Agroforestry Systems

, Volume 92, Issue 1, pp 117–125 | Cite as

Abundance and diversity of flower visitors on wild and cultivated cacao (Theobroma cacao L.) in Bolivia

  • Claudia Chumacero de Schawe
  • Michael Kessler
  • Isabell Hensen
  • Teja Tscharntke


Despite the economic importance of Theobroma cacao, surprisingly little is known about its pollination ecology. Ceratopogonid midges are considered to be the main pollinators, but the limited available evidence on the sexual reproduction is based almost exclusively on cultivated cacao and knowledge is nonexistent for wild populations. We documented flower visitors in wild and cultivated plants by applying glue on 2237 flowers of wild and cultivated cacao trees in Bolivia to trap floral visitors. We caught 631 insects belonging to seven orders, corresponding to a mean capture rate of 0.3 insects per flower. The most abundant and diverse insect order on both cacao types was Hymenoptera, represented mainly by small parasitoids. Hymenoptera were more abundant on wild cacao, whereas species richness was higher on cultivated cacao. The abundance and species richness of Diptera were not significantly different between wild and cultivated cacao. However, species composition and proportion of Diptera species differed between both wild and cultivated cacao. Ceratopogonidae were only represented by 13 individuals belonging to seven species. Cacao pollen was carried by only a single specimen of Encyrtidae. We were thus unable to identify actual pollinators. We found significant differences among the visitor assemblages between wild and cultivated cacao, which suggest that midges alone were probably too rare to act as main or even sole pollinators of cacao in our study region. Potential additional pollinators would be small Diptera (e.g., Chloropidae and Phoridae) and Hymenoptera (e.g., Eulophidae and Platygastridae).


Pollinator Diptera Hymenoptera Forcypomyia Midge 



The authors thank the German Science Foundation (HE 3041/17-1) for funding this project. We also thank the German Academic Exchange Service (DAAD) for the scholarship granted to CC. For assistance in the field, we thank R. Hurtado, C. Campos, and the local assistants J. Navi, C. Ibaguari, E. Amutari and W. Amutari. For insect identification, we thank G. Spinelli and P. Marino (Universidad Nacional de la Plata, Argentina), I. Vollhardt (University of Göttingen, Germany) and M. Limachi (Universidad Mayor de San Andrés, Bolivia). We also thank the National Herbarium of Bolivia (LPB) for logistic support, and the Ministerio de Desarrollo Rural y Medio Ambiente – Dirección General de Biodiversidad y Áreas Protegidas in Bolivia for research permits.


  1. Billes DJ (1941) Pollination of Theobroma cacao L. in Trinidad, BWI. Trop Agric (Trinidad) 28:151–156Google Scholar
  2. Bos MM, Steffan-Dewenter I, Tscharntke T (2007) Shade management affects fruit abortion, pathogens and insect attacks of cacao. Agric Ecosyst Environ 120:201–205CrossRefGoogle Scholar
  3. Brew AH, Boorman J (1993) Preliminary observations on the classification of Forcipomyia midges (Diptera, Ceratopogonidae) of Ghana with special reference to species involved in the pollination of cocoa (Theobroma cacao L.). Café, cacao, thé 37(2):139–144Google Scholar
  4. Brown BV (1992) Generic revision of phoridae of the Neartic region and phylogenetic classification of Phoridae, Sciadoceridae, and Ironomyiidae (Diptera, Phoridae). Mem entomol soc Can 124:3–144CrossRefGoogle Scholar
  5. Cane JH, Payne JA (1993) Regional, annual, and seasonal variation in pollinator guilds: intrinsic traits of bees (Hymenoptera: Apoidea) underlie their patterns of abundance at Vaccinium ashei (Ericaceae). Ann Entomol Soc Am 86:577–588CrossRefGoogle Scholar
  6. Cuatrecasas J (1964) Cacao and its allies: a taxonomic revision of the genus Theobroma. Contrib US Nat Herb 35(6):379–605Google Scholar
  7. de Schawe CC, Durka W, Tscharntke T, Hensen I, Kessler M (2013) Gene flow and genetic diversity in cultivated and wild cacao (Theobroma cacao L.) in Bolivia. Am J Bot 100(11):2271–2279CrossRefGoogle Scholar
  8. Entwistle PF (1972) Pests of cocoa, 1st edn. Longman, LondonGoogle Scholar
  9. Falque M, Vincent A, Vaissiere BE, Eskes AB (1995) Effect of pollination intensity on fruit and seed set in cacao (Theobroma cacao). Sex Plant Reprod 8:354–360CrossRefGoogle Scholar
  10. Groeneveld JH (2008) Cacao pollination and fruit set in differently managed agroforests in Indonesia. Master Thesis, Georg August University Göttingen, GermanyGoogle Scholar
  11. Groeneveld JH, Tscharntke T, Moser G, Clough Y (2010) Experimental evidence for stronger cacao yield limitation by pollen than by plant resources. Perspect Plant Ecol Evol Syst 12:183–191CrossRefGoogle Scholar
  12. Hanson PE, Gauld ID (eds) (1995) The hymenoptera of Costa Rica. Oxford University Press, OxfordGoogle Scholar
  13. Harland SC (1925) Studies in cacao. I. Method of pollination. Ann Appl Biol 12:403CrossRefGoogle Scholar
  14. Herrera CM (1988) Variation in mutualisms: the spatio-temporal mosaic of a pollinator assemblage. Biol J Linn Soc 35:95–125CrossRefGoogle Scholar
  15. Kandori I (2002) Diverse visitors with various pollinator importance and temporal change in the important pollinators of Geranium thunbergii (Geraniaceae). Ecol Res 17:283–294CrossRefGoogle Scholar
  16. Klein AM, Cunningham SA, Bos M, Steffan-Dewenter I (2008) Advances in pollination ecology from tropical plantation crops. Ecology 89(4):935–946CrossRefPubMedGoogle Scholar
  17. Knight R, Rogers HH (1955) Incompatibility in Theobroma cacao L. Heredity 9:69–77CrossRefGoogle Scholar
  18. Lachenaud Ph (1995) Variations in the number of beans per pod in Theobroma cacao L. in the Ivory Coast. II. Pollen germination, fruit setting and ovule development. Journal of Horticultural Science 70(1):1–6CrossRefGoogle Scholar
  19. Lanaud C, Sounigo D, Afemia YK, Paulin D, Lachenaud P, Clement D (1987) Nouvelles données sur le fonctionnement du système d´ incompatibilité du cacaoyer et ses conséquences pour la sélection. Café Cacao Thé 31(4):267–277Google Scholar
  20. Lieberei R, Reisdorf C (2007) Nutzpflanzenkunde. Thieme, StuttgartCrossRefGoogle Scholar
  21. Lucas P (1981) Etude des conditions de pollinisation du cacaoyer au Togo. Café Cacao Thé 25(2):113–120Google Scholar
  22. Mass B, Clough Y, Tscharntke T (2013) Bats and birds increase crop yield in tropical agroforestry landscapes. Ecol Lett 16(12):1480–1487CrossRefGoogle Scholar
  23. Massaux F, Tchiendji C, Misse C, Decazy B (1976) Etude du transport du pollen de cacaoyer par marquage au 32P. Café Cacao Thé 20(3):163–170Google Scholar
  24. Paulin D, Decazy B, Coulibaly N (1983) Etude des variations saisonnières des conditions de pollinisation et de fructification dans une cacaoyère. Café Cacao Thé 27(3):165–176Google Scholar
  25. Posnette AF (1950) Pollination of cacao in the Gold Coast. J Hortic Sci 25(3):155–163CrossRefGoogle Scholar
  26. Sánchez P, Morillo F, Muñoz W, Soria SJ, Marín C (2001) Las especies de Forcipomyia, Meigen (Diptera: Ceratopogonidae) polinizadoras del cacao (Theobroma cacao L.) en la Colección de la Estación Experimental del INIA-Miranda, Venezuela. Entomotropica 16(2):147–148Google Scholar
  27. Saunders LG, Bowman GF (1956). Cacao pollination in Costa RicaGoogle Scholar
  28. Soria SJ (1973) Locais do coleta e distribuição de Forcipomyia (Diptera, Ceratopogonidae) relacionadas com a floração e frutificação do cacaueiro na Bahia, Brasil. Rev Theobroma (Brasil) 3(2):41–49Google Scholar
  29. Soria SJ (1974) O papel das abelhas sem ferrão (Meliponinae) na polinização do cacaueiro na América tropical (Monografia). Rev Theobroma 5(1):12–20Google Scholar
  30. Soria SJ (1975) O papel das abelhas sem ferrão (Meliponinae) na polinização do cacaueiro na América tropical. Rev Theobroma 5:12–20Google Scholar
  31. Soria SJ, Wirth WW (1974) Identidade e caracterização taxonômica preliminar das mosquinhas Forcypomyia (Diptera, Ceratopogonidae) associadas com a polinização da cacaueiro na Bahia. Rev Theobroma (Brasil) 4(1):3–12Google Scholar
  32. Soria SJ, Wirth WW, Chapman K (1980) Insect pollination of cacao in Costa Rica. 1. Preliminary list of the ceratopogonid midges collected from flowers. Rev Theobroma (Brasil) 10(2):61–68Google Scholar
  33. Stejskal M (1969) Nectar y aroma de las flores del cacao. Oriente Agropecuario. 1(2):75–92Google Scholar
  34. Wellensiek SJ (1932) Observations on the flowering biology of cocoa. Archief Koffiecult 6:87–101Google Scholar
  35. Winder JA (1977) Field observations on Ceratopogonidae and other Diptera: Nematocera associated with cocoa flowers in Brazil. Bull Ent Res 67:57–63CrossRefGoogle Scholar
  36. Winder JA, Silva P (1972) Cacao pollination: microdiptera of cacao plantations and some of their breeding places. Bull Entomol Res 61(04):651–655CrossRefGoogle Scholar
  37. Young AM (1981) The ineffectiveness of the stingless bee Trigona jaty (Hymenoptera: apidae: Meliponinae) as a pollinator of cocoa (Theobroma cacao L.). J Appl Ecol 18:149–155CrossRefGoogle Scholar
  38. Young AM (1983) Seasonal differences in abundance and distribution of cocoa-pollinating midges in relation to flowering and fruit-set between shaded and sunny habitats of the La Lola Cocoa Farm. J Appl Ecol 20:801–831CrossRefGoogle Scholar
  39. Young AM (1986a) Habitat differences in cocoa tree flowering, fruit-set, and pollinator availability in Costa Rica. J Trop Ecol 2(2):163–186CrossRefGoogle Scholar
  40. Young AM (1986b) Distribution and abundance of Dipterian flypaper traps at Theobroma cacao L. (Sterculiaceae) flowers in Costarican cacao plantations. J Kansas Entomol Soc 59(4):580–587Google Scholar
  41. Young AM, Schaller M, Strand MA (1984) Floral nectaries and trichomas in relation to pollination in some species of Theobroma and Herrania (Sterculiaceae). Am J Bot 71:466–480CrossRefGoogle Scholar
  42. Young AM, Erickson EH Jr, Strand MA, Erickson BJ (1987) Pollination biology of Theobroma and Herrania (Sterculiaceae). 1. Floral biology. Insect Science and its Application 8(2):151–164Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Claudia Chumacero de Schawe
    • 1
  • Michael Kessler
    • 2
  • Isabell Hensen
    • 3
    • 4
  • Teja Tscharntke
    • 1
  1. 1.Agroecology, Department of Crop SciencesGeorg August University GöttingenGöttingenGermany
  2. 2.Institute of Systematic BotanyUniversity of ZurichZurichSwitzerland
  3. 3.Geobotany and Botanical Garden, Institute of BiologyMartin-Luther-University of Halle-WittenbergHalleGermany
  4. 4.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany

Personalised recommendations