Agroforestry pp 771-795 | Cite as

Pollinator Services in Coffee Agroforests of the Western Ghats

  • Smitha Krishnan
  • Kushalappa G. Cheppudira
  • Jaboury Ghazoul


Pollination services have often been associated with distance to adjoining forest fragments, but few studies have evaluated this in the context of other factors such as fragment size, agroforest characteristics and management regime. We investigated the effects of size of the forest fragment, distance from the forest and the effect of management of the agroforest (shade, shade tree density, coffee plant characteristics and extent of coffee flowering following rain- mass flowering or irrigation-localized flowering) on bee visits, pollen tube abundance and seed-set within coffee agroforests in Kodagu, south India. Three social bees accounted for almost all pollination events. Pollen tube abundance and seed set were enhanced by pollinator visitation, but distance to forest fragments did not affect bee visitation or seed set. Size of the adjoining forest fragment positively affected bee visitation (only irrigated agroforests with localized flowering) and pollen tube abundance but had no effect on seed set. Irrigation, which stimulated flowering of individual agroforests asynchronously of others, resulted in a dramatic increase in pollinator visits, reflected by higher seed set. In rain-fed agroforests, high densities of bee-pollinated co-flowering shade trees reduced bee visits and pollen tube abundance, but high-density shade trees positively affected final seed set. The lack of distance and size effects of forest fragments on coffee seed set does not necessarily mean that forest fragments do not provide pollinator services but rather that such benefits are not explicit at the scale of the study. Wild bees depend upon forest remnants for nesting, and hence to benefit from their pollination services, the conservation of such forests becomes imperative. Further, other agroforest characteristics, notably irrigation, provide alternative means of enhancing pollination and seed production. Nevertheless, agroforest shade trees benefit coffee production, despite competing for pollinators, by ameliorating harsh climatic conditions during the long fruit maturation period and support pollinators within the landscape by providing forge to the bees during coffee non-flowering season. Farmers could enhance pollination services and improve crop production most effectively by managing the time of coffee flowering through irrigation such that agroforests flower nonsynchronously across the landscape.


Co-flowering trees Coffea canephora Coffee agroforests Pollination success Pollinators 



The College of Forestry, Ponnampet, provided support throughout the study, including students who helped with fieldwork. This work would have been impossible without the cooperation of coffee planters and the assistance of field assistants, specifically, Chengappa SK, Raghunath Gowda, Shruthi J, Monappa CS, Bipin K, Veena PG, Nischit, Anil, Sannu, Krishnan, Rangegowda, Dillip, Ravikumar N, Niran B, Vijay Kumar, Shivprakash, Naveen Kumar H, Ranji N, Somesh, Richa, Lucy Rist, Charlotte, Eike LN, Khadeeja, Vidhya, Shali and Umesh. We would like to thank Dr. Raghavendra and Dr. Sathish BN for plant identifications. We thank the University of Agricultural Sciences (UAS Bangalore) and Ashoka Trust for Research in Ecology and the Environment (ATREE), Bangalore, India, for the lab facilities. This study was funded by the North-South Centre, ETH Zürich and the Professorship of Ecosystem Management, ETH Zürich.


  1. Bhagwat SA (2002) Biodiversity and conservation of a cultural landscape in the Western Ghats of India. University of Oxford, OxfordGoogle Scholar
  2. Bhagwat SA, Kushalappa CG, Williams PH, Brown ND (2005a) A landscape approach to biodiversity conservation of sacred groves in the Western Ghats of India. Conserv Biol 19:1853–1862. CrossRefGoogle Scholar
  3. Bhagwat SA, Kushalappa CG, Williams PH, Brown ND (2005b) The role of informal protected areas in maintaining biodiversity in the Western Ghats of India. Ecol Soc 10:8CrossRefGoogle Scholar
  4. Blanche KR, Ludwig JA, Cunningham SA (2006) Proximity to rainforest enhances pollination and fruit set in orchards. J Appl Ecol 43:1182–1187. CrossRefGoogle Scholar
  5. Boreux V, Krishnan S, Cheppudira KG, Ghazoul J (2013) Impact of forest fragments on bee visits and fruit set in rain-fed and irrigated coffee agro-forests. Agric Ecosyst Environ 172(Supplement C):42–48Google Scholar
  6. Boreux V, Vaast P, Madappa LP, Cheppudira KG, Garcia C, Ghazoul J (2016) Agroforestry coffee production increased by native shade trees, irrigation, and liming. Agron Sustain Dev 36(3):42Google Scholar
  7. CAFNET (2011) Connecting, enhancing and sustaining environmental services and market values of coffee agroforestry in Central America, East Africa and India. Consultative Group on International Agricultural Research (CGIAR), IndiaGoogle Scholar
  8. Chacoff NP, Aizen MA, Aschero V (2008) Proximity to forest edge does not affect crop production despite pollen limitation. Proc R Soc B Biol Sci 275:907–913. CrossRefGoogle Scholar
  9. Chazdon RL, Harvey CA, Komar O, Griffith DM, Ferguson BG, Martínez-Ramos M, Morales H, Nigh R, Soto-Pinto L, Van Breugel M, Philpott SM (2009) Beyond reserves: a research agenda for conserving biodiversity in human-modified tropical landscapes. Biotropica 41:142–153. CrossRefGoogle Scholar
  10. Connelly H, Poveda K, Loeb G (2015) Landscape simplification decreases wild bee pollination services to strawberry. Agric Ecosyst Environ 211:51–56. CrossRefGoogle Scholar
  11. Couvillon MJ, Al Toufailia H, Butterfield Thomas M, Schrell F, Ratnieks Francis LW, Schürch R (2015) Caffeinated forage tricks honeybees into increasing foraging and recruitment behaviors. Curr Biol 25:2815–2818. CrossRefPubMedGoogle Scholar
  12. DaMatta FM, Ronchi CP, Maestri M, Barros RS (2007) Ecophysiology of coffee growth and production. Braz J Plant Physiol 19:485–510CrossRefGoogle Scholar
  13. De Marco P, Coelho FM (2004) Services performed by the ecosystem: forest remnants influence agricultural cultures’ pollination and production. Biodivers Conserv 13:1245–1255CrossRefGoogle Scholar
  14. Diaz S, Fargione J, Chapin FS III, Tilman D (2006) Biodiversity loss threatens human well-being. PLoS Biol 4:e277CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dumas C, Knox RB (1983) Callose and determination of pistil viability and incompatibility. Theor Appl Genet 67:1–10CrossRefPubMedGoogle Scholar
  16. Dyer FC, Seeley TD (1991) Dance dialects and foraging range in three Asian honey bee species. Behav Ecol Sociobiol 28:227–233CrossRefGoogle Scholar
  17. Dyer FC, Seeley TD (1994) Colony migration in the tropical honey bee Apis dorsata F. (Hymenoptera: Apidae). Insect Soc 41:129–140CrossRefGoogle Scholar
  18. Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574. CrossRefPubMedGoogle Scholar
  19. Garcia C, Pascal JP (2006) Sacred forests of Kodagu: ecological value and social role. In: Cederlof G, Sivaramakrishnan K (eds) Ecological nationalisms: nature, livelihoods, and identities in South Asia. University of Washington Press, Seattle, pp 199–229Google Scholar
  20. Garcia CA, Bhagwat SA, Ghazoul J, Nath CD, Nanaya KM, Kushalappa CG, Raghuramulu Y, Nasi R, Vaast P (2010) Biodiversity conservation in agricultural landscapes: challenges and opportunities of coffee agroforests in the western Ghats, India. Conserv Biol 24:479–488. CrossRefPubMedGoogle Scholar
  21. Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhoffer JH, Greenleaf SS, Holzschuh A, Isaacs R, Krewenka K, Mandelik Y, Mayfield MM, Morandin LA, Potts SG, Ricketts TH, Szentgyorgyi H, Viana BF, Westphal C, Winfree R, Klein AM (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072. CrossRefPubMedGoogle Scholar
  22. Greenleaf SS, Kremen C (2006) Wild bee species increase tomato production and respond differently to surrounding land use in northern California. Biol Conserv 133:81–87. CrossRefGoogle Scholar
  23. Jha S, Vandermeer JH (2009) Contrasting bee foraging in response to resource scale and local habitat management. Oikos 118:1174–1180. CrossRefGoogle Scholar
  24. Jha S, Bacon CM, Philpott SM, Mendez VE, Laderach P, Rice RA (2014) Shade coffee: update on a disappearing refuge for biodiversity. Bioscience 64:416–428. CrossRefGoogle Scholar
  25. Klein AM, 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 16:1003–1014CrossRefGoogle Scholar
  26. Klein AM, Steffan-Dewenter I, Tscharntke T (2003a) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc Lond Ser B Biol Sci 270:955–961. CrossRefGoogle Scholar
  27. Klein AM, Steffan-Dewenter I, Tscharntke T (2003b) Pollination of Coffea canephora in relation to local and regional agroforestry management. J Appl Ecol 40:837–845CrossRefGoogle Scholar
  28. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274:303–313. CrossRefGoogle Scholar
  29. Krishnan S (2011) Pollinator services and coffee production in a forested landscape mosaic. ETH, ZurichGoogle Scholar
  30. 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 13:277–285CrossRefGoogle Scholar
  31. Landis DA (2017) Designing agricultural landscapes for biodiversity-based ecosystem services. Basic Appl Ecol 18:1–12. CrossRefGoogle Scholar
  32. Lashermes P, Couturon E, Moreau N, Paillard M, Louarn J (1996) Inheritance and genetic mapping of self-incompatibility in Coffea canephora Pierre. Theor Appl Genet 93:458–462CrossRefPubMedGoogle Scholar
  33. Lemmon PE (1956) A spherical densiometer for estimating forest overstory density. For Sci 2:314–320Google Scholar
  34. Lin B (2009) Coffee (Coffea arabica var. Bourbon) fruit growth and development under varying shade levels in the Soconusco region of Chiapas, Mexico. J Sustain Agric 33:51–65. CrossRefGoogle Scholar
  35. Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Biotech Histochem 34:125–128. Google Scholar
  36. Millennium Ecosystem Assessment (MEA) (2005) Ecosystems and human well-being: synthesis. Island Press, Washington, DCGoogle Scholar
  37. Ormsby AA, Bhagwat SA (2010) Sacred forests of India: a strong tradition of community-based natural resource management. Environ Conserv 37:320–326. CrossRefGoogle Scholar
  38. Quinn GP, Keough MJ (2004) Experimental design and data analysis for biologists, 3rd edn. Cambridge University press, CambridgeGoogle Scholar
  39. R Development Core Team (2016) R: a language and environment for statistical computing, 3.3.1 edn. R Foundation for Statistical Computing, ViennaGoogle Scholar
  40. Ramakrishnan PS, Chandrashekara UM, Elouard C, Guilmoto CZ, Maikhuri RK, Rao KS, Sankar S, Saxena KG (2000) Mountain biodiversity, land use dynamics and traditional ecological knowledge. UNESCO/Oxford/IBH Publishers, New DelhiGoogle Scholar
  41. Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv Biol 18:1262–1271CrossRefGoogle Scholar
  42. Ricketts TH, Daily GC, Ehrlich PR, Michener CD (2004) Economic value of tropical forest to coffee production. Proc Natl Acad Sci U S A 101:12579–12582CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515. CrossRefPubMedGoogle Scholar
  44. Roubik DW (2002) Tropical agriculture – the value of bees to the coffee harvest. Nature 417:708–708CrossRefPubMedGoogle Scholar
  45. Tambat B, Rajanikanth G, Ravikanth G, Shaanker RU, Ganeshaiah KN, Kushalappa CG (2005) Seedling mortality in two vulnerable tree species in the sacred groves of western Ghats, South India. Curr Sci 88:350–352Google Scholar
  46. Veddeler D, Klein A-M, Tscharntke T (2006) Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos 112:594–601. CrossRefGoogle Scholar
  47. 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. CrossRefGoogle Scholar
  48. Wille A (1983) Biology of the stingelss bees. Annu Rev Entomol 28:41–64CrossRefGoogle Scholar
  49. Winfree R, Williams NM, Gaines H, Ascher JS, Kremen C (2008) Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. J Appl Ecol 45:793–802. CrossRefGoogle Scholar
  50. Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, Borland AM, Stevenson PC (2013) Caffeine in floral nectar enhances a Pollinator’s memory of reward. Science 339:1202–1204. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Smitha Krishnan
    • 1
  • Kushalappa G. Cheppudira
    • 2
  • Jaboury Ghazoul
    • 1
  1. 1.Institute of Terrestrial Ecosystems, Department of Environmental SciencesETH ZürichZurichSwitzerland
  2. 2.College of ForestryUniversity of Agricultural and Horticultural SciencesPonnampetIndia

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