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Crop pollinators in Brazil: a review of reported interactions

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Abstract

Pollinators are important to maintain ecosystem services, being part of the reproduction and seed formation process of plant species. In this study, we reviewed the literature and developed a database of interactions between pollinators and agricultural crops for Brazil. We classified the pollinators as effective, occasional, or potential, and also identified those species quoted simply as “visitors” (without reference to pollination). We found 250 crop pollinators pertaining to the three categories quoted, with 168 effective ones. Besides, we identified the effective pollinators of 75 agricultural crops. Bees pertaining to the family Apidae, mainly those from the genera Melipona, Xylocopa, Centris, and Bombus, were reportedly the most effective pollinators of agricultural crops. We also found that the exotic managed species Apis mellifera and the stingless bee Trigona spinipes are effective pollinators of some crops. In spite of some data having been originated from gray literature and the taxonomic impediment, this effort is a crucial step to clarify the gaps and bias on data. This study is the first to attempt to build, analyze, and make available a comprehensive data set about pollinators of agricultural crops in a country level, aiming to contribute to protective measures and to enhance the sustainable use of native pollinators in agriculture.

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References

  • Adams, D.C., Rohlf, F.J., Slice, D.E. (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Ital. J. Zool. 71, 5–16

    Article  Google Scholar 

  • Aebi, A., Vaissiere, B.E., vanEngelsdorp, D., Delaplane, K.S., Roubik, D.W., Neumann, P. (2012) Back to the future: Apis versus non-Apis pollination. TREE 27, 142–143

    Google Scholar 

  • Agnarsson, I., Kuntner, M. (2007) Taxonomy in a changing world: seeking solutions for a science in crisis. Syst. Biol. 56, 531–539

    Article  PubMed  Google Scholar 

  • Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M. (2009) How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 103, 1579–1588

    Article  PubMed Central  PubMed  Google Scholar 

  • Aldana, J., Cure, J.R., Almanza, M.T., Vecil, D., Rodríguez, D. (2007) Efecto de Bombus atratus (Hymenoptera: Apidae) sobre la productividad de tomate (Lycopersicon esculentum Mill.) bajo invernadero en la Sabana de Bogotá, Colombia. Agron. Colomb. 25, 62–72

    Google Scholar 

  • Alonso, J.D.S., Silva, J.F., Garófalo, C.A. (2012) The effects of cavity length on nest size, sex ratio and mortality of Centris (Heterocentris) analis (Hymenoptera, Apidae, Centridini). Apidologie 43, 436–448

    Article  Google Scholar 

  • Becher, M.A., Osborne, J.L., Thorbek, P., Kennedy, P.J., Grimm, V. (2013) Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models. J. Appl. Ecol. 50, 868–880

    Article  PubMed Central  PubMed  Google Scholar 

  • Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354

    Article  CAS  PubMed  Google Scholar 

  • Boiça Jr., A.I., Santos, T.M., Passilongo, J. (2004) Trigona spinipes (Fabr.) (Hymenoptera: Apidae) em espécies de maracujazeiro: flutuação populacional, horário de visitação e danos às flores. Neotrop. Entomol. 33, 135–139

    Article  Google Scholar 

  • Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordesa, N., Solter, L.F., Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. PNAS 108, 662–666

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cartolano Jr., E. A., Saraiva, A. M., Correa, P. L. P., Giannini, T. C., Giovanni, R. (2007) Uma proposta de esquema de dados de relacionamento entre espécimes. In: Proceedings of XXXIII Conferencia Latinoamericana de Informática, San Jose

  • Cortopassi-Laurino, M., Ramalho, M. (1988) Pollen harvest by africanized Apis mellifera and Trigona spinipes in São Paulo: botanical and ecological views. Apidologie 19, 1–24

    Article  Google Scholar 

  • Dafni, A., Kevan, P.G., Husband, B.C. (2005) Practical pollination biology. Enviroquest, Ontario

    Google Scholar 

  • Delaplane, K.S., Dag, A., Danka, R.G., Freitas, B.F., Garibaldi, L.A., Goodwin, R.M., Hormaza, J.I. (2013) Standard methods for pollination research with Apis mellifera. J. Apic. Res. 52, 1–28

    Article  Google Scholar 

  • Dupont, Y.L., Damgaard, C., Simonsen, V. (2011) Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields. PLoS One 6, e25172

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dupont, Y.L., Hansen, D.M., Valido, A., Olesen, J.M. (2004) Impact of introduced honey bees on native pollination interactions of the endemic Echium wildpretii (Boraginaceae) on Tenerife, Canary Islands. Biol. Cons. 118, 301–311

    Article  Google Scholar 

  • Francisco, F.O., Nunes-Silva, P., Francoy, T.M., Wittmann, D., Imperatriz-Fonseca, V.L., Arias, M.C., Morgan, E.D. (2008) Morphometrical, biochemical and molecular tools for assessing biodiversity. An example in Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Insect. Soc. 55, 231–237

    Article  Google Scholar 

  • Francoy, T.M., Grassi, M.L., Imperatriz-Fonseca, V.L., May-Itzá, W.J., Quezada-Euán, J.J.G. (2011) Geometric morphometrics of the wing as a tool for assigning genetic lineages and geographic origin to Melipona beecheii (Hymenoptera: Meliponini). Apidologie 42, 499–507

    Article  Google Scholar 

  • Francoy, T.M., Silva, R.A.O., Nunes-Silva, P., Menezes, C., Imperatriz-Fonseca, V.L. (2009) Gender identification of five genera of stingless bees (Apidae, Meliponini) based on wing morphology. Genet. Mol. Res. 8, 207–214

  • Free, J.B. (1993) Insect pollination of crops. Academic, London, UK

    Google Scholar 

  • Freitas, B.M., Oliveira Filho, J.H. (2001) Criação racional de mamangavas para polinização em áreas agrícolas. Banco do Nordeste, Fortaleza

    Google Scholar 

  • Freitas, B.M., Oliveira Filho, J.H. (2003) Ninhos racionais para mamangava (Xylocopa frontalis) na polinização do maracujá-amarelo (Passiflora edulis). Ciênc. Rural 33, 1135–1139

    Article  Google Scholar 

  • Gallai, N., Salles, J.M., Settele, J., Vaissière, B.E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821

    Article  Google Scholar 

  • Garibaldi, L.A., Aizen, M.A., Klein, A.M., Cunningham, S.A., Harder, L.D. (2011) Global growth and stability of agricultural yield decrease with pollinator dependence. PNAS 108, 5909–5914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A., Kremen, C., Carvalheiro, L.G., Harder, L.D., Afik, O., et al. (2013) Wild pollinators enhance fruit set of crops regardless of honey-bee abundance. Science 339, 1608–1611

    Article  CAS  PubMed  Google Scholar 

  • Giannini, T.C., Acosta, A.L., Garófalo, C.A., Saraiva, A.M., Alves dos Santos, I., Imperatriz-Fonseca, V.L. (2012) Pollination services at risk: bee habitats will decrease owing to climate change in Brazil. Ecol. Model. 244, 127–131

    Article  Google Scholar 

  • Giannini, T.C., Acosta, A.L., Silva, C.I., Oliveira, P.E.A.M., Imperatriz-Fonseca, V.L., Saraiva, A.M. (2013a) Identifying the areas to preserve passion fruit pollination service in Brazilian Tropical Savannas under climate change. Agric. Ecosyst. Environ. 171, 39–46

    Article  Google Scholar 

  • Giannini, T.C., Pinto, C.E., Acosta, A.L., Taniguchi, M., Saraiva, A.M., Alves-dos-Santos, I. (2013b) Interactions at large spatial scale: the case of Centris bees and floral oil producing plants in South America. Ecol. Model. 258, 74–81

    Article  Google Scholar 

  • Girão, L.C., Lopes, A.V., Tabarelli, M., Bruna, E.M. (2007) Changes in tree reproductive traits reduce functional diversity in a fragmented Atlantic Forest landscape. PLoS One 2, e908

    Article  PubMed Central  PubMed  Google Scholar 

  • Gotelli, N.J. (2004) A taxonomic wish-list for community ecology. Phil. Trans. R. Soc. B 359, 585–597

    Article  PubMed Central  PubMed  Google Scholar 

  • Heard, T.A. (1999) The role of stingless bees in crop pollination. Annu. Rev. Entomol. 44, 183–206

    Article  CAS  PubMed  Google Scholar 

  • Imperatriz-Fonseca, V.L., Saraiva, A.M., Jong, D. (2006) Bees as pollinators in Brazil: assessing the status and suggesting best practices. Holos, Brasília

    Google Scholar 

  • Kim, K.C., Byrne, L.B. (2006) Biodiversity loss and the taxonomic bottleneck: emerging biodiversity science. Ecol. Res. 21, 794–810

    Article  Google Scholar 

  • Kennedy, C.M., Lonsdorf, E., Neel, M.C., Williams, N.M., Ricketts, T.H., Winfree, R., Bommarco, R., Brittain, C., Burley, A.L., Cariveau, D., et al. (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599

    Article  PubMed  Google Scholar 

  • Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313

    Article  PubMed Central  PubMed  Google Scholar 

  • Kleinert, A. M. P., Giannini, T. C. (2012) Generalist bee species on Brazilian bee-plant interaction networks. Psyche, 291519, 7 pages

  • Lautenbach, S., Seppelt, R., Liebscher, J., Dormann, C.F. (2012) Spatial and temporal trends of global pollination benefit. PLoS One 7, e35954

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • LeBuhn, G., Droege, S., Connor, E.F., Gemmill-Herren, B., Potts, S.G., Minckley, R.L., Griswold, T., Jean, R., Kula, E., Roubik, D.W., et al. (2013) Detecting insect pollinator declines on regional and global scales. Cons. Biol. 27, 113–120

    Article  Google Scholar 

  • Lennartsson, L. (2002) Extinction thresholds and disrupted plant–pollinator interactions in fragmented plant populations. Ecology 83, 3060–3072

    Google Scholar 

  • Magnacca, K.N., Brown, M.J.F. (2012) DNA barcoding a regional fauna: Irish solitary bees. Mol. Ecol. Resour. 12, 990–998

    Article  CAS  PubMed  Google Scholar 

  • Magalhães, C.B., Freitas, B.M. (2013) Introducing nests of the oil-collecting bee Centris analis (Hymenoptera: Apidae: Centridini) for pollination of acerola (Malpighia emarginata) increases yield. Apidologie 44, 234–239

    Article  Google Scholar 

  • Malagodi-Braga, K.S., Kleinert, A.M.P. (2004) Could Tetragonisca angustula Latreille (Apinae, Meliponini) be used as strawberry pollinator in greenhouses? Australian J. Agric. Res. 55, 771–773

    Article  Google Scholar 

  • Michener, C.D. (2007) The Bees of the World. Johns Hopkins, Baltimore

    Google Scholar 

  • Morandin, L.A., Winston, M.L. (2005) Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol. Appl. 15, 871–881

    Article  Google Scholar 

  • Nunes-Silva, P., Hrncir, M., Silva, C.I., Roldao, Y., Imperatriz-Fonseca, V.L. (2013) Stingless bees, Melipona fasciculata, as efficient pollinators of eggplant (Solanum melongena) in greenhouses. Apidologie 44, 537–546

    Article  Google Scholar 

  • Oliveira, R., Schlindwein, C. (2009) Searching for a manageable pollinator for acerola orchards: the solitary oil-collecting bee Centris analis (Hymenoptera: Apidae: Centridini). J. Econ. Entomol. 102, 265–273

    Article  PubMed  Google Scholar 

  • Ollerton, J., Price, V., Armbruster, W.S., Memmott, J., Watt, S., Waser, N.M., Totland, O., Goulson, D., Alarcón, R., Stout, J.C., Tarrant, S. (2012) Overplaying the role of honey bees as pollinators: a comment on Aebi and Neumann (2011). TREE 27, 141–142

    PubMed  Google Scholar 

  • Ollerton, J., Winfree, R., Tarrant, S. (2011) How many flowering plants are pollinated by animals? Oikos 120, 321–326

    Article  Google Scholar 

  • Pereira, M., Garófalo, C.A. (2010) Biologia da nidificação de Xylocopa frontalis e Xylocopa grisescens (Hymenoptera, Apidae, Xylocopini) em ninhos-armadilha. Oecologia Aust. 14, 193–209

    Article  Google Scholar 

  • Polce, C., Termansen, M., Aguirre-Gutierrez, J., Boatman, N.D., Budge, G.E., Andrew, C., Garratt, M.P., Pietravalle, S., Potts, S.G., Ramirez, J.A., Somerwill, K.E., Biesmeijer, J.C. (2013) Species distribution models for crop pollination: a modelling framework applied to Great Britain. PLoS One 8, e76308

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. TREE 25, 345–353

    PubMed  Google Scholar 

  • Rohlf, J.F., Marcus, L.F. (1993) A revolution in morphometrics. TREE 8, 129–132

    Google Scholar 

  • Roubik, D.W. (1980) Foraging behavior of competing Africanized honey bees and stingless bees. Ecology 61, 836–845

    Article  Google Scholar 

  • Roubik, D.W., Villanueva-Gutierrez, R. (2009) Invasive Africanized honey bee impact on native solitary bees: a pollen resource and trap nest analysis. Biol. J. Linn. Soc. 98, 152–160

    Article  Google Scholar 

  • Saraiva, A. M., Veiga, A. K., Cartolano Junior, E. A. (2011) Biodiversity Data Digitizer – A tool for a richer biodiversity data content digitization. Proceedings of TDWG, New Orleans

  • Sazima, I., Sazima, M. (1989) Mamangavas e irapuás (Hymenoptera, Apoidea): visitas, interações e conseqüências para polinização do maracujá (Passifloraceae). Rev. Bras. Entomol. 33, 109–118

    Google Scholar 

  • Schneider, S.S., DeGrandi-Hoffman, G., Smith, D.R. (2004) The African Honey Bee: factors contributing to a successful biological invasion. Annu. Rev. Entomol. 49, 351–376

    Article  CAS  Google Scholar 

  • Silveira, F.A., Pinheiro-Machado, C., Alves dos Santos, I., Kleinert, A.M.P., Imperatriz-Fonseca, V.L. (2002) Taxonomic constraints for the conservation and sustainable use of wild pollinators—the Brazilian wild bees. In: Kevan, P., Imperatriz Fonseca, V.L. (eds.) Pollinating Bees, pp. 41–50. Ministry of Environment, Brasília

    Google Scholar 

  • Slaa, E.J., Chaves, L.A.S., Malagodi-Braga, K.S., Hofstede, F.E. (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37, 293–315

    Article  Google Scholar 

  • Thomson, D. (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85, 458–470

    Article  Google Scholar 

  • Valentini, A., Pompanon, F., Taberlet, P. (2009) DNA barcoding for ecologists. TREE 24, 110–117

    PubMed  Google Scholar 

  • Velthuis, H.H.W., Doorn, A. (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37, 421–451

    Article  Google Scholar 

  • Vogel, S. (1974) Ölblumen und ölsammelnde Bienen. Tropische und Subtropische flanzenwelt 7, 285–547

    Google Scholar 

  • Wieczorek, J., Bloom, D., Guralnick, R., Blum, S., Doring, M., Giovanni, R., Robertson, T., Vieglais, D. (2012) Darwin Core: an evolving community-developed biodiversity data standard. PLoS One 7, e29715

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to three anonymous referees, Carlos Alberto Garófalo, Márcia Ribeiro, and Luisa Gigante Carvalheiro for suggestions in the manuscript, and also to National Counsel of Technological and Scientific Development (CNPq) (472702/2013-0), São Paulo Research Foundation (FAPESP) (2011/06811-5), Coordination for the Improvement of Higher Education Personnel (CAPES), and Biodiversity and Computation (Biocomp, University of São Paulo).

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Authors and Affiliations

  1. Escola Politécnica, Universidade de São Paulo, Av. Prof. Luciano Gualberto, Trav. 3, n. 380, 05508-010, São Paulo, São Paulo, Brazil

    T. C. Giannini, E. A. Cartolano Jr., A. K. Veiga & A. M. Saraiva

  2. Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Trav. 14, n. 321, 05508-900, São Paulo, São Paulo, Brazil

    T. C. Giannini & V. L. Imperatriz-Fonseca

  3. Universidade Santo Amaro, Rua Professor Enéas de Siqueira Neto, n. 340, 4829-300, São Paulo, São Paulo, Brazil

    T. C. Giannini

  4. Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo, Av. Bandeirantes, n. 3900, 14040-901, Ribeirão Preto, São Paulo, Brazil

    S. Boff & G. D. Cordeiro

  5. Research Center on Biodiversity and Computing, BioComp, Av. Prof. Luciano Gualberto, Trav. 3, n. 380, 05508-010, São Paulo, São Paulo, Brazil

    T. C. Giannini, S. Boff, G. D. Cordeiro, E. A. Cartolano Jr., A. K. Veiga, V. L. Imperatriz-Fonseca & A. M. Saraiva

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  1. T. C. Giannini
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  2. S. Boff
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Correspondence to T. C. Giannini.

Additional information

Manuscript editor: David Tarpy

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Giannini, T.C., Boff, S., Cordeiro, G.D. et al. Crop pollinators in Brazil: a review of reported interactions. Apidologie 46, 209–223 (2015). https://doi.org/10.1007/s13592-014-0316-z

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