Agroforestry Systems

, Volume 85, Issue 1, pp 95–103 | Cite as

Temporal variation in coffee flowering may influence the effects of bee species richness and abundance on coffee production

  • Valerie E. PetersEmail author
  • C. Ronald Carroll


Accurately estimating the contribution of pollinators to production in crop species is important but could be challenging for species that are widely cultivated. One factor that may influence the pollinator-production relationship across regions is phenology, or the timing of recurring biological events, because crop phenology can be proximately controlled by climatic variables and phenology can affect plant reproductive success. For the economically important crop, coffee (Coffea arabica), at least three aspects of flowering phenology (onset, density and frequency) are influenced by precipitation, which varies across coffee’s cultivated range. Of these aspects of flowering phenology, flower density may particularly impact production in coffee because high-density flowering can severely limit outcrossing which is a major contributor to high yields and larger, high quality beans. We studied the C. arabica coffee plant-pollinator interaction over 3 years and across two distinct types of coffee blooms: (1) low-density, synchronous flowering and (2) high-density, synchronous (mass) flowering. Bee species richness was similar for four out of five flowering periods (9.8 ± 2.7 95% CI), but nearly tripled during one high-density flowering period (26 ± 8.6 95% CI). During low-density flowering coffee fruit set rates were varied, but when coffee flowered at high-density, initial fruit set rates remained close to 60% (the rate obtained from manual self-pollination of coffee flowers in pollination experiments). We discuss how changing precipitation patterns may alter coffee flowering phenology and the coffee plant-pollinator relationship, providing insight into how climate change may influence this interaction as well as the resultant coffee production.


Agroforestry Bees Climate Shade-coffee Phenology 



This research was supported by grants from the EarthWatch Institute. We thank all the EarthWatch volunteers and two field assistants, M. Garro Cruz and R. Rojas Herrera. We are especially grateful for the support of the individual farmers and for their hospitality, without their support and willingness to open their farms to research this study would not have been possible, O. Salazar, A. Vega, G. Lobo, R. Leiton, O. Ramirez and O. Garro.


  1. Augspurger CK (1980) Mass-flowering of a tropical shrub (Hybanthus prunifolius): influence on pollinator attraction and movement. Evolution 34:475–488CrossRefGoogle Scholar
  2. Bawa KS, Kang H, Grayum MH (2003) Relationships among time, frequency and duration of flowering in tropical rain forest trees. Am J Bot 90:877–887PubMedCrossRefGoogle Scholar
  3. Bos MM, Veddeler D, Bogdanski AK, Klein AM, Tscharntke T, Steffan-Dewenter I, Tylianakis JM (2007) Caveats to quantifying ecosystem services: fruit abortion blurs benefits from crop pollination. Ecol Appl 17:1841–1849PubMedCrossRefGoogle Scholar
  4. Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2. User’s guide and application published at:
  5. Eakin H, Tucker CM, Castellanos E (2005) Market shocks and climate variability; the coffee crisis in Mexico, Guatemala and Honduras. Mount Res Dev 25:304–309CrossRefGoogle Scholar
  6. Elliott SE, Irwin RE (2009) Effects of flowering plant density on pollinator visitation, pollen receipt, and seed production in Delphinium barbeyi (Ranunculaceae). Am J Bot 96:912–919PubMedCrossRefGoogle Scholar
  7. Ellstrand NC, Torres AM, Levin DA (1978) Density and the rate of apparent outcrossing in Helianthus annuus (Asteraceae). Syst Bot 3:403–407CrossRefGoogle Scholar
  8. Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carbalheiro LG, Chacoff NP, Dudenhoffer JH, Greenleaf SS et al (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072PubMedCrossRefGoogle Scholar
  9. Gay C, Estrada F, Conde C, Eakin H, Villers L (2006) Potential impacts of climate change on agriculture: a case of study of coffee production in Veracruz, Mexico. Clim Change 79:259–288CrossRefGoogle Scholar
  10. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  11. Grindeland JM, Sletvold N, Ims RA (2005) Effects of floral display size and plant density on pollinator visitation rate in natural population of Digitalis purpurea. Funct Ecol 19:383–390CrossRefGoogle Scholar
  12. Hegland SJ, Nielsen A, Lazaro A, Bjerknes AL, Totland O (2009) How does climate warming affect plant-pollinator interactions. Ecol Lett 12:184–195PubMedCrossRefGoogle Scholar
  13. Jha S, Vandermeer JH (2009) Contrasting bee foraging in response to resource scale and local habitat management. Oikos 118:1174–1180CrossRefGoogle Scholar
  14. Kitamoto N, Ueno S, Takenaka A, Tsumura Y, Washitani I, Ohsawa R (2006) Effect of flowering phenology on pollen flow distance and the consequences for spatial genetic structure within a population of Primula sieboldii (Primulaceae). Am J Bot 93:226–233PubMedCrossRefGoogle Scholar
  15. Klein AM, Steffan-Dewenter I, Tscharntke T (2003a) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc B 270:955–961PubMedCrossRefGoogle Scholar
  16. Klein AM, Steffan-Dewenter I, Tscharntke T (2003b) Pollination of Coffea canephora in relation to local regional agroforestry management. J Appl Ecol 40:837–845CrossRefGoogle Scholar
  17. 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 274:303–313PubMedCrossRefGoogle Scholar
  18. Klein AM, Cunningham SA, Bos M, Steffan-Dewenter I (2008) Advances in pollination ecology from tropical plantation crops. Ecology 89:935–943PubMedCrossRefGoogle Scholar
  19. Koptur S, Haber WA, Frankie GW, Baker HG (1988) Phenological studies of shrub and treelet species in tropical cloud forests of Costa Rica. J Trop Ecol 4:323–346CrossRefGoogle Scholar
  20. Levin DA, Kerster HW (1969) The dependence of bee-mediated pollen and gene dispersal upon plant density. Evolution 23:560–571CrossRefGoogle Scholar
  21. Maindonald J, Braun, WJ (2010) Data analysis and graphics using R: an example-based approach, 3rd edn. In: Cambridge series in statistical and probabilistic mathematics. Cambridge University Press, LondonGoogle Scholar
  22. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717PubMedCrossRefGoogle Scholar
  23. Michener C (2007) The bees of the world, 2nd edn. John Hopkins University Press, BaltimoreGoogle Scholar
  24. Millennium Ecosystem Assessment (2005) Ecosystems and Human Well-Being: synthesis. Island Press, Washington, DCGoogle Scholar
  25. Minckley RL, Wcislo WT, Yanega D, Buchmann SL (1994) Behavior and phenology of a specialist bee (Dieunomia) and sunflower (Helianthus) pollen availability. Ecology 75:1406–1419CrossRefGoogle Scholar
  26. NRC-USA (2007) Status of Pollinators in North America. The National Academies Press, Washington, DCGoogle Scholar
  27. Post E, Forchhammer MC, Stenseth NC, Callaghan TV (2001) The timing of life-history events in a changing climate. Proc R Soc B 268:15–23PubMedCrossRefGoogle Scholar
  28. Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv Biol 18:1262–1271CrossRefGoogle Scholar
  29. 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 11:499–515PubMedCrossRefGoogle Scholar
  30. Roubik DW (2002) The value of bees to the coffee harvest. Nature 417:708PubMedCrossRefGoogle Scholar
  31. Sakai S (2001) Phenological diversity in tropical forests. Popul Ecol 43:77–86CrossRefGoogle Scholar
  32. Schroth G, Laderach P, Dempewolf J, Philpott S, Haggar J, Eakin H, Castillejos T, Moreno JG, Pinto LS, Hernandez R, Eitzinger A, Ramirez-Villegas J (2009) Towards a climate change adaptation strategy for coffee communities and ecosystems in the Sierra Madre de Chiapas, Mexico. Mitig Adapt Strateg Glob Change 14:605–625CrossRefGoogle Scholar
  33. Stenseth NC, Mysterud A (2002) Climate, changing phenology, and other life history traits: nonlinearity and match-mismatch to the environment. PNAS 99:13379–13381PubMedCrossRefGoogle Scholar
  34. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol Lett 8:857–874CrossRefGoogle Scholar
  35. Van Rossum F, Stiers I, Van Geert A, Triest L, Hardy OJ (2011) Flourescent dye particles as pollen analogues for measuring pollen dispersal in an insect-pollinated forest herb. Oecologia 165:663–674PubMedCrossRefGoogle Scholar
  36. Van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377CrossRefGoogle Scholar
  37. Vergara CH, Badano EI (2009) Pollinator diversity increases fruit production in Mexican coffee plantations: the importance of rustic management systems. Agricult Ecosys Environ 129:117–123CrossRefGoogle Scholar
  38. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc Roy Soc B 272:2561–2569CrossRefGoogle Scholar
  39. Waddington KD (1980) Flight patterns of foraging bees relative to density of artificial flowers and distribution of nectar. Oecologia 44:199–204CrossRefGoogle Scholar
  40. Willmer PG, Stone GN (1989) Incidence of entomophilous pollination of lowland coffee (Coffea canephora); the role of leaf cutter bees in Papua New Guinea. Entomol Exp Appl 50:113–124CrossRefGoogle Scholar
  41. Wolda H (1989) Seasonal cues in tropical organisms. Rainfall? Not necessarily! Oecologia 80:437–442CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Odum School of EcologyUniversity of GeorgiaAthensUSA
  2. 2.Smithsonian Conservation Biology InstituteNational Zoological ParkWashington, DCUSA

Personalised recommendations