Pollinators, pests, and predators: Recognizing ecological trade-offs in agroecosystems

Abstract

Ecological interactions between crops and wild animals frequently result in increases or declines in crop yield. Yet, positive and negative interactions have mostly been treated independently, owing partly to disciplinary silos in ecological and agricultural sciences. We advocate a new integrated research paradigm that explicitly recognizes cost-benefit trade-offs among animal activities and acknowledges that these activities occur within social-ecological contexts. Support for this paradigm is presented in an evidence-based conceptual model structured around five evidence statements highlighting emerging trends applicable to sustainable agriculture. The full range of benefits and costs associated with animal activities in agroecosystems cannot be quantified by focusing on single species groups, crops, or systems. Management of productive agroecosystems should sustain cycles of ecological interactions between crops and wild animals, not isolate these cycles from the system. Advancing this paradigm will therefore require integrated studies that determine net returns of animal activity in agroecosystems.

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References

  1. Abson, D.J., E.D.G. Fraser, and T.G. Benton. 2013. Landscape diversity and the resilience of agricultural returns: A portfolio analysis of land-use patterns and economic returns from lowland agriculture. Agriculture & Food Security 2: 2. doi:10.1186/2048-7010-2-2.

    Article  Google Scholar 

  2. Aizen, M.A., C.L. Morales, D.P. Vázquez, L.A. Garibaldi, A. Sáez, and L.D. Harder. 2014. When mutualism goes bad: Density-dependent impacts of introduced bees on plant reproduction. New Phytologist 204: 322–328.

    Article  Google Scholar 

  3. Altieri, M.A. 2004. Linking ecologists and traditional farmers in the search for sustainable agriculture. Frontiers in Ecology and Environment 2: 35–42.

    Article  Google Scholar 

  4. Aragona, F.B., and B. Orr. 2011. Agricultural intensification, monocultures, and economic failure: The case of onion production in the Tipajara watershed on the eastern slope of the Bolivian Andes. Journal of Sustainable Agriculture 35: 467–492.

    Article  Google Scholar 

  5. Bartomeus, I., and R. Winfree. 2011. The Circe principle: Are pollinators waylaid by attractive habitats? Current Biology 21: 652–654.

    Article  Google Scholar 

  6. Barua, M., S.A. Bhagwat, and S. Jadhav. 2013. The hidden dimensions of human-wildlife conflict: Health impacts, opportunity and transaction costs. Biological Conservation 157: 309–316.

    Article  Google Scholar 

  7. Bennett, A.J., G.D. Bending, D. Chandler, S. Hilton, and P. Mills. 2012. Meeting the demand for crop production: The challenge of yield decline in crops grown in short rotations. Biological Reviews 80: 52–71.

    Article  Google Scholar 

  8. Blitzer, E.J., C.F. Dormann, A. Holzschuh, A.-M. Klein, T.A. Rand, and T. Tscharntke. 2012. Spillover of functionally important organisms between managed and natural habitats. Agriculture, Ecosystems & Environment 146: 34–43.

    Article  Google Scholar 

  9. Bollinger, E.K., and J.W. Caslick. 1985. Factors influencing blackbird damage to field corn. The Journal of Wildlife Management 49: 1109–1115.

    Article  Google Scholar 

  10. Bommarco, R., F. Miranda, H. Bylund, and C. Björkman. 2011. Insecticides suppress natural enemies and increase pest damage in cabbage. Journal of Economic Entomology 104: 782–791.

    CAS  Article  Google Scholar 

  11. Bommarco, R., D. Kleijn, and S.G. Potts. 2013. Ecological intensification: Harnessing ecosystem services for food security. Trends in Ecology & Evolution 28: 230–238.

    Article  Google Scholar 

  12. Cardinale, B.J., C.T. Harvey, K. Gross, and A.R. Ives. 2003. Biodiversity and biocontrol: Emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecology Letters 6: 857–865.

    Article  Google Scholar 

  13. Carvalheiro, L.G., R. Veldtman, A.G. Shenkute, G.B. Tesfay, C.W.W. Pirk, J.S. Donaldson, and S.W. Nicolson. 2011. Natural and within-farmland biodiversity enhances crop productivity. Ecology Letters 14: 251–259.

    Article  Google Scholar 

  14. Cavanagh, A.F., L.S. Adler, and R.V. Hazzard. 2010. Buttercup squash provides a marketable alternative to Blue Hubbard as a trap crop for control of striped cucumber beetles (Coleoptera: Chrysomelidae). Environmental Entomology 39: 1953–1960.

    Article  Google Scholar 

  15. Chagnon, M., D. Kreutzweiser, E.A.D. Mitchell, C.A. Morrissey, D.A. Noome, and J.P. Van der Sluijs. 2015. Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environmental Science and Pollution Research 22: 119–134.

    CAS  Article  Google Scholar 

  16. Chakravarthy, A.K. 1988. Bird predators of pod borers of field bean (Lablab niger Medick). Tropical Pest Management 34: 395–398.

    Article  Google Scholar 

  17. Chamberlain, D.E., B.J. Hatchwell, and C.M. Perrins. 1999. Importance of feeding ecology to the reproductive success of Blackbirds Turdus merula nesting in rural habitats. Ibis 141: 415–427.

    Article  Google Scholar 

  18. Chaplin-Kramer, R., M.E. O’Rourke, E.J. Blitzer, and C. Kremen. 2011. A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecology Letters 14: 922–932.

    Article  Google Scholar 

  19. Classen, A., M.K. Peters, S.W. Ferger, M. Helbig-Bonitz, J.M. Schmack, G. Maassen, M. Schleuning, E.K.V. Kalko, et al. 2014. Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields. Proceedings of the Royal Society B 281: 20133148.

    Article  Google Scholar 

  20. Cunningham, S.A., S.J. Attwood, K.S. Bawa, T.G. Benton, L.M. Broadhurst, R.K. Didham, S. McIntyre, I. Perfecto, et al. 2013. To close the yield-gap while saving biodiversity will require multiple locally relevant strategies. Agriculture, Ecosystems & Environment 173: 20–27.

    Article  Google Scholar 

  21. Flynn, D.F.B., M. Gogol-Prokurat, T. Nogeire, M. Molinari, B.T. Richers, B.B. Lin, N. Simpson, M.M. Mayfield, and F. DeClerck. 2009. Loss of functional diversity under land use intensification across multiple taxa. Ecology Letters 12: 22–33.

    Article  Google Scholar 

  22. Gabarra, R., C. Castañé, and R. Albajes. 1995. The mirid bug Dicyphus tamaninii as a greenhouse whitefly and western flower thrips predator on cucumber. Biocontrol Science and Technology 5: 475–488.

    Article  Google Scholar 

  23. Gaigher, R., J.S. Pryke, and M.J. Samways. 2015. High parasitoid diversity in remnant natural vegetation, but limited spillover into the agricultural matrix in South African vineyard agroecosystems. Biological Conservation 186: 69–74.

    Article  Google Scholar 

  24. Garibaldi, L.A., I. Steffan-Dewenter, R. Winfree, M.A. Aizen, R. Bommarco, S.A. Cunningham, C. Kremen, L.G. Carvalheiro, et al. 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339: 1608–1611.

    CAS  Article  Google Scholar 

  25. Garibaldi, L.A., I. Steffan-Dewenter, C. Kremen, J.M. Morales, R. Bommarco, S.A. Cunningham, L.G. Carvalheiro, N.P. Chacoff, et al. 2011. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters 14: 1062–1072.

    Article  Google Scholar 

  26. Gebhardt, K., A.M. Anderson, K.N. Kirkpatrick, and S.A. Shwiff. 2011. A review and synthesis of bird and rodent damage estimates to select California crops. Crop Protection 30: 1109–1116.

    Article  Google Scholar 

  27. Gillespie, S., R. Long, N. Seitz, and N. Williams. 2014. Insecticide use in hybrid onion seed production affects pre- and postpollination processes. Journal of Economic Entomology 107: 29–37.

    CAS  Article  Google Scholar 

  28. Greenleaf, S.S., and C. Kremen. 2006. Wild bees enhance honey bees’ pollination of hybrid sunflower. Proceedings of the National Academy of Sciences of the United States of America 103: 13890–13895.

    CAS  Article  Google Scholar 

  29. Gurung, A.B. 2003. Insects—A mistake in God’s creation? Tharu farmers’ perception and knowledge of insects: A case study of Gobardiha Village Development Committee, Dang-Deukhuri. Nepal. Agriculture and Human Values 20: 337–370.

    Article  Google Scholar 

  30. Haaland, C., R.E. Naisbit, and L.-F. Bersier. 2011. Sown wildflower strips for insect conservation: A review. Insect Conservation and Diversity 4: 60–80.

    Article  Google Scholar 

  31. Hallmann, C.A., R.P.B. Foppen, C.A.M. van Turnhout, H. de Kroon, and E. Jongejans. 2014. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511: 341–343.

    CAS  Article  Google Scholar 

  32. Jauker, F., F. Peter, V. Wolters, and T. Diekötter. 2012. Early reproductive benefits of mass-flowering crops to the solitary bee Osmia rufa outbalance post-flowering disadvantages. Basic and Applied Ecology 13: 268–276.

    Article  Google Scholar 

  33. Keogh, R.C., Robinson, A.P.W., Mullins, I.J. 2010. Pollination aware, Case Study 24: Paterson’s Curse. Rural Industries Research and Development Corporation Canberra. RIRDC Pub. No. 10/131. URL: https://rirdc.infoservices.com.au/items/10-131.

  34. King, L.E., I. Douglas-Hamilton, and F. Vollrath. 2011. Beehive fences as effective deterrents for crop-raiding elephants: Field trials in northern Kenya. African Journal of Ecology 49: 431–439.

    Article  Google Scholar 

  35. Krupnick, G.A., A.E. Weis, and D.R. Campbell. 1999. The consequences of floral herbivory for pollinator service to Isomera arborea. Ecology 80: 125–134.

    Article  Google Scholar 

  36. Lamarque, P., P. Meyfroidt, B. Nettier, and S. Lavorel. 2014. How ecosystem services knowledge and values influence farmers’ decision-making. PLoS One 9: e107572. doi:10.1371/journal.pone.0107572.

    Article  Google Scholar 

  37. Luck, W.G. 2013. The net return from animal activity in agro-ecosystems: trading off benefits from ecosystem services against costs from crop damage. F1000 Research 2: 239. doi:10.12688/f1000research.2-239.v1.

    Google Scholar 

  38. Luck, G.W., S. Triplett, and P.G. Spooner. 2013. Bird use of almond plantations: Implications for conservation and production. Wildlife Research 40: 523–535.

    Article  Google Scholar 

  39. Lundin, O., H.G. Smith, M. Rundlöf, and R. Bommarco. 2013. When ecosystem services interact: Crop pollination benefits depend on the level of pest control. Proceedings of the Royal Society B 280: 20122243.

    Article  Google Scholar 

  40. Mackenzie, C.A., and P. Ahabyona. 2012. Elephants in the garden: Financial and social costs of crop raiding. Ecological Economics 75: 72–82.

    Article  Google Scholar 

  41. Martins, D.J., and S.D. Johnson. 2009. Distance and quality of natural habitat influence hawkmoth pollination of cultivated papaya. International Journal of Tropical Insect Science 29: 114–123.

    Article  Google Scholar 

  42. Meehan, T.D., H.M. Lease, and B.O. Wolf. 2005. Negative indirect effects of an avian insectivore on the fruit set of an insect-pollinated herb. Oikos 109: 297–304.

    Article  Google Scholar 

  43. Mothershead, K., and R.J. Marquis. 2000. Fitness impacts of herbivory through indirect effects on plant–pollinator interactions in Oenothera macrocarpa. Ecology 81: 30–40.

    Google Scholar 

  44. Murray, D.A.H., M.B. Clarke, and D.A. Ronning. 2013. Estimating invertebrate pest losses in six major Australian grain crops. Australian Journal of Entomology 52: 227–241.

    Article  Google Scholar 

  45. Nsibande, M.L. 1999. Sweet potato, Ipomoea batatas (L), cropping practices and perceived production constraints in Swaziland: Implications for pest management. International Journal of Pest Management 45: 29–33.

    Article  Google Scholar 

  46. Rader, R., B.G. Howlett, S.A. Cunningham, D.A. Westcott, and W. Edwards. 2012. Spatial and temporal variation in pollinator effectiveness: Do unmanaged insects provide consistent pollination services to mass flowering crops? Journal of Applied Ecology 49: 126–134.

    Article  Google Scholar 

  47. Rand, T.A., J.M. Tylianakis, and T. Tscharntke. 2006. Spillover edge effects: The dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecology Letters 9: 603–614.

    Article  Google Scholar 

  48. Raymond, L., J.-P. Sarthou, M. Plantegenest, B. Gauffre, S. Ladet, and A. Vialatte. 2014. Immature hoverflies overwinter in cultivated fields and may significantly control aphid populations in autumn. Agriculture, Ecosystems & Environment 185: 99–105.

    Article  Google Scholar 

  49. Rundlöf, M., G.K.S. Andersson, R. Bommarco, I. Fries, V. Hederström, L. Herbertsson, O. Jonsson, B.K. Klatt, et al. 2015. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521: 77–80.

    Article  Google Scholar 

  50. Stewart, A.M., and J.L. Craig. 1989. Factors affecting pollinator effectiveness in Feijoa sellowiana. New Zealand Journal of Crop and Horticultural Science 17: 145–154.

    Article  Google Scholar 

  51. Suttle, K.B. 2003. Pollinators as mediators of top-down effects on plants. Ecology Letters 6: 688–694.

    Article  Google Scholar 

  52. Taki, H., K. Okabe, Y. Yamaura, T. Matsuura, M. Sueyoshi, S. Makino, and K. Maeto. 2010. Effects of landscape metrics on Apis and non-Apis pollinators and seed set in common buckwheat. Basic and Applied Ecology 11: 594–602.

    Article  Google Scholar 

  53. Tracey, J., Saunders, G. 2003. Bird damage to the wine grape industry. Report to the Bureau of Rural Sciences, Department of Agriculture, Fisheries and Forestry; Canberra, Australia.

  54. Tscharntke, T., Y. Clough, T.C. Wanger, L. Jackson, I. Motzke, I. Perfecto, J. Vandermeer, and A. Whitbread. 2012. Global food security, biodiversity conservation and the future of agricultural intensification. Biological Conservation 151: 53–59.

    Article  Google Scholar 

  55. Ulluwishewa, R. 1992. Indigenous knowledge systems for sustainable development: The case of pest control by traditional paddy farmers in Sri Lanka. Vidvodaya Journal of Social Science 6: 79–88.

    Google Scholar 

  56. Valera, F., R. Martín-Hernández, and M. Higes. 2011. Evaluation of large-scale dissemination of Nosema ceranae spores by European bee-eaters Merops apiaster. Environmental Microbiology 3: 47–53.

    CAS  Article  Google Scholar 

  57. Veres, A., S. Petit, C. Conord, and C. Lavigne. 2013. Does landscape composition affect pest abundance and their control by natural enemies? A review. Agriculture, Ecosystems & Environment 166: 110–117.

    Article  Google Scholar 

  58. Watson, S.J., G.W. Luck, P.G. Spooner, and D.M. Watson. 2013. Land-use change: Incorporating the frequency, sequence, time span, and magnitude of changes into ecological research. Frontiers in Ecology and Environment 12: 241–249.

    Article  Google Scholar 

  59. Weis, T. 2010. The accelerating biophysical contradictions of industrial capitalist agriculture. Journal of Agrarian Change 10: 315–341.

    Article  Google Scholar 

  60. Wenny, D.G., T.L. DeVault, M.D. Johnson, D. Kelly, C.H. Sekercioglu, D.F. Tomback, and C.J. Whelan. 2011. The need to quantify ecosystem services provided by birds. Auk 128: 1–14.

    Article  Google Scholar 

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Acknowledgments

This research was funded by an Australian Research Council Discovery Grant DP140100709 awarded to G.W.L. All authors reviewed the literature, wrote the manuscript and approved publication. The authors have no conflicts of interest to declare. We thank three anonymous reviewers for providing helpful comments on the manuscript.

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Correspondence to Manu E. Saunders.

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Saunders, M.E., Peisley, R.K., Rader, R. et al. Pollinators, pests, and predators: Recognizing ecological trade-offs in agroecosystems. Ambio 45, 4–14 (2016). https://doi.org/10.1007/s13280-015-0696-y

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Keywords

  • Agroecology
  • Ecosystem services
  • Animal–plant interactions
  • Sustainable agriculture
  • Cost-benefit analysis