Table of Contents
ISRN Biodiversity
Volume 2014, Article ID 368953, 52 pages
http://dx.doi.org/10.1155/2014/368953
Research Article

Is Cut-Flower Industry Promotion by the Government Negatively Affecting Pollinator Biodiversity and Environmental/Human Health in Uganda?

1Academic Affairs and Research Program, Cinquantenaire University (UNIC/Lwiro), D.S. Bukavu, South-Kivu Province, Democratic Republic of Congo
2Departments of Biology and Environment, National Center for Research in Natural Sciences (CRSN/Lwiro), D.S. Bukavu, South-Kivu Province, Democratic Republic of Congo
3Centre of Research for Health Promotion (CRPS), Department of Nutrition and Dietetics, Institute of Higher Education in Medical Techniques (ISTM/Bukavu), P.O. Box 3036, Bukavu, South-Kivu Province, Democratic Republic of Congo
4Department of Natural Resources and Environmental Economics, Faculty of Natural Resources and Environmental Sciences, Namasagsali Campus, Busitema University, P.O. Box 236, Tororo, Uganda

Received 27 September 2013; Accepted 30 October 2013; Published 16 March 2014

Academic Editors: I. Bisht, H. Ford, R. Rico-Martinez, and P. K. S. Shin

Copyright © 2014 Bin Mushambanyi Théodore Munyuli. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Economic Policy Research Center (EPRC), “Integrated Assessment of Trade-Related Policies on Biological Diversity in the Agricultural Sector in Uganda. The potential impacts of the EU-ACP Economic Partnership Agreement. A case study in the horticulture sector. Ministry of Water and Environment, Republic of Uganda, National Environment Management Authority (NEMA), United Nations Environment Programme (UNEP), Kampala, Uganda,” 2009.
  2. G. Allen-Wardell, P. Bernhardt, R. Bitner et al., “The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields,” Conservation Biology, vol. 12, no. 1, pp. 8–17, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. C. D. Eardley, M. Gikungu, and M. P. Schwarz, “Bee conservation in Sub-Saharan Africa and Madagascar: diversity, status and threats,” Apidologie, vol. 40, no. 3, pp. 355–366, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Winfree, N. M. Williams, H. Gaines, J. S. Ascher, and C. Kremen, “Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA,” Journal of Applied Ecology, vol. 45, no. 3, pp. 793–802, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Neumann and N. L. Carreck, “Honey bee colony losses,” Journal of Apicultural Research, vol. 49, no. 1, pp. 1–6, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. A.-M. Klein, B. E. Vaissière, J. H. Cane et al., “Importance of pollinators in changing landscapes for world crops,” Proceedings of the Royal Society B: Biological Sciences, vol. 274, no. 1608, pp. 303–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Goulso, “Conserving wild bees for crop pollination,” Food, Agriculture & Environment, vol. 1, no. 1, pp. 142–144, 2003. View at Google Scholar
  8. O. MacIas-Macias, J. Chuc, P. Ancona-Xiu, O. Cauich, and J. J. G. Quezada-Euán, “Contribution of native bees and Africanized honey bees (Hymenoptera: Apoidea) to Solanaceae crop pollination in tropical México,” Journal of Applied Entomology, vol. 133, no. 6, pp. 456–465, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. M. G. Park, M. C. Orr, and B. N. Danforth, “The role of native bees in apple pollination,” New York Fruit Quarterly, vol. 18, no. 1, pp. 1–24, 2010. View at Google Scholar
  10. C. Kremen, N. M. Williams, M. A. Aizen et al., “Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change,” Ecology Letters, vol. 10, no. 4, pp. 299–314, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. L. A. Garibaldi, M. A. Aizen, S. A. Cunningham, and A. M. Klein, “Pollinator shortage and global crop yield,” Communicative and Integrative Biology, vol. 2, no. 1, pp. 1–3, 2009. View at Google Scholar
  12. D. R. Campbell, “Pollinator shifts and the origin and loss of plant species,” Annals of the Missouri Botanical Garden, vol. 95, no. 2, pp. 264–274, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. M. A. Aizen, L. A. Garibaldi, S. A. Cunningham, and A. M. Klein, “How much does agriculture depend on pollinators? Lessons from long-term trends in crop production,” Annals of botany, vol. 103, no. 9, pp. 1579–1588, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. A. G. S. Cuthbertson and M. A. Brown, “Issues affecting British honey bee biodiversity and the need for conservation of this important ecological component,” International Journal of Environmental Science and Technology, vol. 6, no. 4, pp. 695–699, 2009. View at Google Scholar · View at Scopus
  15. R. Winfree, “The conservation and restoration of wild bees,” Annals of the New York Academy of Sciences, vol. 1195, pp. 169–197, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Gallai, J.-M. Salles, J. Settele, and B. E. Vaissière, “Economic valuation of the vulnerability of world agriculture confronted with pollinator decline,” Ecological Economics, vol. 68, no. 3, pp. 810–821, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. M. A. Aizen and L. D. Harder, “The global stock of domesticated honey bees is growing slower than agricultural demand for pollination,” Current Biology, vol. 19, no. 11, pp. 915–918, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Kasina, M. Kraemer, C. Martius, and D. Wittmann, “Farmerś knowledge of bees and their natural history in Kakamega district, Kenya,” Journal of Apicultural Research, vol. 48, no. 2, pp. 126–133, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. M. J. F. Brown and R. J. Paxton, “The conservation of bees: a global perspective,” Apidologie, vol. 40, no. 3, pp. 410–416, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. T. M. B. Munyuli, S. G. Potts, and P. Nyeko, “Patterns of bee biodiversity and conservation values of localities with contrasting mini-ecological structures found within, nearby and between agricultural mosaic landscapes from central Uganda,” Life Sciences International Journal, vol. 2, no. 4, pp. 866–914, 2008. View at Google Scholar
  21. T. M. B. Munyuli, “The status of pollinators around flower growing zones in Uganda,” Economic policy Research Center (EPRC) and National Environmental management authority (NEMA).
  22. T. Munyuli, “Factors governing flower visitation patterns and quality of pollination services delivered by social and solitary bee species to coffee in central Uganda,” African Journal of Ecology, vol. 49, no. 4, pp. 501–509, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. T. M. B. Munyuli, “Farmers' perceptions of pollinators importance in coffee production in Uganda,” Agricultural Sciences, vol. 2, pp. 318–333, 2011. View at Google Scholar
  24. T. M. B. Munyuli, “Pollinator biodiversity in Uganda and in sub-Saharan Africa: landscape and habitat management strategies for its conservation,” International Journal of Biodiversity and Conservation, vol. 3, pp. 551–609, 2011. View at Google Scholar
  25. T. Munyuli, “Assessment of indicator species of butterfly assemblages in coffee-banana farming system in central Uganda,” African Journal of Ecology, vol. 50, no. 1, pp. 77–89, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. T. M. B. Munyuli, “Diversity of life-history traits, functional groups and indicator species of bee communities from farmlands of central Uganda,” Jordan Journal of Biological Sciences, vol. 5, pp. 1–14, 2011. View at Google Scholar
  27. T. M. B. Munyuli, “Micro, local, landscape and regional drivers of bee biodiversity and pollination services delivery to coffee (Coffea canephora) in Uganda,” International Journal of Biodiversity, Ecosystem Services and Management, vol. 8, pp. 190–203, 2012. View at Publisher · View at Google Scholar
  28. T. M. B. Munyuli, “Is pan-trapping the most reliable sampling method for measuring and monitoring bee biodiversity in agroforestry systems in sub-Saharan Africa?” International Journal of Tropical Insect Science, vol. 33, no. 1, p. 1437, 2013. View at Google Scholar
  29. T. M. B. Munyuli, P. Nyeko, S. G. Potts, P. Atkinson, D. Pomeroy, and J. Vickery, “Patterns of bee diversity in mosaic agricultural landscapes of central Uganda: implication of pollination services for conservation for food security,” Journal of Insect Conservation, vol. 17, pp. 79–93, 2013. View at Google Scholar
  30. T. M. B. Munyuli, “Climatic, regional land-use intensity, landscape, and local variables predicting best the occurrence and distribution of bee community diversity in various farmland habitats in Uganda,” Psyche, vol. 2013, Article ID 564528, 38 pages, 2013. View at Publisher · View at Google Scholar
  31. T. M. B. Munyuli, “Trends in responses to drivers by different bee ecological traits and functional groups in agricultural landscapes in Uganda,” Trends in Entomology, vol. 9, no. 9, pp. 1–23, 2013. View at Google Scholar
  32. J. C. Biesmeijer, S. P. M. Roberts, M. Reemer et al., “Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands,” Science, vol. 313, no. 5785, pp. 351–354, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. J. C. Grixti, L. T. Wong, S. A. Cameron, and C. Favret, “Decline of bumble bees (Bombus) in the North American Midwest,” Biological Conservation, vol. 142, no. 1, pp. 75–84, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Holzschuh, I. Steffan-Dewenter, and T. Tscharntke, “How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids?” Journal of Animal Ecology, vol. 79, no. 2, pp. 491–500, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. L. A. Morandin and M. L. Winston, “Wild bee abundance and seed production in conventional, organic, and genetically modified canola,” Ecological Applications, vol. 15, no. 3, pp. 871–881, 2005. View at Google Scholar · View at Scopus
  36. K. Goka, “Introduction to the special feature for ecological risk assessment of introduced bumblebees: status of the European bumblebee, Bombus terrestris, in Japan as a beneficial pollinator and an invasive alien species,” Applied Entomology and Zoology, vol. 45, no. 1, pp. 1–6, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Jaffé, V. Dietemann, M. H. Allsopp et al., “Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses,” Conservation Biology, vol. 24, no. 2, pp. 583–593, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Maini, P. Medrzycki, and C. Porrini, “The puzzle of honey bee losses: a brief review,” Bulletin of Insectology, vol. 63, no. 1, pp. 153–160, 2010. View at Google Scholar · View at Scopus
  39. S. G. Potts, J. C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger, and W. E. Kunin, “Global pollinator declines: trends, impacts and drivers,” Trends in Ecology and Evolution, vol. 25, no. 6, pp. 345–353, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. L. A. Garibaldi, I. Steffan-Dewenter, R. Winfree et al., “Wild pollinators enhance fruit set of crops worldwide, regardless of honey-bee abundance,” Science, vol. 339, no. 6127, pp. 1608–1611, 2013. View at Google Scholar
  41. V. Le Féon, A. Schermann-Legionnet, Y. Delettre et al., “Intensification of agriculture, landscape composition and wild bee communities: a large scale study in four European countries,” Agriculture, Ecosystems and Environment, vol. 137, no. 1-2, pp. 143–150, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. C. A. Brittain, M. Vighi, R. Bommarco, J. Settele, and S. G. Potts, “Impacts of a pesticide on pollinator species richness at different spatial scales,” Basic and Applied Ecology, vol. 11, no. 2, pp. 106–115, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. P. G. Kevan, “Pollinators as bioindicators of the state of the environment: species, activity and diversity,” Agriculture, Ecosystems and Environment, vol. 74, no. 1–3, pp. 373–393, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. B. A. Woodcock, S. G. Potts, T. Tscheulin et al., “Responses of invertebrate trophic level, feeding guild and body size to the management of improved grassland field margins,” Journal of Applied Ecology, vol. 46, no. 4, pp. 920–929, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. K. W. Richards and P. G. Kevan, “Aspects of bee biodiversity, crop pollination, and conservation in Canada,” in Pollinating Bees—The Conservation Link Between Agriculture and Nature, P. Kevan and V. L. Imperatriz Fonseca, Eds., pp. 77–94, Ministry of Environment-Brasília, 2002. View at Google Scholar
  46. A. E. Magurran, Measuring Biology Diversity, Blackwell, Oxford, UK, 2010.
  47. C. Porrini, A. G. Sabatini, S. Girotti et al., “The death of honey bees and environmental pollution by pesticides: the honey bees as biological indicators,” Bulletin of Insectology, vol. 56, no. 1, pp. 147–152, 2003. View at Google Scholar · View at Scopus
  48. D. Gabriel, S. M. Sait, J. A. Hodgson, U. Schmutz, W. E. Kunin, and T. G. Benton, “Scale matters: the impact of organic farming on biodiversity at different spatial scales,” Ecology Letters, vol. 13, no. 7, pp. 858–869, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. C. N. Kaiser-Bunbury, S. Muff, J. Memmott, C. B. Müller, and A. Caflisch, “The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour,” Ecology Letters, vol. 13, no. 4, pp. 442–452, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Kovács-Hostyánszki, P. Batáry, and A. Báldi, “Local and landscape effects on bee communities of Hungarian winter cereal fields,” Agricultural and Forest Entomology, vol. 13, pp. 59–66, 2011. View at Google Scholar
  51. D. Pimentel, “Environmental and economic costs of the application of pesticides primarily in the United States,” Environment, Development and Sustainability, vol. 7, no. 2, pp. 229–252, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Naidoo, L. London, A. Burdorf, R. N. Naidoo, and H. Kromhout, “Agricultural activities, pesticide use and occupational hazards among women working in small scale farming in Northern Kwazulu-Natal, South Africa,” International Journal of Occupational and Environmental Health, vol. 14, no. 3, pp. 218–224, 2008. View at Google Scholar · View at Scopus
  53. E. M. Tegtemeier and D. Duffy, “External cost of agriculture production in the United States of America,” International Journal of Agriculture Sustainability, vol. 2, no. 1, pp. 1–20, 2004. View at Google Scholar
  54. J. K. Tuell and R. Isaacs, “Community and species-specific responses of wild bees to insect pest control programs applied to a pollinator-dependent crop,” Journal of Economic Entomology, vol. 103, no. 3, pp. 668–675, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. M.-P. Chauzat, A.-C. Martel, N. Cougoule et al., “An assessment of honeybee colony matrices, Apis mellifera (Hymenoptera: Apidae) to monitor pesticide presence in continental France,” Environmental Toxicology and Chemistry, vol. 30, no. 1, pp. 103–111, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Alix and G. Lewis, “Guidance for the assessment of risks to bees from the use of plant protection products under the framework of Council Directive 91/414 and Regulation 1107/2009,” EPPO Bulletin, vol. 40, no. 2, pp. 196–203, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. D. G. Alston, V. J. Tepedino, B. A. Bradley, T. R. Toler, T. L. Griswold, and S. M. Messinger, “Effects of the insecticide phosmet on solitary bee foraging and nesting in orchards of Capitol Reef National Park, Utah,” Environmental Entomology, vol. 36, no. 4, pp. 811–816, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Kajobe, G. Marris, G. Budge et al., “First molecular detection of a viral pathogen in Ugandan honey bees,” Journal of Invertebrate Pathology, vol. 104, no. 2, pp. 153–156, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. M. M. Mekonnen, A. Y. Hoekstra, and R. Becht, “Mitigating the water footprint of export cut flowers from the lake Naivasha Basin, Kenya,” Water Resources Management, vol. 26, pp. 3725–3742, 2010. View at Google Scholar
  60. W. A. Qualls, R.-D. Xue, and H. Zhong, “Impact of bifenthrin on honeybees and Culex quinquefasciatus,” Journal of the American Mosquito Control Association, vol. 26, no. 2, pp. 223–225, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. D. Holt and A. Watson, “Exploring the dilemma of local sourcing versus international development—the case of the flower industry,” Business Strategy and the Environment, vol. 17, no. 5, pp. 318–329, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. H. van der Valk, I. Koomen, R. C. F. Nocelli et al., Aspects Determining the Risk of Pesticides to Wild Bees: Risk Profiles for Focal Crops on Three Continents, FAO, Rome, Italy, 2013.
  63. D. Van Engelsdorp, N. Speybroeck, J. D. Evans et al., “Weighing risk factors associated with bee colony collapse disorder by classification and regression tree analysis,” Journal of Economic Entomology, vol. 103, no. 5, pp. 1517–1523, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. M. N. Rashed, M. T. A. El-Haty, and S. M. Mohamed, “Bee honey as environmental indicator for pollution with heavy metals,” Toxicological and Environmental Chemistry, vol. 91, no. 3, pp. 389–403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. T. M. B. Munyuli, “Influence of functional traits on foraging behaviour and pollination efficiency of wild social and solitary bees visiting coffee (canephora) flowers in Uganda,” Grana. In press. View at Publisher · View at Google Scholar