Effect of Agricultural Matrices on the Biodiversity Metrics of Bees (Hymenoptera: Anthophila): A Review

José Victor Alves Ferreira; Juliana Monteiro Almeida-Rocha; José Carlos Morante-Filho; Danielle Storck-Tonon; Maíra Benchimol

doi:10.13102/sociobiology.v72i3.11410

Authors

José Victor Alves Ferreira Applied Ecology and Conservation Lab, Universidade Estadual de Santa Cruz, Ilhéus-BA, Brazil https://orcid.org/0000-0002-3671-3876
Juliana Monteiro Almeida-Rocha The Nature Conservancy, São Paulo-SP, Brazil https://orcid.org/0000-0002-2968-5504
José Carlos Morante-Filho Applied Ecology and Conservation Lab, Universidade Estadual de Santa Cruz, Ilhéus, BA, Brazil https://orcid.org/0000-0002-1625-9872
Danielle Storck-Tonon Programa de Pós-Graduação em Ambiente e Sistemas de Produção Agrícola, Universidade do Estado de Mato Grosso, Tangará da Serra, MT, Brazil https://orcid.org/0000-0002-4402-0607
Maíra Benchimol Applied Ecology and Conservation Lab, Universidade Estadual de Santa Cruz, Ilhéus, BA, Brazil https://orcid.org/0000-0002-1238-1619

DOI:

https://doi.org/10.13102/sociobiology.v72i3.11410

Keywords:

biodiversity conservation, biodiversity-friendly matrices, cropland, pollinators, species loss

Abstract

Agriculture has been globally responsible for biodiversity decay. Since bees are key pollinators, their diversity reduction can affect biodiversity conservation and agricultural production. Although agricultural matrices have been reported as pervasive to bees, these effects are not always consistent and may vary according to evaluated parameters. To fill this gap, we conducted a global review of studies that compared bee abundance and/or species richness between agricultural and native habitats. In addition to describing the overall pattern observed in the studies (n = 32), we also conducted a meta-analysis with a subset of data (14 studies and 38 comparisons). We calculated the effect size from the standardized mean difference among agriculture-native habitats in the meta-analysis. We considered moderators that may influence this effect, including response type, flowering type, crop life cycle, and region. Based on the review, which mainly included studies conducted in the neotropical region, we identified that half of the studies (50%) concluded that agricultural matrices negatively affect biodiversity metrics of bees. In comparison, only five (15.6%) and eight studies (25%) observed a positive and neutral effect, respectively. Three studies (9.4%) observed a varied effect (positive or negative), depending on the type of response assessed (richness or abundance) or the management intensity (as such, cocoa agroforests with low or high diversity of native shade trees). Additionally, meta-analysis supports this finding by revealing an overall negative effect, especially for abundance. Negative effects were consistent for non-mass-flowering crops, perennial crops, and temperate regions. We thus recommend that agricultural landscapes across the globe should maintain native habitats to ensure high bee diversity and potentially contribute to the delivery of ecosystem services.

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References

Aguiar, W.M., Sofia, S.H., Melo, G.A.R. & Gaglianone, M.C. (2015). Changes in orchid bee communities across forest-agroecosystem boundaries in Brazilian Atlantic Forest landscapes. Environmental Entomology, 44: 1465-1471. DOI: https://doi.org/10.1093/ee/nvv130

Almeida-Rocha, J.M. d., Peres, C.A. & Oliveira, L.C. (2017). Primate responses to anthropogenic habitat disturbance: A pantropical meta-analysis. Biological Conservation, 215: 30-38. DOI: https://doi.org/10.1016/j.biocon.2017.08.018

Almeida, M.L.S., Carvalho, G.S., Novais, J.R., Storck Tonon, D., Oliveira, M.L., Mahlmann, T., Nogueira, D.S. & Pereira, M.J. (2020). Contribution of the Cerrado as habitat for sunflower pollinating bees. Sociobiology, 67: 281-291. DOI: https://doi.org/10.13102/sociobiology.v67i2.4865

Asbjornsen, H., Hernandez-Santana, V., Liebman, M., Bayala, J., Chen, J., Helmers, M., Ong, C.K. & Schulte, L.A. (2014). Targeting perennial vegetation in agricultural landscapes for enhancing ecosystem services. Renewable Agriculture and Food Systems, 29: 101-125. DOI: https://doi.org/10.1017/S1742170512000385

Bailey, S., Requier, F., Nusillard, B., Roberts, S.P.M., Potts, S.G. & Bouget, C. (2014). Distance from forest edge affects bee pollinators in oilseed rape fields. Ecology and Evolution, 4: 370-380. DOI: https://doi.org/10.1002/ece3.924

Belsky J. & Joshi N.K. (2020) Effects of fungicide and herbicide chemical exposure on Apis and non-Apis bees in agricultural landscape. Frontiers in Environmental Science, 8: 1-10. DOI: https://doi.org/10.3389/fenvs.2020.00081

Briggs, H.M., Perfecto, I. & Brosi, B.J. (2013). The role of the agricultural matrix: Coffee management and euglossine bee (Hymenoptera: Apidae: Euglossini) communities in Southern Mexico. Environmental Entomology, 42: 1210-1217. DOI: https://doi.org/10.1603/EN13087

Brittain, C.A., Vighi, M., Bommarco, R., Settele, J. & Potts, S.G. (2010). Impacts of a pesticide on pollinator species richness at different spatial scales. Basic and Applied Ecology, 11: 106-115. DOI: https://doi.org/10.1016/j.baae.2009.11.007

Campbell, B.M., Beare, D.J., Bennett, E.M., Hall-Spencer, J.M., Ingram, J.S.I., Jaramillo, F., Ortiz, R., Ramankutty, N., Sayer, J.A. & Shindell, D. (2017). Agriculture production as a major driver of the Earth system exceeding planetary boundaries. Ecology and Society, 22: 8. DOI: https://doi.org/10.5751/ES-09595-220408

Dainese, M., Martin, E.A., Aizen, M.A., Albrecht, M., Bartomeus, I. et al. (2019). A global synthesis reveals biodiversity-mediated benefits for crop production. Science Advances, 5: 1-14.

Diekötter, T., Peter, F., Jauker, B., Wolters, V. & Jauker, F. (2014). Mass-flowering crops increase richness of cavity-nesting bees and wasps in modern agro-ecosystems. Global Change Biology Bioenergy, 6: 219-226. DOI: https://doi.org/10.1111/gcbb.12080

Duval, S. & Tweedie, R. (2000). A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis. Journal of the American Statistical Association, 95: 89-98. DOI: https://doi.org/10.1080/01621459.2000.10473905

Ellis, E.C., Goldewijk, K.K., Siebert, S., Lightman, D. and Ramankutty, N. (2010). Anthropogenic transformation of the biomes, 1700 to 2000. Global Ecology and Biogeography, 19: 589-606. DOI: https://doi.org/10.1111/j.1466-8238.2010.00540.x

Fahrig, L. (2013). Rethinking patch size and isolation effects: The habitat amount hypothesis. Journal of Biogeography, 40: 1649-1663. DOI: https://doi.org/10.1111/jbi.12130

Ferreira, J.V.A., Arroyo-Rodríguez, V., Morante-Filho, J.C., Storck-Tonon, D., Somavilla, A., dos Santos-Silva, J.A., Mahlmann, T., Oliveira & M.L., Benchimol, M. (2024). Landscape forest cover and regional context shape the conservation value of shaded cocoa agroforests for bees and social wasps. Landscape Ecology, 39: 1-15. DOI: https://doi.org/10.1007/s10980-024-01994-x

Ferreira, J.V.A., Storck-Tonon, D., Ramos, A.W.P., Costa, H.C.M., Nogueira, D.S., Mahlmann, T., Oliveira, M.L., Pereira, M.J.B., da Silva, D.J. & Peres, C.A. (2022). Critical role of native forest and savannah habitats in retaining neotropical pollinator diversity in highly mechanized agricultural landscapes. Agriculture, Ecosystems and Environment, 338: 108084. DOI: https://doi.org/10.1016/j.agee.2022.108084

Ferreira, P.A., Boscolo, D., Carvalheiro, L.G., Biesmeijer, J.C., Rocha, P.L.B. & Viana, B.F. (2015). Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic Rainforest. Landscape Ecology, 30: 2067-2078. DOI: https://doi.org/10.1007/s10980-015-0231-3

Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R. et al. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339: 1608-1611. DOI: https://doi.org/10.1126/science.1230200

Giannini, T.C., Cordeiro, G.D., Freitas, B.M., Saraiva, A.M. & Imperatriz-Fonseca, V.L. (2015). The dependence of crops for pollinators and the economic value of pollination in Brazil. Journal of Economic Entomology, 108: 849-857. DOI: https://doi.org/10.1093/jee/tov093

Hansen, M. C., Potapov, P. V., Pickens, A. H., Tyukavina, A., Hernandez-Serna, A., Zalles, V., Turubanova, S., Kommareddy, I., Stehman, S. V., Song, X. P., & Kommareddy, A. (2022). Global land use extent and dispersion within natural land cover using Landsat data. Environmental Research Letters, 17: 034050. DOI: https://doi.org/10.1088/1748-9326/ac46ec

Hoehn, P., Steffan-Dewenter, I. & Tscharntke, T. (2010). Relative contribution of agroforestry, rainforest and openland to local and regional bee diversity. Biodiversity and Conservation, 19: 2189-2200. DOI: https://doi.org/10.1007/s10531-010-9831-z

Holzschuh, A., Steffan-Dewenter, I., Kleijn, D. & Tscharntke, T. (2007). Diversity of flower-visiting bees in cereal fields: Effects of farming system, landscape composition and regional context. Journal of Applied Ecology, 44: 41-49. DOI: https://doi.org/10.1111/j.1365-2664.2006.01259.x

IPBES (2016). The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. In: S.G. Potts, V. L. Imperatriz-Fonseca, & H. T. Ngo, (eds). Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn, Germany.

Kammerer, M., Goslee, S.C., Douglas, M.R., Tooker, J.F. & Grozinger, C.M. (2021). Wild bees as winners and losers: Relative impacts of landscape composition, quality, and climate. Global Change Biology, 27: 1250-1265. DOI: https://doi.org/10.1111/gcb.15485

Kendall, L.K., Mola, J.M., Portman, Z.M., Cariveau, D.P., Smith, H.G. & Bartomeus, I. (2022). The potential and realized foraging movements of bees are differentially determined by body size and sociality. Ecology, 103: 1-8. DOI: https://doi.org/10.1002/ecy.3809

Kleijn, D., Winfree, R., Bartomeus, I., Carvalheiro, L.G. & Henry, M. (2015). Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nature Communications, 6: 1-9.

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. Proceedings of the Royal Society B, 274: 303-313. DOI: https://doi.org/10.1098/rspb.2006.3721

van Klink, R., Bowler, D.E., Gongalsky, K.B., Swengel, A.B., Gentile, A. & Chase, J.M. (2020). Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science, 368: 417-420. DOI: https://doi.org/10.1126/science.aax9931

Laurance, W.F., Sayer, J. & Cassman, K.G. (2014). Agricultural expansion and its impacts on tropical nature. Trends in Ecology and Evolution, 29: 107-116. DOI: https://doi.org/10.1016/j.tree.2013.12.001

Lisón, F., Jiménez-Franco, M. V., Altamirano, A., Haz, Á., Calvo, J.F. & Jones, G. (2020). Bat ecology and conservation in semi-arid and arid landscapes: a global systematic review. Mammal Review, 50: 52-67. DOI: https://doi.org/10.1111/mam.12175

Losey, J.E. & Vaughan, M. (2006). The economic value of ecological services provided by insects. Bioscience, 56: 311-323. DOI: https://doi.org/10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2

Medeiros, H.R., Martello, F., Almeida, E.A.B., Mengual, X., Harper, K.A., Gradinete, Y.C., Metzger, J.P., Righi, C.A. & Ribeiro, M.C. (2019). Landscape structure shapes the diversity of beneficial insects in coffee producing landscapes. Biological Conservation, 238: 108193. DOI: https://doi.org/10.1016/j.biocon.2019.07.038

Michener, C.D. (2007). The Bees of the World. 2nd ed. Baltimore, The John Hopkins University Press. DOI: https://doi.org/10.56021/9780801885730

Millard, J., Outhwaite, C.L., Kinnersley, R., Freeman, R., Gregory, R.D. et al. (2021). Global effects of land-use intensity on local pollinator biodiversity. Nature Communications, 12: 1-11. DOI: https://doi.org/10.1038/s41467-021-23228-3

Montero-Castaño, A., Ortiz-Sánchez, F.J. & Vilà, M. (2016). Mass flowering crops in a patchy agricultural landscape can reduce bee abundance in adjacent shrublands. Agriculture, Ecosystems and Environment, 223: 22-30. DOI: https://doi.org/10.1016/j.agee.2016.02.019

Morandin, L.A. & Winston, M.L. (2005). Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecological Applications, 15: 871-881. DOI: https://doi.org/10.1890/03-5271

Newbold, T., Hudson, L.N., Hill, S.L.L., Contu, S., Lysenko, I. et al. (2015). Global effects of land use on local terrestrial biodiversity. Nature, 520: 45-50.

Newbold, T., Oppenheimer, P., Etard, A. & Williams, J.J. (2020). Tropical and Mediterranean biodiversity is disproportionately sensitive to land-use and climate change. Nature Ecology and Evolution, 4: 1630-1638. DOI: https://doi.org/10.1038/s41559-020-01303-0

Oakley, J.L. & Bicknell, J.E. (2022). The impacts of tropical agriculture on biodiversity: a meta-analysis. Journal of Applied Ecology, 59: 1-11. DOI: https://doi.org/10.1111/1365-2664.14303

Ockermüller, E., Kratschmer, S., Hainz-Renetzeder, C., Sauberer, N., Meimberg, H., Frank, T., Pascher, K. & Pachinger, B. (2023). Agricultural land-use and landscape composition: Response of wild bee species in relation to their characteristic traits. Agriculture, Ecosystems and Environment, 353: 108540. DOI: https://doi.org/10.1016/j.agee.2023.108540

Oliveira, N.S., Ferreira, J.V., da Silva, R.J., Somavilla, A., Volff, C.E., Pereira, M.J., da Silva, D.J., Butnariu, A.R. & Storck-Tonon, D. (2024). The importance of legal reserve for predator social wasp diversity in an agroecosystem in the Brazilian Cerrado. Studies on Neotropical Fauna and Environment, 59: 360-369. DOI: https://doi.org/10.1080/01650521.2022.2147045

Ollerton, J., Winfree, R. & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120: 321-326. DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x

Papanikolaou, A.D., Kühn, I., Frenzel, M. & Schweiger, O. (2017). Semi-natural habitats mitigate the effects of temperature rise on wild bees. Journal of Applied Ecology, 54: 527-536. DOI: https://doi.org/10.1111/1365-2664.12763

Paz, F.S., Pinto, C.E., de Brito, R.M., Imperatriz-Fonseca, V.L. & Giannini, T.C. (2021). Edible fruit plant species in the Amazon forest rely mostly on bees and beetles as pollinators. Journal of Economic Entomology, 114: 710-722. DOI: https://doi.org/10.1093/jee/toaa284

Porto, R.G., de Almeida, R.F., Cruz-Neto, O., Tabarelli, M. & Viana, B.F. (2020). Pollination ecosystem services: A comprehensive review of economic values, research funding and policy actions. Food Security, 12: 1425-1442. DOI: https://doi.org/10.1007/s12571-020-01043-w

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 and Evolution, 25: 345-353. DOI: https://doi.org/10.1016/j.tree.2010.01.007

Prado, S. G., Ngo, H. T., Florez, J. A. & Collazo, J. A. (2017). Sampling bees in tropical forests and agroecosystems: a review. Journal of Insect Conservation, 21: 753-770. DOI: https://doi.org/10.1007/s10841-017-0018-8

R Core Team (2022). A language and environment for statistical computing. Available at: <https://www.r-project.org/>.

Rahimi, E., Barghjelveh, S. & Dong, P. (2022). Amount, distance-dependent and structural effects of forest patches on bees in agricultural landscapes. Agriculture and Food Security, 11: 1-15. DOI: https://doi.org/10.1186/s40066-022-00360-x

Ramankutty, N., Evan, A.T., Monfreda, C. & Foley, J.A. (2008). Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Global Biogeochemical Cycles, 22: 1-19. DOI: https://doi.org/10.1029/2007GB002952

Raven, P.H. & Wagner, D.L. (2021). Agricultural intensification and climate change are rapidly decreasing insect biodiversity. Proceedings of the National Academy of Sciences USA, 118: 1-6. DOI: https://doi.org/10.1073/pnas.2002548117

Ricketts, T.H., Regetz, J., Steffan-Dewenter, I., Cunningham, S.A. & Kremen, C. (2008). Landscape effects on crop pollination services: Are there general patterns? Ecology Letters, 11: 499-515. DOI: https://doi.org/10.1111/j.1461-0248.2008.01157.x

Rogers, S.R., Tarpy, D.R. & Burrack, H.J. (2014). Bee species diversity enhances productivity and stability in a perennial crop. PLoS ONE, 9: 1-8. DOI: https://doi.org/10.1371/journal.pone.0097307

Roulston, T.H. & Goodell, K. (2011). The role of resources and risks in regulating wild bee populations. Annual Review of Entomology, 56: 293-312. DOI: https://doi.org/10.1146/annurev-ento-120709-144802

Rutschmann, B., Kohl, P.L., Machado, A. & Steffan-Dewenter, I. (2022). Semi-natural habitats promote winter survival of wild-living honeybees in an agricultural landscape. Biological Conservation, 266: 109450. DOI: https://doi.org/10.1016/j.biocon.2022.109450

Sabbahi, R., De Oliveira, D. & Marceau, J. (2005). Influence of honey bee (Hymenoptera: Apidae) density on the production of canola (Crucifera: Brassicacae). Journal of Economic Entomology, 98: 367-372. DOI: https://doi.org/10.1603/0022-0493-98.2.367

Schüepp, C., Rittiner, S. & Entling, M.H. (2012). High bee and wasp diversity in a heterogeneous tropical farming system compared to protected forest. PLoS ONE, 7: 1-8. DOI: https://doi.org/10.1371/journal.pone.0052109

Serralta-Batun, L.P., Jiménez-Osornio, J.J., Meléndez-Ramírez, V. & Munguía-Rosas, M.A. (2024). Taxonomic and functional diversity of bees in traditional agroecosystems and tropical forest patches on the Yucatan Peninsula. Tropical Conservation Science, 17: 1-16. DOI: https://doi.org/10.1177/19400829231225428

Shaw, R.F., Phillips, B.B., Doyle, T., Pell, J.K. & Redhead, J.W. (2020). Mass-flowering crops have a greater impact than semi-natural habitat on crop pollinators and pollen deposition. Landscape Ecology, 35: 513-527. DOI: https://doi.org/10.1007/s10980-019-00962-0

Sheffield, C.S., Kevan, P.G., Westby, S.M. & Smith, R.F. (2008). Diversity of cavity-nesting bees (Hymenoptera: Apoidea) within apple orchards and wild habitats in the Annapolis Valley, Nova Scotia, Canada. The Canadian Entomologist, 140: 235-249. DOI: https://doi.org/10.4039/n07-058

Springmann, M., Clark, M., Mason-D’Croz, D., Wiebe, K. & Bodirsky, B.L. (2018). Options for keeping the food system within environmental limits. Nature, 562: 519-525. DOI: https://doi.org/10.1038/s41586-018-0594-0

Stodden, V., Seiler, J. & Ma, Z. (2018). An empirical analysis of journal policy effectiveness for computational reproducibility. Proceedings of the National Academy of Sciences USA, 115: 2584-2589. DOI: https://doi.org/10.1073/pnas.1708290115

Tilman, D., Clark, M., Williams, D.R., Kimmel, K., Polasky, S. & Packer, C. (2017). Future threats to biodiversity and pathways to their prevention. Nature, 546: 73-81. DOI: https://doi.org/10.1038/nature22900

Vides-Borrell, E., Porter-Bolland, L., Ferguson, B.G., Gasselin, P., Vaca, R., Valle-Mora, J. & Vandame, R. (2019). Polycultures, pastures and monocultures: Effects of land use intensity on wild bee diversity in tropical landscapes of southeastern Mexico. Biological Conservation, 236: 269-280. DOI: https://doi.org/10.1016/j.biocon.2019.04.025

Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor Package. Journal of Statistical Software, 36: 1-48. DOI: https://doi.org/10.18637/jss.v036.i03

Westphal, C., Steffan-Dewenter, I. & Tscharntke, T. (2003). Mass flowering crops enhance pollinator densities at a landscape scale. Ecology Letters, 6: 961-965. DOI: https://doi.org/10.1046/j.1461-0248.2003.00523.x

Wille, A. (1983). Biology of the stingless bees. Annual Review of Entomology, 28: 41-64. DOI: https://doi.org/10.1146/annurev.en.28.010183.000353

Winfree, R., Aguilar, R., Vázquez, D.P., LeBuhn, G. & Aizen, M.A. (2009). A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology, 90: 2068-2076. DOI: https://doi.org/10.1890/08-1245.1

Yang, L.H. and Gratton, C. (2014). Insects as drivers of ecosystem processes. Current Opinion in Insect Science, 2: 26-32. DOI: https://doi.org/10.1016/j.cois.2014.06.004

Zabel, F., Delzeit, R., Schneider, J.M., Seppelt, R., Mauser, W. & Václavík, T. (2019). Global impacts of future cropland expansion and intensification on agricultural markets and biodiversity. Nature Communications, 10: 1-10. DOI: https://doi.org/10.1038/s41467-019-10775-z

Zurbuchen, A., Landert, L., Klaiber, J., Müller, A., Hein, S. & Dorn, S. (2010). Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biological Conservation, 143: 669-676. DOI: https://doi.org/10.1016/j.biocon.2009.12.003