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Intensification of Ethiopian coffee agroforestry drives impoverishment of the Arabica coffee flower visiting bee and fly communities

  • L. Geeraert
  • R. Aerts
  • K. Jordaens
  • I. Dox
  • S. Wellens
  • M. Couri
  • G. Berecha
  • O. Honnay
Article

Abstract

Intensively managed shade coffee plantations are expanding in SW Ethiopia, at the cost of the more natural coffee agroforestry systems. Here, we investigated consequences for the potential pollinator community of Arabica coffee (Coffea arabica L.) in its natural range. We surveyed coffee flower visitors at six different sites in the Jimma region in SW Ethiopia, and compared species richness and abundance between semi-natural coffee forests and shaded coffee plantations. Overall, we found six bee (Hymenoptera: Anthophila) and twenty fly species (Diptera: Brachycera) visiting C. arabica flowers. Species richness and overall abundance of flower visitors was significantly higher in the semi-natural forests compared to the plantations. A significantly higher abundance of non-Apis bees and hoverflies (Syrphidae) visiting C. arabica flowers was observed in the semi-natural forest plots, but numbers for other Diptera and honeybees (Apis mellifera L.) did not differ significantly between the agroforestry systems. Our results show an impoverishment of the coffee flower visiting insect community in response to agricultural intensification. This suggests a functional shift of the coffee pollinator community and, hence, may influence the stability of the provided pollination ecosystem services and coffee yield in the long term. We did, however, not quantify pollination services in this study.

Keywords

Coffea arabica Anthophila Brachycera Flower visitors Moist Afromontane forest 

Notes

Acknowledgements

This research was financially supported by the Flemish Interuniversity Council (VLIR-UOS) and by the Flemish Fund for Scientific Research (FWO) (Project G.0565.17). We gratefully thank Daniel Damtew, Research Assistant at Jimma University, for his high-level field expertise and translation skills during data collection. We are also very thankful to Gerba Daba, Bemhiretu Boka, and Dr. Debissa Lemessa for their logistical help, to Yalew and Kasu for their hospitality and extra field support, and to Horizon Plantations P.L.C. for permission to access the coffee plantations. We gratefully acknowledge Alain Pauly (Royal Belgian Institute of Natural Sciences) for the species-level identifications of the Anthophila (Hymenoptera: Anthophila). This study benefited from the comments and suggestions of three anonymous reviewers. There are no disputes over the ownership of the data presented in the paper. All authors approved the final manuscript and agreed to be accountable for all aspects of the work.

Author’s contribution

OH, RA, KJ, GB and LG conceived and designed the study; LG and SW collected field data and exported insects to Belgium with permission of the Ethiopian Biodiversity Institute (Reference number: EBI71/5065/2016); LG, OH, RA, and ID performed the statistical analysis; LG prepared the initial draft of the manuscript. LG and ID prepared the insect specimens for identification. KJ identified all Brachycera (Diptera: Brachycera) to family level, and identified the Syrphidae, Calliphoridae, Rhiniidae, and Sarcophagidae to species level; MC identified the Muscidae to species level. All authors contributed to interpretation of research data, to preparing, discussing and editing of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aerts R, Hundera K, Berecha G, Gijbels P, Baeten M, Van Mechelen M, Hermy M, Muys B, Honnay O (2011) Semi-forest coffee cultivation and the conservation of Ethiopian Afromontane rainforest fragments. For Ecol Manag 261:1034–1041.  https://doi.org/10.1016/j.foreco.2010.12.025 CrossRefGoogle Scholar
  2. Aerts R, Berecha G, Gijbels P, Hundera K, Van Glabeke S, Vandepitte K, Muys B, Roldán-Ruiz I, Honnay O (2013) Genetic variation and risks of introgression in the wild Coffea arabica gene pool in south-western Ethiopian montane rainforests. Evol Appl 6(2):243–252.  https://doi.org/10.1111/j.1752-4571.2012.00285.x CrossRefPubMedGoogle Scholar
  3. Aerts R, Geeraert L, Berecha G, Hundera K, Muys B, De Kort H, Honnay O (2017) Conserving wild Arabica coffee: emerging threats and opportunities. Agric Ecosyst Environ 237:75–79.  https://doi.org/10.1016/j.agee.2016.12.023 CrossRefGoogle Scholar
  4. Aizen MA, Feinsinger P (1994) Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology 75:330–351.  https://doi.org/10.2307/1939538 CrossRefGoogle Scholar
  5. Albrecht M, Schmid B, Hautier Y, Müller CB (2012) Diverse pollinator communities enhance plant reproductive success. Proc R Soc B 279:4845–4852.  https://doi.org/10.1098/rspb.2012.1621 CrossRefPubMedGoogle Scholar
  6. 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.  https://doi.org/10.1007/s00122-001-0798-8 CrossRefPubMedGoogle Scholar
  7. 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.  https://doi.org/10.1111/j.1461-9563.2011.00527.x CrossRefGoogle Scholar
  8. Berecha G, Aerts R, Vandepitte K, Van Glabeke S, Muys B, Roldán-Ruiz I, Honnay O (2014) Effects of forest management on mating patterns, pollen flow and intergenerational transfer of genetic diversity in wild Arabica coffee (Coffea arabica L.) from Afromontane forests. Biol J Linn Soc 112:76–88.  https://doi.org/10.1111/bij.12274 CrossRefGoogle Scholar
  9. Berecha G, Aerts R, Muys B, Honnay O (2015) Fragmentation and management of Ethiopian moist evergreen forest drive compositional shifts of insect communities visiting wild Arabica coffee flowers. Environ Manag 55:373–382.  https://doi.org/10.1007/s00267-014-0393-9 CrossRefGoogle Scholar
  10. Blüthgen N, Klein A-M (2011) Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic Appl Ecol 12:282–291.  https://doi.org/10.1016/j.baae.2010.11.001 CrossRefGoogle Scholar
  11. Brittain C, Kremen C, Klein A-M (2013a) Biodiversity buffers pollination from changes in environmental conditions. Glob Chang Biol 19:540–547.  https://doi.org/10.1111/gcb.12043 CrossRefPubMedGoogle Scholar
  12. Brittain C, Williams N, Kremen C, Klein A-M, Brittain C (2013b) Synergistic effects of non-Apis bees and honey bees for pollination services. Proc R Soc B 280:1–7.  https://doi.org/10.1111/gcb.12043 CrossRefGoogle Scholar
  13. Cannell MGR (1985) Physiology of the coffee crop. In: Clifford MN, Willson KC (eds) Coffee: botany, biochemistry and production of beans and beverage. Springer, Berlin, pp 108–134.  https://doi.org/10.1007/978-1-4615-6657-1_5 CrossRefGoogle Scholar
  14. Davis AP, Govaerts R, Bridson DM, Stoffelen P (2006) An annotated taxonomic conspectus of the genus Coffea (Rubiaceae). Bot J Linn Soc 152:465–512.  https://doi.org/10.1111/j.1095-8339.2006.00584.x CrossRefGoogle Scholar
  15. De Beenhouwer M, Aerts R, Hundera K, Van Overtveld K, Honnay O (2015) Management intensification in Ethiopian coffee forests is associated with crown habitat contraction and loss of specialized epiphytic orchid species. Basic Appl Ecol 16:592–600.  https://doi.org/10.1016/j.baae.2015.06.006 CrossRefGoogle Scholar
  16. De Beenhouwer M, Geeraert L, Mertens J, Van Geel M, Aerts R, Vanderhaegen K, Honnay O (2016) Biodiversity and carbon storage co-benefits of coffee agroforestry across a gradient of increasing management intensity in the SW Ethiopian highlands. Agric Ecosyst Environ 222:193–199.  https://doi.org/10.1016/j.agee.2016.02.017 CrossRefGoogle Scholar
  17. Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marín M, Winn AA (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43.  https://doi.org/10.1016/j.tree.2009.06.013 CrossRefPubMedGoogle Scholar
  18. Garibaldi LA, Aizen MA, Klein A-M, Cunningham SA, Harder LD (2011) Global growth and stability of agricultural yield decrease with pollinator dependence. PNAS 108:5909–5914.  https://doi.org/10.1073/pnas.1012431108 CrossRefPubMedGoogle Scholar
  19. Garibaldi LA, Steffan-dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611.  https://doi.org/10.1126/science.1230200 CrossRefPubMedGoogle Scholar
  20. Gross M (2014) Coffee and chocolate in danger. Curr Biol 24:R503–R506.  https://doi.org/10.1016/j.cub.2014.05.035 CrossRefPubMedGoogle Scholar
  21. Heard TA (1994) Behavior and pollinator efficiency of stingless bees and honey-bees on macadamia flowers. J Apic Res 33:191–198.  https://doi.org/10.1080/00218839.1994.11100870 CrossRefGoogle Scholar
  22. Hirons M, Mehrabi Z, Gonfa TA, Morel A, Gole TW, McDermott C, Boyd E, Robinson E, Sheleme D, Malhi Y, Mason J, Norris K (2018) Pursuing climate resilient coffee in Ethiopia—a critical review. Geoforum 91:108–116.  https://doi.org/10.1016/j.geoforum.2018.02.032 CrossRefGoogle Scholar
  23. Hoehn P, Tscharntke T, Tylianakis JM, Steffan-dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proc R Soc B 275:2283–2291.  https://doi.org/10.1098/rspb.2008.0405 CrossRefPubMedGoogle Scholar
  24. Hundera K, Aerts R, Fontaine A, Van Mechelen M, Gijbels P, Honnay O, Muys B (2013) Effects of coffee management intensity on composition, structure, and regeneration status of Ethiopian moist evergreen afromontane forests. Environ Manag 51:801–809.  https://doi.org/10.1007/s00267-012-9976-5 CrossRefGoogle Scholar
  25. International Coffee Organization (ICO) (2017a) Trade statistics tables. Version 01.2017. http://www.ico.org/trade_statistics.asp?section=Statistics. Accessed 30 May 2017
  26. International Coffee Organization (ICO) (2017b) Historical data on the global coffee trade. http://www.ico.org/new_historical.asp?section=Statistics. Accessed 30 May 2017
  27. Jha S, Vandermeer JH (2010) Impacts of coffee agroforestry management on tropical bee communities. Biol Conserv 143:1423–1431.  https://doi.org/10.1016/j.biocon.2010.03.017 CrossRefGoogle Scholar
  28. Klein A-M (2009) Nearby rainforest promotes coffee pollination by increasing spatio-temporal stability in bee species richness. For Ecol Manag 258:1838–1845.  https://doi.org/10.1016/j.foreco.2009.05.005 CrossRefGoogle Scholar
  29. Klein A-M, Steffan-Dewenter I, Buchori D, Tscharntke T (2002) Effects of land-use intensity in tropical agroforestry systems on coffee flower-visiting and trap-nesting bees and wasps. Conserv Biol 16:1003–1014.  https://doi.org/10.1046/j.1523-1739.2002.00499.x CrossRefGoogle Scholar
  30. Klein A-M, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc B 270:955–961.  https://doi.org/10.1098/rspb.2002.2306 CrossRefPubMedGoogle Scholar
  31. Klein A-M, Cunningham SA, Bos M, Steffan-Dewenter I (2008) Advances in pollinator ecology from tropical plantation crops. Ecology 89:935–943.  https://doi.org/10.1890/07-0088.1 CrossRefPubMedGoogle Scholar
  32. Longino JT, Coddington J, Colwell RK (2002) The ant fauna of a tropical rain forest: estimating species richness three different ways. Ecology 83:689–702.  https://doi.org/10.1890/0012-9658(2002)083[0689:TAFOAT]2.0.CO;2 CrossRefGoogle Scholar
  33. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808.  https://doi.org/10.1126/science.1064088 CrossRefPubMedGoogle Scholar
  34. Melaku E, Ewnetu Z, Teketay D (2014) Non-timber forest products and household incomes in Bonga forest area, southwestern Ethiopia. J For Res 25:215–223CrossRefGoogle Scholar
  35. Mertens JEJ, Tropek R, Dzekashu FF, Maicher V, Fokam EB, Janeček Š (2017) Communities of flower visitors of Uvariopsis dioica (Annonaceae) in lowland forests of Mt. Cameroon, with notes on its potential pollinators. Afr J Ecol 56:146–152.  https://doi.org/10.1111/aje.12429 CrossRefGoogle Scholar
  36. Moat J, Williams J, Baena S, Wilkinson T, Gole TW, Challa ZK, Demissew S, Davis AP (2017) Resilience potential of the Ethiopian coffee sector under climate change. Nat Plants 3:17081.  https://doi.org/10.1038/nplants.2017.81 CrossRefPubMedGoogle Scholar
  37. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2016) Vegan: community ecology package. https://cran.r-project.org/package=vegan. Accessed 05 April 2017
  38. Paini DR (2004) Impact of the introduced honey bee (A. mellifera mellifera) (Hymenoptera: Apidae) on native bees: a review. Austral Ecol 29:399–407.  https://doi.org/10.1111/j.1442-9993.2004.01376.x CrossRefGoogle Scholar
  39. Peh KSH, de Jong J, Sodhi NS, Lim SLH, Yap CAM (2005) Lowland rainforest avifauna and human disturbance: persistence of primary forest birds in selectively logged forests and mixed-rural habitats of southern Peninsular Malaysia. Biol Conserv 123:489–505.  https://doi.org/10.1016/j.biocon.2005.01.010 CrossRefGoogle Scholar
  40. Priess JA, Mimler M, Klein A-M, Schwarze S, Tscharntke T, Steffan-Dewenter I (2007) Linking deforestation scenarios to pollination services and economic returns in coffee agroforestry systems. Ecol Appl 17:407–417.  https://doi.org/10.1890/05-1795 CrossRefPubMedGoogle Scholar
  41. Primack RB (1978) Variability in New Zealand montane and alpine pollinator assemblages. N Z J Ecol 1:66–73Google Scholar
  42. R Core Team (2016) R: a language and environment for statistical computing. https://www.r-project.org. Accessed 05 April 2017
  43. Rader R, Edwards W, Westcott DA, Cunningham SA, Howlett BG (2011) Pollen transport differs among bees and flies in a human-modified landscape. Divers Distrib 17:519–529.  https://doi.org/10.1111/j.1472-4642.2011.00757.x CrossRefGoogle Scholar
  44. Raw A, Free JB (1977) The pollination of coffee (Coffea arabica) by honeybees. Trop Agric 54:365–370Google Scholar
  45. Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv Biol 18:1262–1271.  https://doi.org/10.1111/j.1523-1739.2004.00227.x CrossRefGoogle Scholar
  46. Ricketts TH, Daily GC, Ehrlich PR, Michener CD (2004) Economic value of tropical forest to coffee production. PNAS 101:12579–12582.  https://doi.org/10.1073/pnas.0405147101 CrossRefPubMedGoogle Scholar
  47. Roubik DW (1980) Foraging behavior of competing africanized honeybees and stingless bees. Ecology 61:836–845.  https://doi.org/10.2307/1936754 CrossRefGoogle Scholar
  48. Roubik DW (2002) The value of bees to the coffee harvest. Nature 417:708.  https://doi.org/10.1002/(SICI)1097-0177(199909)216:1%3c1:AID-DVDY1%3e3.0.CO;2-T CrossRefPubMedGoogle Scholar
  49. Samnegård 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.  https://doi.org/10.1017/s0266467414000327 CrossRefGoogle Scholar
  50. 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.  https://doi.org/10.1111/j.1365-2028.2009.01084.x CrossRefGoogle Scholar
  51. Senbeta F, Denich M (2006) Effects of wild coffee management on species diversity in the Afromontane rainforests of Ethiopia. For Ecol Manag 232:68–74.  https://doi.org/10.1016/j.foreco.2006.05.064 CrossRefGoogle Scholar
  52. Steen R, Aase O, Thorsdatter AL (2011) Portable digital video surveillance system for monitoring flower-visiting bumblebees. J Pollinat Ecol 5:90–94Google Scholar
  53. Steffan-Dewenter I, Tscharntke T (2000) Resource overlap and possible competition between honey bees and wild bees in central Europe. Oecologia 122:288–296.  https://doi.org/10.1007/s004420050034 CrossRefPubMedGoogle Scholar
  54. Suetsugu K, Hayamizu M (2014) Moth floral visitors of the three rewarding Platanthera orchids revealed by interval photography with a digital camera. J Nat Hist 48:1103–1109.  https://doi.org/10.1080/00222933.2013.861940 CrossRefGoogle Scholar
  55. Verboven HAF, Aertsen W, Brys R, Hermy M (2014) Pollination and seed set of an obligatory outcrossing plant in an urban–peri-urban gradient. Perspect Plant Ecol Evol Syst 16:121–131.  https://doi.org/10.1016/j.ppees.2014.03.002 CrossRefGoogle Scholar
  56. 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.  https://doi.org/10.1016/j.agee.2008.08.001 CrossRefGoogle Scholar
  57. Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environ Entomol 29:413–420.  https://doi.org/10.1603/0046-225X-29.3.413 CrossRefGoogle Scholar
  58. Walker BH (1992) Biodiversity and ecological redundancy. Biol Conserv 8:18–23.  https://doi.org/10.1046/j.1523-1739.1992.610018.x CrossRefGoogle Scholar
  59. Zamir D (2014) A wake-up call with coffee. Science 345:1124.  https://doi.org/10.1126/science.1258941 CrossRefPubMedGoogle Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Plant Conservation and Population BiologyUniversity of LeuvenLeuvenBelgium
  2. 2.Division Forest, Nature and LandscapeUniversity of LeuvenLeuvenBelgium
  3. 3.Department of BiologyRoyal Museum for Central AfricaTervurenBelgium
  4. 4.Biodiversity Inventory for Conservation (BINCO)GlabbeekBelgium
  5. 5.Marine Biology Research GroupGhent UniversityGentBelgium
  6. 6.Department of Entomology, Museu NacionalFederal University of Rio de JaneiroRio de JaneiroBrazil
  7. 7.Department of Horticulture and Plant ScienceJimma UniversityJimmaEthiopia

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