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Forest proximity rather than local forest cover affects bee diversity and coffee pollination services

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Abstract

Context

As agricultural demands for land continues to expand, strategies are urgently needed to balance agricultural production with biodiversity conservation and ecosystem service provision in agricultural landscapes.

Objectives

We used a factorial landscape design to assess the relative contributions of forest proximity and local forest cover to bee diversity and the provision of coffee pollination services.

Methods

We quantified bee diversity and fruit set in 24 sun-grown coffee fields in Southeast Region of Brazil that were selected following a factorial sampling design to test the independent effects of local forest cover (in a radius of 400 m) and proximity to forest fragments. To assess the impact of landscape simplification, we also evaluated local coffee cover.

Results

Bee richness and abundance were higher in the proximity of forest fragments, but only bee abundance decreased when the coffee cover dominated the surrounding landscapes. Coffee fruit set was 16% higher overall with bee visitations compared with bee exclusion and increased to 20% when coffee bushes were near forest fragments, and the coffee cover was low. Surprisingly, local forest cover did not affect the bee community or coffee fruit set.

Conclusion

Our results provide clear evidence that the proximity of coffee crops to forest fragments can affect the abundance and richness of bees visiting the coffee flowers and thereby facilitate the provision of pollination services. The positive association between forest proximity and fruit set reinforces the importance of natural vegetation in enhancing bee diversity and, therefore, in the provision of pollination services. The negative effect of coffee cover on fruit set at the local scale suggests that the service demand can surpass the capacity of pollinators to provide it. These effects were independent of the local forest cover, although all studied landscapes had more than 20% remaining forest cover (within a 2 km radius), which is considered the extinction threshold for Atlantic Forest species. Interspersion of forest fragments and coffee plantations in regions with more than 20% of forest cover left could thus be a useful landscape management target for facilitating pollinator flows to coffee crops and thus for increasing coffee yields.

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References

  • Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2009) How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann Bot 103:1579–1588

    PubMed  PubMed Central  Google Scholar 

  • Araújo ED, Costa M, Chaud-Netto J, Fowler HG (2004) Body size and flight distance in stingless bees (Hymenoptera: Meliponini): inference of flight range and possible ecological implications. Braz J Biol 64:563–568

    PubMed  Google Scholar 

  • Aristizábal N, Metzger JP (2019) Landscape structure regulates pest control provided by ants in sun coffee farms. J Appl Ecol 56:21–30

    Google Scholar 

  • Banks-Leite C, Pardini R, Tambosi LR, Pearse WD, Bueno AA, Bruscagin RT, Condez TH, Dixo M, Igari AT, Martensen AC, Metzger JP (2014) Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science 80(345):1041–1045

    Google Scholar 

  • Barton K (2015) MuMIn: Multi-model inference. R package version 1.9.13. Version 1:18. 11961261

  • Batáry P, Báldi A, Kleijn D, Tscharntke T (2011) Landscape-moderated biodiversity effects of agri-environmental management: a meta-analysis. Proc Biol Sci 278:1894–1902

    PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • 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 4:19–23

    Google Scholar 

  • Benjamin FE, Reilly JR, Winfree R (2014) Pollinator body size mediates the scale at which land use drives crop pollination services. J Appl Ecol 51:440–449

    Google Scholar 

  • Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188

    Google Scholar 

  • Blitzer EJ, Dormann CF, Holzschuh A, Klein  AM, Rand TA, Tscharntke T (2012) Spillover of functionally important organisms between managed and natural habitats. Agric Ecosyst Environ 146:34–43. https://doi.org/10.1016/J.AGEE.2011.09.005

    Article  Google Scholar 

  • Boesing AL, Nichols E, Metzger JP (2018) Biodiversity extinction thresholds are modulated by matrix type. Ecography 41(9):1520–1533

    Google Scholar 

  • Brosi BJ, Daily GC, Shih TM, Oviedo F, Durán G (2008) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45:773–783

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Burton RJF, Kuczera C, Schwarz G (2008) Exploring farmers’ cultural resistance to voluntary agri-environmental schemes. Sociol Ruralis 48:16–37

    Google Scholar 

  • Connelly H, Poveda K, Loeb G (2015) Landscape simplification decreases wild bee pollination services to strawberry. Agric Ecosyst Environ 211:51–56

    Google Scholar 

  • Dainese M, Martin EA, Aizen M , Albrecht M, Bartomeus I, Bommarco R, Ghazoul J (2019) A global synthesis reveals biodiversity-mediated benefits for crop production. Sci Adv 5:554170

    Google Scholar 

  • DaMatta FM (2004) Ecophysiological constraints on the production of shaded and unshaded coffee: a review. F Crop Res 86:99–114

    Google Scholar 

  • De Marco P, Coelho FM (2004) Services performed by the ecosystem: Forest remnants influence agricultural cultures’ pollination and production. Biodivers Conserv 13:1245–1255

    Google Scholar 

  • Ekroos J, Olsson O, Rundlöf M, Wätzold F, Smith HG (2014) Optimizing agri-environment schemes for biodiversity, ecosystem services or both? Biol Conserv 172:65–71

    Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Syst 34:487–515

    Google Scholar 

  • Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

    Google Scholar 

  • Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Balzer C (2011) Solutions for a cultivated planet. Nature 478:337–342

    CAS  PubMed  Google Scholar 

  • Garibaldi LA, Carvalheiro LG, Vaissiere BE, Gemmill-Herren B, Hipólito J, Freitas BM, An J (2016) Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 351:388–391

    CAS  PubMed  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Holzschuh A (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072

    PubMed  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Bartomeus I (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 340:1608–1611

    Google Scholar 

  • Giannini TC, Garibaldi LA, Acosta AL, Silva JS, Maia KP, Saraiva AM, Kleinert AM (2015) Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS ONE 10:e0137198

    PubMed  PubMed Central  Google Scholar 

  • Gibbs HK, Ruesch AS, Achard F, Clayton MK, Holmgren P, Ramankutty N, Foley JA (1990) Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proc Natl Acad Sci USA 107:16732–16737

    Google Scholar 

  • Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined Stress from parasites, pesticides, and lack of flowers. Science 347:6229

    Google Scholar 

  • Hartig F (2017) Package “DHARMa” Title Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models

  • Hipólito J, Boscolo D, Viana BF (2018) Landscape and crop management strategies to conserve pollination services and increase yields in tropical coffee farms. Agric Ecosyst Environ 256:218–225

    Google Scholar 

  • Holzschuh A, Dainese M, González-Varo JP, Mudri-Stojnić S, Riedinger V, Rundlöf M, Kleijn D (2016) Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe. Ecol Lett 19:1228–1236

    PubMed  PubMed Central  Google Scholar 

  • Holzschuh A, Dormann CF, Tscharntke T, Steffan-Dewenter I (2011) Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination. Proc R Soc B Biol Sci 278:3444–3451

    Google Scholar 

  • Jaffé R, Castilla A, Pope N, Imperatriz-Fonseca VL, Metzger JP, Arias MC, Jha S (2015) Landscape genetics of a tropical rescue pollinator. Conserv Genet. https://doi.org/10.1007/s10592-015-0779-0

    Article  Google Scholar 

  • Jha S, Vandermeer JH (2009) Contrasting bee foraging in response to resource scale and local habitat management. Oikos 118:1174–1180

    Google Scholar 

  • Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R, Carvalheiro LG (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599

    PubMed  Google Scholar 

  • Klein AM (2009) Nearby rainforest promotes coffee pollination by increasing spatio-temporal stability in bee species richness. For Ecol Manag 258:1838–1845

    Google Scholar 

  • Klein A-M, Steffan-Dewenter I, Tscharntke T (2003a) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc B Biol Sci 270:955–961

    Google Scholar 

  • Klein AM, Steffan-Dewenter I, Tscharntke T (2003b) Bee pollination and fruit set of Coffea arabica and C. canephora (Rubiaceae). Am J Bot 90:153–157

    PubMed  Google Scholar 

  • Krishnan S, Kushalappa CG, Shaanker RU, Ghazoul J (2012) Status of pollinators and their efficiency in coffee fruit set in a fragmented landscape mosaic in South India. Basic Appl Ecol 13:277–285

    Google Scholar 

  • Librán-Embid F, De Coster G, Metzger JP (2017) Effects of bird and bat exclusion on coffee pest control at multiple spatial scales. Landsc Ecol 32:1907–1920

    Google Scholar 

  • Lichtenberg EM, Mendenhall CD, Brosi B (2017) Foraging traits modulate stingless bee community disassembly under forest loss. J Anim Ecol 86:1404–1416

    PubMed  Google Scholar 

  • Losey JE, Vaughn M (2006) The economic value of ecological services provided by insects. Bioscience 56:311

    Google Scholar 

  • Martin EA, Dainese M, Clough Y, Báldi A, Bommarco R, Gagic V, Marini L (2019) The interplay of landscape composition and configuration: new pathways to manage functional biodiversity and agroecosystem services across Europe. Ecol Lett 22:1083–1094

    PubMed  Google Scholar 

  • Metzger JP, Bustamante MMC, Ferreira J, Fernandes GW, Librán-Embid F, Pillar VD, Overbeck GE (2019) Why Brazil needs its Legal Reserves. Perspect Ecol Conserv. https://doi.org/10.1016/j.pecon.2019.07.002

    Article  Google Scholar 

  • Mitchell MGE, Suarez-Castro AF, Martinez-Harms M, Maron M, McAlpine C, Gaston KJ, Rhodes JR (2015) Reframing landscape fragmentation’s effects on ecosystem services. Trends Ecol Evol 30:190–198

    PubMed  Google Scholar 

  • Moreira EF, Boscolo D, Viana BF (2015) Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS ONE 10:1–19

    Google Scholar 

  • Moure JS, Melo GAR, Vivallo F (2012) Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version. https://www.moure.cria.org.br/catalogue

  • Munyuli T (2011) Factors governing flower visitation patterns and quality of pollination services delivered by social and solitary bee species to coffee in central Uganda. Afr J Ecol 49:501–509

    Google Scholar 

  • Ngo HT, Mojica AC, Packer L (2011) Coffee plant – pollinator interactions: a review. Can J Zool 89:647–660

    Google Scholar 

  • Olschewski R, Tscharntke T, Benítez PC, Schwarze S, Klein AM (2006) Economic evaluation of pollination services comparing coffee landscapes in Ecuador and Indonesia. Ecol Soc 11:7

    Google Scholar 

  • Perfecto I, Vandermeer J (2010) The agroecological matrix as alternative to the land-sparing/agriculture intensification model. Proc Natl Acad Sci USA 107:5786–5791

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • R Develop Core Team (2018) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.T-project.org/

  • Renner S (1983) The widespread occurrence of anther destruction by Trigona bees in Melastomataceae. Biotropica. https://doi.org/10.2307/2387649

    Article  Google Scholar 

  • Rezende CL, Scarano FR, Assad ED, Joly CA, Metzger JP, Strassburg BBN, Mittermeier RA (2018) From hotspot to hopespot: an opportunity for the Brazilian Atlantic Forest. Perspect Ecol Conserv 16:208–214

    Google Scholar 

  • 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

    Google Scholar 

  • Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops\rfragmentos de bosque tropical incrementan la actividad de polinizadores en cultivos de café cercanos. Conserv Biol 18:1262–1271

    Google Scholar 

  • Ricketts T, Daily G, Ehrlich P, Michener C (2004) Economic value of tropical forest to coffee production. Proc Natl Acad Sci USA 101:12579–12661

    CAS  PubMed  Google Scholar 

  • Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Morandin LA (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515

    PubMed  Google Scholar 

  • Roubik DW (2000) Pollination system stability in tropical America. Conserv Biol 14:1235–1236

    Google Scholar 

  • Saturni FT, Jaffé R, Metzger JP (2016) Landscape structure influences bee community and coffee pollination at different spatial scales. Agric Ecosyst Environ 235:1–12

    Google Scholar 

  • Saunders ME, Peisley RK, Rader R, Luck GW (2015) Pollinators, pests, and predators: recognizing ecological trade-offs in agroecosystems. Ambio 45:4–14

    PubMed  PubMed Central  Google Scholar 

  • Sirami C, Gross N, Baillod AB, Bertrand C, Carrié R, Hass A, Girard J (2019) Increasing crop heterogeneity enhances multitrophic diversity across agricultural regions. Proc Natl Acad Sci USA 116:16442–16447

    CAS  PubMed  Google Scholar 

  • Taki H, Kevan PG, Ascher JS (2007) Landscape effects of forest loss in a pollination system. Landsc Ecol 22:1575–1587

    Google Scholar 

  • Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Ewers RM (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87:661–685

    PubMed  Google Scholar 

  • Vanbergen AJ (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259

    Google Scholar 

  • Veddeler D, Klein AM, Tscharntke T (2006) Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos 112:594–601

    Google Scholar 

  • Vieira KM, Netto P, Dlas A, Mendes SS, Castro LC, Prezoto F (2016) Nesting stingless bees in urban areas: a reevaluation after eight years. Sociobiology 63:976–981

    Google Scholar 

  • Villard MA, Metzger JP (2014) Beyond the fragmentation debate: a conceptual model to predict when habitat configuration really matters. J Appl Ecol 51:309–318

    Google Scholar 

  • Westphal C, Steffan-Dewenter I, Tscharntke T (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol Lett 6:961–965

    Google Scholar 

  • Zanette LRS, Martins RP, Ribeiro SP (2005) Effects of urbanization on Neotropical wasp and bee assemblages in a Brazilian metropolis. Landsc Urban Plan 71:105–121

    Google Scholar 

  • Zuckerberg B, Desrochers A, Hochachka WM, Fink D, Koenig WD, Dickinson JL (2012) Overlapping landscapes: a persistent, but misdirected concern when collecting and analyzing ecological data. J Wildl Manag 76:1072–1080

    Google Scholar 

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Acknowledgements

We are profoundly thankful to the coffee farmers for granting us access to their properties. Especially to the Leite Marquezini family for the support during the fieldwork and throughout the research project. We would like to acknowledge Tereza Cristina Giannini, for her inputs on the experimental design and contributions throughout this project. Also, we thank Luisa G. Carvalheiro, Blandina F. Viana and Denise Araujo for valuable discussions over the first version of this manuscript. We thank Chris Davis for English revisions. We will also like to thank the teamwork which included all members of the Interface project, especially Natalia Aristizabal, Isabela Romitelli, Francisco d’Albertas, Felipe Libran, Larissa Boesing from the LEPaC laboratory, Liedson Carneiro, Sheina Koffler and William Sabino from the Bee Laboratory, USP.

Funding

The study was funded by a FAPESP grant (Interface Project, N. 2013/23457-6). RJ and JPM were supported by the Brazilian Science Council (CNPq; grants 301616/2017-5, 306121/2016-6, and 305484/2017-6). The Brazilian Ministry of Education supported A.G-Ch (CAPES–DS; 2014- 2016).

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Authors and Affiliations

  1. Departamento de Ecologia, Universidade de São Paulo, Rua do Matão 321, São Paulo, 05508-090, Brazil

    Adrian González-Chaves, Rodolfo Jaffé, Jean Paul Metzger & Astrid de M. P. Kleinert

  2. Instituto Tecnológico Vale, Rua Boaventura da Silva 955, Belém, PA, 66055-090, Brazil

    Rodolfo Jaffé

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  1. Adrian González-Chaves
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  2. Rodolfo Jaffé
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  3. Jean Paul Metzger
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  4. Astrid de M. P. Kleinert
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Contributions

Adrian González-Chaves (AGCh), Rodolfo Jaffé (RJ), Jean Paul Metzger (JPM), and Astrid de Matos Peixoto Kleinert (AMPK) together planned and design the project, as well as were involved in writing the manuscript. JPM obtained project funding was obtained by. AGCh collected the data, which was analyzed by AGCh and RJ.

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Correspondence to Adrian González-Chaves.

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González-Chaves, A., Jaffé, R., Metzger, J.P. et al. Forest proximity rather than local forest cover affects bee diversity and coffee pollination services. Landscape Ecol 35, 1841–1855 (2020). https://doi.org/10.1007/s10980-020-01061-1

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