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Fragmentation and Management of Ethiopian Moist Evergreen Forest Drive Compositional Shifts of Insect Communities Visiting Wild Arabica Coffee Flowers

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Abstract

Coffea arabica is an indigenous understorey shrub of the moist evergreen Afromontane forest of SW Ethiopia. Coffee cultivation here occurs under different forest management intensities, ranging from almost no intervention in the ‘forest coffee’ system to far-reaching interventions that include the removal of competing shrubs and selective thinning of the upper canopy in the ‘semi-forest coffee’ system. We investigated whether increasing forest management intensity and fragmentation result in impacts upon potential coffee pollination services through examining shifts in insect communities that visit coffee flowers. Overall, we netted 2,976 insect individuals on C. arabica flowers, belonging to sixteen taxonomic groups, comprising 10 insect orders. Taxonomic richness of the flower-visiting insects significantly decreased and pollinator community changed with increasing forest management intensity and fragmentation. The relative abundance of honey bees significantly increased with increasing forest management intensity and fragmentation, likely resulting from the introduction of bee hives in the most intensively managed forests. The impoverishment of the insect communities through increased forest management intensity and fragmentation potentially decreases the resilience of the coffee production system as pollination increasingly relies on honey bees alone. This may negatively affect coffee productivity in the long term as global pollination services by managed honey bees are expected to decline under current climate change scenarios. Coffee agroforestry management practices should urgently integrate pollinator conservation measures.

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References

  • Aerts R, Hundera K, Berecha G, Gijbels P, Baeten M, Van Mechelen M et al (2011) Semi-forest coffee cultivation and the conservation of Ethiopian Afromontane rainforest fragments. For Ecol Manage 261:1034–1041

    Article  Google Scholar 

  • Aerts R, Berecha G, Gijbels P, Hundera K, Van Glabeke S, Vandepitte K et al (2013) Genetic variation and risks of introgression in the wild Coffea arabica gene pool in southwestern Ethiopian montane rainforests. Evol Applic 6:243–252

    Article  Google Scholar 

  • Aizen MA, Feinsinger P (1994) Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine chaco serrano. Ecol Appl 4:378–392

    Article  Google Scholar 

  • Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918

    Article  CAS  Google Scholar 

  • Anthony F, Bertrand B, Quiros O, Wilches A, Lashermes P, Berthaud J et al (2001) Genetic diversity of wild coffee (Coffea arabica L.) using molecular markers. Euphytica 118:53–65

    Article  CAS  Google Scholar 

  • Anthony F, Combes MC, Astorga C, Bertrand B, Graziosi G, Lashermes P (2002) The origin of cultivated Coffea arabica L. varieties revealed by AFLP and SSR markers. Theor Appl Genet 104:894–900

    Article  CAS  Google Scholar 

  • Badano EI, Vergara CH (2011) Potential negative effects of exotic honey bees on the diversity of native pollinators and yield of highland coffee plantations. Agric For Entomol 13:365–372

    Article  Google Scholar 

  • Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Ann Rev Ecol Systemat 21:399–422

    Article  Google Scholar 

  • Berecha G (2014) Genetic diversity, pollination ecology and organoleptic characteristics of Coffea arabica L. in Ethiopian moist forests of different management intensity. Dissertation. Ph.D. University of Leuven. ISBN 978-90-8649-765-2

  • Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    Article  CAS  Google Scholar 

  • Boreux V, Krishnan S, Cheppudira KG, Ghazoul J (2013a) Impact of forest fragments on bee visits and fruit set in rain-fed and irrigated coffee agro-forests. Agric Ecosyst Environ 172:42–48

    Article  Google Scholar 

  • Boreux V, Kushalappa CG, Vaast P, Ghazoul J (2013b) Interactive effects among ecosystem services and management practices on crop production: pollination in coffee agroforestry systems. Proc Natl Acad Sci USA 110:8387–8392

    Article  CAS  Google Scholar 

  • Briggs HM, Perfecto I, Brosi BJ (2013) The role of the agricultural matrix: coffee management and Euglossine bee (Hymenoptera: Apidae: Euglossini) communities in Southern Mexico. Environ Entomol 42:1210–1217

    Article  CAS  Google Scholar 

  • Broadbent EN, Asner GP, Keller M, Knapp DE, Oliveira PJC, Silva JN (2008) Forest fragmentation and edge effects from deforestation and selective logging in the Brazilian Amazon. Biol Conserv 141:1745–1757

    Article  Google Scholar 

  • Brosi BJ (2009) The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biol Conserv 142:414–423

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Burkle LA, Marlin JC, Knight TM (2013) Plant–pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615

    Article  CAS  Google Scholar 

  • Carvalheiro LG, Veldtman R, Shenkute AG, Tesfay GB, Pirk CWW, Donaldson JS et al (2011) Natural and within-farmland biodiversity enhances crop productivity. Ecol Lett 14:251–259

    Article  Google Scholar 

  • Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. Plant Ecol 5:3–21

    Article  Google Scholar 

  • De Beenhouwer M, Aerts R, Honnay O (2013) A global meta-analysis of the biodiversity and ecosystem service benefits of coffee and cacao agroforestry. Agric Ecosyst Environ 175:1–7

    Article  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

    Article  Google Scholar 

  • Dick CW (2001) Genetic rescue of remnant tropical trees by an alien pollinator. Proc Roy Soc London B Biol Sci 268:2391–2396

    Article  CAS  Google Scholar 

  • Didham RK, Lawton JH (1999) Edge structure determines the magnitude of changes in microclimate and vegetation structure in tropical forest fragments. Biotropica 31:17–30

    Google Scholar 

  • Donald PF (2004) Biodiversity impacts of some agricultural commodity production systems. Conserv Biol 18:17–37

    Article  Google Scholar 

  • Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO et al (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43

    Article  Google Scholar 

  • FAO (2011) State of the world’s forests report. Food and Agriculture Organization (FAO), Rome

  • Fichtl R, Adi A (1994) Honeybee flora of Ethiopia. The National Herbarium, Addis Ababa, and Deutscher Entwicklungsdienst (DED). Margraf, Weikersheim

  • Friis I (1992) Forests and forest trees of northeast tropical Africa: their natural habitats and distribution patterns in Ethiopia, Djibouti and Somalia. Volume 15 of Kew bulletin additional series. Her Majesty's Stationery Office, London

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611

    Article  CAS  Google Scholar 

  • Getahun K, Van Rompaey A, Van Turnhout P, Poesen J (2013) Factors controlling patterns of deforestation in moist evergreen Afromontane forests of Southwest Ethiopia. For Ecol Manage 304:171–181

    Article  Google Scholar 

  • Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–108

    Article  CAS  Google Scholar 

  • González-Varo JP, Arroyo J, Aparicio A (2009) Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biol Conserv 142:1058–1065

    Article  Google Scholar 

  • Hendrickx F, Maelfait J, Van Wingerden W, Schweiger O, Speelmans M, Aviron S et al (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44:340–351

    Article  Google Scholar 

  • Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432

    Article  Google Scholar 

  • Hundera K, Aerts R, Fontaine A, Van Mechelen M, Gijbels P, Honnay O et al (2013a) Effects of wild coffee management intensity on composition, structure and regeneration of Ethiopian montane rainforests. Environ Manage 51:801–809

    Article  Google Scholar 

  • Hundera K, Aerts R, De Beenhouwer M, Van Overtveld K, Helsen K, Muys B (2013b) Both forest fragmentation and coffee cultivation negatively affect epiphytic orchid diversity in Ethiopian moist evergreen Afromontane forests. Biol Conserv 159:285–291

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Jha S, Vandermeer JH (2010) Impacts of coffee agroforestry management on tropical bee communities. Biol Conserv 143:1423–1431

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C et al (2007) Importance of pollinators in changing landscapes for world crops. Proc Roy Soc B Biol Sci 274:303–313

    Article  Google Scholar 

  • Labouisse JP, Bellachew B, Kotech S, Bertrand B (2008) Current status of coffee (Coffea arabica L.) genetic resources in Ethiopia: implication for conservation. Genet Res Crop Evol 55:1079–1093

    Article  Google Scholar 

  • Martins DJ (2007) Coffee (Coffea arabica) in forest and agroforestry cultivation in Jimma, Ethiopia: global survey of good pollination practices. Food and Agriculture Organization (FAO), Rome

  • McCune B, Mefford MJ (2006) PC-ORD multivariate analysis of ecological data version 531 MjM software. Gleneden Beach, Oregon

    Google Scholar 

  • Menz MH, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD et al (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci 16:4–12

    Article  CAS  Google Scholar 

  • Meyer B, Jauker F, Steffan-Dewenter I (2009) Contrasting resource-dependent responses of hoverfly richness and density to landscape structure. Basic Appl Ecol 10:178–186

    Article  Google Scholar 

  • Montero-Castano A, Vila M (2012) Impact of landscape alteration and invasions on pollinators: a meta-analysis. J Ecol 100:884–893

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  Google Scholar 

  • O’Brien T, Kinnaird M (2003) Caffeine and conservation. Science 300:587

    Article  Google Scholar 

  • Ockinger E, Smith HG (2006) Landscape composition and habitat area affects butterfly species richness in semi-natural grasslands. Oecologia 149:526–534

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Perfecto I, Vandermeer J (2008) Biodiversity conservation in tropical agroecosystems: a new conservation paradigm. Ann N Y Acad Sci 1134:173–200

    Article  Google Scholar 

  • Perfecto I, Rice RA, Greenberg R, VanderVoort ME (1996) Shade coffee: a disappearing refuge for biodiversity. Bioscience 46:598–608

    Article  Google Scholar 

  • Peters VE, Carroll CR (2012) Temporal variation in coffee flowering may influence the effects of bee species richness and abundance on coffee production. Agrofor Syst 85:95–103

    Article  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Nuemann P, Sweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  Google Scholar 

  • Rader R, Reilly J, Bartomeus I, Winfree R (2013) Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops. Global Change Biol 19:3103–3110

    Article  Google Scholar 

  • Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv Biol 18:1262–1271

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Roubik DW (2002) The value of bees to the coffee harvest. Nature 417:708

    Article  CAS  Google Scholar 

  • Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Ann Rev Entomol 56:293–312

    Article  CAS  Google Scholar 

  • Samnegard U, Hambäck PA, Nemomissa S, Hylander K (2014) Dominance of the semi-wild honeybee as coffee pollinator across a gradient of shade-tree structure in Ethiopia. J Trop Ecol 30:401–408

    Article  Google Scholar 

  • Schmitt CB, Senbeta F, Denich M, Preisinger H, Boehmer HJ (2009) Wild coffee management and plant diversity in the montane rainforest of southwestern Ethiopia. Afr J Ecol 48:78–86

    Article  Google Scholar 

  • Senbeta F, Denich M (2006) Effects of wild coffee management on species diversity in the Afromontane rainforest of Ethiopia. For Ecol Manage 232:68–74

    Article  Google Scholar 

  • Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440

    Article  Google Scholar 

  • Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–652

    Article  Google Scholar 

  • Tadesse G, Zavaleta E, Shennan C (2014) Coffee landscapes as refugia for native woody biodiversity as forest loss continues in southwest Ethiopia. Biol Conserv 169:384–391

    Article  Google Scholar 

  • Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216

    Article  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol Lett 8:857–874

    Article  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

    Article  Google Scholar 

  • Veddeler D, Olschewski R, Tscharntke T, Klein AM (2008) The contribution of non-managed social bees to coffee production: new economic insights based on farm-scale yield data. Agrofor Syst 73:109–114

    Article  Google Scholar 

  • Vergara CH, Badano EI (2009) Pollinator diversity increases fruit production in Mexican coffee plantations: the importance of rustic management systems. Agric Ecosyst Environ 129:117–123

    Article  Google Scholar 

  • Vidau C, Diogon M, Aufauvre J, Fontbonne R, Viguès B, Brunet JL et al (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6:e21550. doi:10.1371/journal.pone.0021550

    Article  CAS  Google Scholar 

  • Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen M (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076

    Article  Google Scholar 

  • Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Ann Rev Ecol Evol Systemat 42:1–22

    Article  Google Scholar 

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Acknowledgments

This research was carried out within the framework of the Institutional University Collaboration partnership between Jimma University and universities in Flanders (JU-IUC), which was funded by the University Development Cooperation of the Flemish Interuniversity Council (VLIR-UOS). We gratefully credit the landowners/farmers for their permission and guidance, and Chemeda Abdeta, Daniel Damtew, and Sabit Abadiga for their assistance during data collection, labeling, and pollinators identification. The valuable comments and suggestions of the editor in chief Rebecca A. Efroymson and four anonymous reviewers are highly appreciated. The authors received funding from the Efico Foundation/King Baudouin Foundation for putting environmental management science into practice. To date, thirty households have received bee hives and bee keeping training in an effort to diversify coffee farms, increase income, and conserve forests and ecosystem services in Ethiopia.

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Correspondence to Gezahegn Berecha.

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Berecha, G., Aerts, R., Muys, B. et al. Fragmentation and Management of Ethiopian Moist Evergreen Forest Drive Compositional Shifts of Insect Communities Visiting Wild Arabica Coffee Flowers. Environmental Management 55, 373–382 (2015). https://doi.org/10.1007/s00267-014-0393-9

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