenoptera: Apiformes) community in a Neotropical savanna using pan traps. Papéis Avulsos De Zoologia, 60, e20206031. https://doi.org/10.11606/1807-0205/2020.60.31

Funding data