Cerrado, landscape heterogeneity, networks, Savanna, structure


The role of agriculture as a menace or a contribution to the maintenance of the biodiversity and ecosystems function (such as pollination) in heterogeneous landscapes is critical to the balance in the tradeoff relationships between food production and biodiversity. Recent studies suggested that the role of agriculture to the maintenance of biodiversity can be context dependent. Therefore, this study aimed to evaluate the interplay between the proportion of agriculture and landscape heterogeneity on the maintenance of pollinators richness and abundance, and plant-pollinators interactions in agro-natural landscapes. Plant-pollinator surveys were conducted in seminatural areas near agricultural areas in 22 landscapes in the agricultural pole of Chapada Diamantina, Bahia, Brazil. By a combination of PCA and clustering analysis the landscapes were divided into two groups characterized by the inverse correlation of proportion of agriculture and heterogeneity. The first group had low proportion of agriculture and high landscape diversity and the second group had high proportion of agriculture and low landscape diversity. Using linear models, we investigated the differences in plant-pollinator networks structure between these two landscape groups and its relationship with the proportion of agriculture. Our results showed that there is a positive relationship between the plant-pollinator networks number of links, the pollinator species richness and native pollinators abundance with the proportion of agriculture in the landscapes. However, the most heterogeneous landscapes, with smaller proportions of agriculture have networks with more links, higher pollinator species richness and native pollinators abundance than more homogenous landscapes with greater proportions of agriculture. In this sense, even if agricultural areas can favor some pollinators, there are evident losses of pollinator diversity and plant-pollinator interactions associated with the landscape homogenization.

Author Biographies

Eduardo Freitas Moreira, Universidade Federal da Bahia

Phd studant in the Programa de Pós-graduação em Ecologia e Biomonitoramento from the Intituto de Biologia da Universidade Federal da Bahia

National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE).

Danilo Boscolo, Universidade de São Paulo

Professor in the Faculdade de Filosofia Ciências e Letras de Ribeirão Preto Departamento de Biologia: Ribeirao Preto

National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE).

Blandina Felipe Viana, Universidade Federal da Bahia

Professor in the Departamento de Zologia, Instituto de Biologia, Universidade Federal da Bahia


Almeida-Neto, M., & Ulrich, W. 2011. A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling & Software, 26(2), 173–178. DOI: 10.1016/j.envsoft.2010.08.003

Bascompte, J., Jordano, P., & Olesen, J. M. 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science, 312(5772), 431–3. DOI: 10.1126/science.1123412

Blüthgen, N., Fründ, J., Vazquez, D. P., & Menzel, F. 2008. What do interaction network metrics tell us about specialization and biological traits? Ecology, 89(12), 3387–3399. DOI: 10.1890/07-2121.1

Blüthgen, N., Menzel, F., Hovestadt, T., Fiala, B., & Blüthgen, N. 2007. Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology, 17(4), 341–6. DOI: 10.1016/j.cub.2006.12.039

Blüthgen, N., Menzel, F., & Blüthgen, N. 2006. Measuring specialization in species interaction networks. BMC Ecology, 6(9), 1–12. DOI: 10.1186/1472-6785-6-9

Chaplin-Kramer, R., Dombeck, E., Gerber, J., Knuth, K. A, Mueller, N. D., Mueller, M., & Klein, A. M. 2014. Global malnutrition overlaps with pollinator-dependent micronutrient production. Proceedings Biological Sciences, 281(1794), 1–2. DOI: 10.1098/rspb.2014.1799

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. GCB Bioenergy, 6(3), 219–226. DOI: 10.1111/gcbb.12080

Dormann, C. F., Gruber, B., & Fründ, J. 2008. Introducing the bipartite Package: Analysing Ecological Networks, 8–11.

Eilers, E. J., Kremen, C., Smith Greenleaf, S., Garber, A. K., & Klein, A. M. 2011. Contribution of pollinator-mediated crops to nutrients in the human food supply. PloS One, 6(6), e21363. DOI: 10.1371/journal.pone.0021363

Fahrig, L., Girard, J., Duro, D., Pasher, J., Smith, A., Javorek, S., & Mitchell, S. 2015. Farmlands with smaller crop fields have higher within-field biodiversity. Agriculture, Ecosystems & Environment, 219–234. DOI: 10.1016/j.agee.2014.11.018

Fahrig, L., Baudry, J., Brotons, L., Burel, F. G., Crist, T. O., Fuller, R. J., & Martin, J. L. 2011. Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecology Letters, 14(2), 101–112. DOI: 10.1111/j.1461-0248.2010.01559.x

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(10), 2067–2078. DOI: 10.1007/s10980-015-0231-3

Ferreira, P. A., Boscolo, D., & Viana, B. F. 2013. What do we know about the effects of landscape changes on plant-pollinator interaction networks? Ecological Indicators, 31, 35–40. DOI: 10.1016/j.ecolind.2012.07.025

Foley, J. A., DeFries, R., Asnes, G. P., Barford, C., Bonan, G., Carpenter, S. R., Chapin, F. S., Coe, M. T., Daily, G. C., Gibbs, H. K., Helkowski, J. H., Holloway, T., Howard, E. A., Kucharik, C. J., Monfreda, C., Patz, J. A., Prentice, I. C., Ramankutty, N., & Snyder, P. K. 2005. Global consequences of land use. Science, 309, 570–574. DOI: 10.1126/science.1111772

Fortuna, M. A., Krishna, A., & Bascompte, J. 2013. Habitat loss and the disassembly of mutualistic networks. Oikos, 122, 938–942. DOI: 10.1111/j.1600-0706.2012.00042.x

Fründ, J., McCann, K. S., & Williams N, M. 2016. Sampling bias is a challenge for quantifying specialization and network structure: lessons from a quantitative niche model. Oikos, 125, 502–513. DOI: 10.1111/oik.02256

Garibaldi, L. A., Carvalheiro, L. G., Vaissière, B. E., Gemmill-Herren, B., Hipólito, J., Freitas, B. M., & Zhang, H. 2016. Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science, 351(6271), 388–391. DOI: 10.1126/science.aac7287

Garibaldi, L. A., Carvalheiro, L. G., Leonhardt, S. D., Aizen, M. A., Blaauw, B. R., Isaacs, R., & Winfree, R. 2014. From research to action: Enhancing crop yield through wild pollinators. Frontiers in Ecology and the Environment, 12(8), 439–447. DOI: 10.1890/130330

Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., & Klein, A. M. 2013. Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance. Science, 339(6127), 1608–1611. DOI: 10.1126/science.1230200

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. Proceedings of the National Academy of Sciences of the United States of America, 108(14), 5909–14. DOI: 10.1073/pnas.1012431108

Hipólito, J., Boscolo, D., & Viana, B. F. 2018. Landscape and crop management strategies to conserve pollination services and increase yields in tropical coffee farms. Agriculture, Ecosystems & Environment, 256, 218–225. DOI: 10.1016/j.agee.2017.09.038

Hothorn, T., & Everitt, B. S. 2014. A handbook of statistical analyses using R. 3rd ed. Chapman & Hall/CRC: p. 456.

IBGE. 2012 Manual técnico da vegetação brasileira. 2nd ed, Manuais Técnicos em Geociências, Rio de Janeiro. p. 271

Juncá, F.A., Funch, L., & Rocha, W. 2005. Biodiversidade e conservação da Chapada Diamantina. Ministério do Meio Ambiente, Brasília: p. 411.

Kennedy, C. M., Lonsdorf, E., Neel, M. C., Williams, N. M., Ricketts, T. H., Winfree, R., & Kremen, C. 2013. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecology Letters, 16(5), 584–599. DOI: 10.1111/ele.12082

Kottek, M., Grieser, J., Beck, C., Rudolf, B., & Rubel, F. 2006. World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift, 15(3), 259–263. DOI: 10.1127/0941-2948/2006/0130

Moreira, E. F., Ferreira, P. A., Lopes, L. E., Soares, R. G. S., & Boscolo, D. 2018. Ecological Networks in Changing Tropics. In: W. Dáttilo, & V. Rico-Gray (Eds.), Ecological Networks in the Tropics. pp. 155–169. Springer, Cham. DOI: 10.1007/978-3-319-68228-0_11

Moreira, E. F., Lorena, R., De, W., Sant, J., Boscolo, D., & Pigozzo, C. M. 2016. Comparison and performance of parametric algorithms in supervised classification of naturally heterogeneous and dynamic area. Revista Brasileira de Cartografia, 68(3), 581–594.

Moreira, E. F., Boscolo, D., & Viana, B. F. 2015. Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS ONE, 10(4), 1–19. DOI: 10.1371/journal.pone.0123628

Okuyama, T., & Holland, J. N. 2008. Network structural properties mediate the stability of mutualistic communities. Ecology Letters, 11(3), 208–216. DOI: 10.1111/j.1461-0248.2007.01137.x

Peel, M. C., Finlayson, B. L., & McMahon, T. A. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences, 11, 1633–1644. DOI: 10.5194/hess-11-1633-2007

Phalan, B., Onial, M., Balmford, A., & Green, R. E. 2011. Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science, 333(6047), 1289–1291. DOI: 10.1126/science.1208742

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(6), 345–53. DOI: 10.1016/j.tree.2010.01.007

Power, A. G. 2010. Ecosystem services and agriculture: tradeoffs and synergies. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365(1554), 2959–71. DOI: 10.1098/rstb.2010.0143

Quinn, G. P., & M. J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge University Press: p. 553.

Ricketts, T. H., Regetz, J., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., Bogdanski, A., Gemmill-Herren, B., Greenleaf, S. S., Klein, A. M., Mayfield, M. M., Morandin, L. A., Ochieng, A., & Viana, B. F. 2008. Landscape effects on crop pollination services: are there general patterns? Ecology Letters, 11, 499–515. DOI: 0.1111/j.1461-0248.2008.01157.x

Rodríguez, A., & Kouki, J. 2017. Disturbance‐mediated heterogeneity drives pollinator diversity in boreal managed forest ecosystems. Ecological Applications, 27(2), 589–602. DOI: 10.1002/eap.1468

Rundlöf, M., Nilsson, H., & Smith, H. G. 2008. Interacting effects of farming practice and landscape context on bumble bees. Biological Conservation, 141(2), 417–426. DOI: 10.1016/j.biocon.2007.10.011

Soares, R. G. S., Ferreira, P. A., & Lopes, L. E. 2017. Can plant-pollinator network metrics indicate environmental quality? Ecological Indicators, 78(July), 361–370. DOI: 10.1016/j.ecolind.2017.03.037

Stein, A., Gerstner, K., & Kreft, H. 2014. Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology Letters, 17, 866–880. DOI: 10.1111/ele.12277

Tylianakis, J. M., Laliberté, E., Nielsen, A., & Bascompte, J. 2010. Conservation of species interaction networks. Biological Conservation, 143, 2270–2279. DOI: 10.1016/j.biocon.2009.12.004

Veloso, P. H., Filho, R. R. L. A., & Lima, A. C. J. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal. Fundação Instituto Brasileiro de Geografia e Esatística. IBGE: p. 117.

Vieira, M. C., & Almeida-Neto, M. 2015. A simples stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance. Ecology Letters, 18(2), 144–152. DOI: 10.1111/ele.12394

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

Winfree, R., Aguilar, R., Vazquez, D. P., LeBuhn, G., & Aizen, M. 2009. A meta-analysis of bees' responses to anthropogenic disturbance. Ecology, 90, 2068–2076. DOI: 10.1890/08-1245.1

Zhang, W., Ricketts, T. H., Kremen, C., Carney, K., & Swinton, S. M. 2007. Ecosystem services and dis-services to agriculture, 1–8. DOI: 10.1016/j.ecolecon.2007.02.024

Zou, Y., Bianchi, F. J. J. A., Jauker, F., Xiao, H., Chen, J., Cresswell, J., & van der Werf, W. 2017. Landscape effects on pollinator communities and pollination services in small-holder agroecosystems. Agriculture, Ecosystems and Environment, 246, 109–116. DOI: 10.1016/j.agee.2017.05.035