Global pollinator declines: trends, impacts and drivers
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O. and Kunin, W. E. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25 (6). pp. 345-353. ISSN 0169-5347
Full text not archived in this repository.
To link to this article DOI: 10.1016/j.tree.2010.01.007
Pollinators are a key component of global biodiversity, providing vital ecosystem services to crops and wild plants. There is clear evidence of recent declines in both wild and domesticated pollinators, and parallel declines in the plants that rely upon them. Here we describe the nature and extent of reported declines, and review the potential drivers of pollinator loss, including habitat loss and fragmentation, agrochemicals, pathogens, alien species, climate change and the interactions between them. Pollinator declines can result in loss of pollination services which have important negative ecological and economic impacts that could significantly affect themaintenance of wild plant diversity, wider ecosystemstability, crop production, food security and human welfare.
● Ashman, T.L. et al. (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421 ● Aguilar, R. et al. (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol. Lett. 9, 968–980 ● Klein, A.M. et al. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. London B. Biol. Sci. 274, 303–313 ● Ricketts, T.H. et al. (2008) Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11, 499–515 ● Ghazoul, J. (2005) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol. Evol. 20, 367–373 ● Natural Research Council (2006) Status of Pollinators in North America, National Academic Press ● vanEngelsdorp, D. et al. (2008) A survey of honey bee colony losses in the U.S., Fall 2007 to Spring 2008. PLoS ONE 3, e4071. DOI:10.1371/ journal.pone.0004071 ● Potts, S.G. et al. (2010) Declines of managed honeybees and beekeepers in Europe? J. Apic. Res. 49, 15–22 ● Sammataro, D. et al. (2000) Parasitic mites of honey bees: life history, implications, and impact. Annu. Rev. Entomol. 45, 519–548 ● Kraus, B. and Page, R.E. (1995) Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral Apis mellifera (Hymenoptera: Apidae) in California. Environ. Entomol. 24, 1473–1480 ● Moritz, R.F.A. et al. (2007) The size of wild honeybee populations (Apis mellifera) and its implications for the conservation of honeybees. J. Insect Conserv. 11, 391–397 ● Jaffe´e, R. et al. (2010) Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conserv. Biol. 24, 583–593 ● Aizen, M.A. and Harder, L.D. (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19, 1–4 ● Rasmont, P. and Mersch, P. (1988) Premie`re estimation de la derive faunique chez les bourdons de la Belgique (Hymenoptera, Apidae). Ann. Soc. R. Zool. Belg 118, 141–147 ● Goulson, D. et al. (2008) Decline and conservation of bumble bees. Annu. Rev. Entomol. 53, 191–208 ● Williams, P.H. and Osborne, J.L. (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40, 367–387 ● Settele, J. et al. (2008). Climatic risk atlas of European butterflies. BioRisk 1, 1–710, DOI:10.3897/biorisk.1 ● Biesmeijer, J.C. et al. (2006) Parallel declines in pollinators and insectpollinated plants in Britain and the Netherlands. Science 313, 351–354 ● Kremen, C. et al. (2002) Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. U. S. A. 99, 16812– 16816 ● Larsen, T.H. et al. (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol. Lett. 8, 538–547 ● Winfree, R. et al. (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076 ● Kleijn, D. and Raemakers, I. (2008) A retrospective analysis of pollen host plant use by stable and declining bumblebee species. Ecology 89, 1811–1823 ● Burd, M. (1994) Bateman principle and reproduction-the role of pollen limitation in fruit and seed set. Bot. Rev. 60, 83–139 ● Fontaine, C. et al. (2006) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biol. 4, e1 DOI:10.1371/journal.pbio.0040001 ● Hegland, S.J. and Totland, Ø. (2008) Is the magnitude of pollen limitation in a plant community affected by pollinator visitation and plant species specialisation levels? Oikos 117, 883–891 ● Bond, W.J. (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Proc. R. Soc. Lond. B Biol. Sci. 344, 83–90 ● Bascompte, J. et al. (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431–433 ● Bascompte, J. et al. (2003) The nested assembly of plant animal mutualistic networks. Proc. Natl. Acad. Sci. U. S. A. 100, 9383–9387 ● Memmott, J. et al. (2004) Tolerance of pollination networks to species extinctions. Proc. R. Soc. Lond. B Biol. Sci. 271, 2605–2611 ● Fortuna,M.A. and Bascompte, J. (2006) Habitat loss and the structure of plant–animal mutualistic networks. Ecol. Lett. 9, 278–283 ● Le Conte, Y. and Navajas, M. (2008) Climate change: impact on honey bee populations and diseases. Rev. Sci. Tech. Off. Int. Epizoot. 27, 499– 510 ● Tylianakis, J.M. et al. (2008) Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 ● Aizen, M.A. et al. (2008) Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18, 1–4 ● Garibaldi, L.A. et al. (2009) Pollinator shortage and global crop yield - Looking at the whole spectrum of pollinator dependency. Commun. Integr. Biol. 2, 37–39 ● Losey, J.E. and Vaughan, M. (2006) The economic value of ecological services provided by Insects. BioScience 311–323 ● Hoehn, P. et al. (2008) Functional group diversity of bee pollinators increases crop yield. Proc. R. Soc. Lond. B Biol. Sci. 275, 2283–2291 ● Winfree, R. and Kremen, C. (2009) Are ecosystem services stabilized by differences among species? A test using crop pollination. Proc. R. Soc. Lond. B Biol. Sci. 276, 229–237 ● Gallai, N. et al. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 ● Didham, R.K. et al. (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol. Evol. 22, 489–496 ● Oldroyd, B.P. (2007) What’s killing American honey bees? Plos Biol. 5, 1195–1199 ● Schweiger, O. et al. Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol. Rev. DOI:10.1111/j.1469-185X.2010.00125.x ● Steffan-Dewenter, I. et al. (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83, 1421–1432 ● Hendrickx, F. et al. (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J. Appl. Ecol. 44, 340–351 ● Kevan, P.G. et al. (1997) Log-normality of biodiversity and abundance in diagnosis and measuring of ecosystemic health: pesticide stress on pollinators on blueberry heaths. J. Appl. Ecol. 34, 1122–1136 ● Rortais, A. et al. (2005) Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36, 71–83 ● Thomson, D.M. (2006) Detecting the effects of introduced species: a case study of competition between. Apis and Bombus. Oikos 114, 407– 418 ● Stout, J. and Morales, C.L. (2009) Ecological impacts of invasive alien species on bees. Apidologie 40, 388–409 ● Cox-Foster, D.L. et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287 ● Neumann, P. and Carreck, C. (2010) Honey bee colony losses: a global perspective. J. Apic. Res. 49, 1–6 ● Williams, P.H. et al. (2007) Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth? Biol. Conserv. 138, 493–505 ● Dormann, C.F. et al. (2008) Prediction uncertainty of environmental change effects on temperate European biodiversity. Ecol. Lett. 11, 235– 244 ● Brown, M.J.F. and Paxton, R.J. (2009) The conservation of bees: a global perspective. Apidologie 40, 410–416 ● Cane, J.H. et al. (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol. Appl. 16, 632–644 ● Carre´, G. et al. (2009) Landscape context and habitat type as drivers of bee diversity in European annual crops. Agric. Ecosyst. Environ. 133, 40–47 ● Winfree, R. et al. (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv. Biol. 21, 213–223 ● Winfree, R. et al. (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 ● Steffan-Dewenter, I. et al. (2006) Bee diversity and plant-pollinator interactions in fragmented landscapes. In Specialization and Generalization in Plant-Pollinator Interactions (Waser, N.M. and Ollerton, J., eds), pp. 387–410, University of Chicago Press ● Brosi, B.J. et al. (2008) The effects of forest fragmentation on bee communities in tropical countryside. J. Appl. Ecol. 45, 773–783 ● Donaldson, J. et al. (2002) Effects of habitat fragmentation on pollinator diversity and plant reproductive success in renosterveld shrublands of South Africa. Conserv. Biol. 16, 1267–1276 ● Tscharntke, T. et al. (2002) Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecol. Appl. 12, 354–363 ● Westrich, P. (1996)Habitat requirements of central European bees and the problems of partial habitats. In The Conservation of Bees (Matheson, A., et al. eds), pp 1–16, Academic Press ● Pauw, A. (2007) Collapse of a pollination web in small conservation areas. Ecology 88, 1759–1769 ● Kremen, C. et al. (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land use change. Ecol. Lett. 10, 219–314 ● Alston, D.G. et al. (2007) Effects of the insecticide Phosmet on solitary bee foraging and nesting in orchards of Capitol Reef National Park, Utah. Environ. Entomol. 36, 811–816 ● Brittain, C.A. et al. (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl. Ecol. 11, 106–115 ● Gabriel, D. and Tscharntke, T. (2007) Insect pollinated plants benefit from organic farming. Agric. Ecosyst. Environ. 118, 43–48 ● Holzschuh, A. et al. (2008) Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 117, 354–361 ● Thompson, H.M. and Hunt, L.V. (1999) Extrapolating from honeybees to bumblebees in pesticide risk assessment. Ecotoxicology 8, 147– 166 ● Morandin, L.A. et al. (2005) Lethal and sub-lethal effects of spinosad on bumble bees (Bombus impatiens Cresson). Pest Manag. Sci. 61, 619– 626 ● Lavergne, S. et al. (2006) Fingerprints of environmental change on the rare Mediterranean flora: a 115-year study. Glob. Change Biol. 12, 1466–1478 ● Carvell, C. et al. (2006) Declines in forage availability for bumblebees at a national scale. Biol. Conserv. 132, 481–489 ● Westphal, C. et al. (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol. Lett. 6, 961–965 ● Lambdon, P.W. et al. (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80, 101–149 ● Traveset, A. and Richardson, D.M. (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol. Evol. 21, 208–216 Review Trends in Ecology and Evolution Vol.25 No.6 352 ● Matsumura, C. et al. (2004) Invasion status and potential ecological impacts of an invasive alien bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) naturalized in Southern Hokkaido, Japan. Glob. Environ. Res. 8, 51–66 ● Steffan-Dewenter, I. and Tscharntke, T. (2000) Resource overlap and possible competition between honey bees and wild bees in central Europe. Oecologia 122, 288–296 ● Roubik, D.W. and Wolda, H. (2001) Do competing honey bees matter? Dynamics and abundance of native bees before and after honey bee invasion. Popul. Ecol. 43, 53–62 ● Goulson, D. and Sparrow, K. (2009) Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size. J. Insect Conserv. 13, 177–181 ● Franck, P. et al. (1998) The origin of west European subspecies of honeybees (Apis mellifera): new insights from microsatellite and mitochondrial data. Evolution 52, 1119–1134 ● Anderson, D. and East, I.J. (2008) The latest buzz about Colony Collapse Disorder. Science 319, 724–725 ● Watanabe, M.E. (2008) Colony collapse disorder: many suspects, no smoking gun. Bioscience 58, 384–388 ● Woolhouse, M.E.J. et al. (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol. Evol. 20, 238–244 ● Ribie`re, M. et al. (2008) Natural history and geographical distribution of honey bee viruses. In Virology and the Honey Bee (Aubert, M.F.A. et al., eds), pp. 15–84, European Commission ● Ongus, J.R. et al. (2004) Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol. 85, 3747–3755 ● Eyer, M. et al. (2009) Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses. Apidologie 40, 419–428 ● Genersch, E. et al. (2006) Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J. Invertebr. Pathol. 91, 61–63 ● Goulson, D. (2003) Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Syst. 34, 1–26 ● Neumann, P. and Elzen, P.J. (2004) The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): gaps in our knowledge of an invasive species. Apidologie 35, 229–247 ● Spiewok, S. and Neumann, P. (2006) Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida). Ecol. Entomol. 31, 623–628 ● Hickling, R. et al. (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob. Change Biol. 12, 450–455 ● Stone, G.N. and Willmer, P.G. (1989) Warm-up rates and body temperatures in bees - the importance of body size, thermal regime and phylogeny. J. Exp. Biol. 147, 303–328 ● Hegland, S.J. et al. (2009) How does climate warming affect plant– pollinator interactions? Ecol. Lett. 12, 184–195 ● Parmesan, C. et al. (1999) Poleward shifts in geographical ranges of butterfly species associated with regionalwarming. Nature 399, 579–583 ● Thomas, C.D. et al. (2001) Ecological and evolutionary processes at expanding range margins. Nature 411, 577–581 ● Memmott, J. et al. (2007) Global warming and the disruption of plant– pollinator interactions. Ecol. Lett. 10, 710–717 ● Schweiger, O. et al. (2008) Climate change can cause spatial mismatch of trophic interacting species. Ecology 89, 3472–3479 ● Ellis, J.D. and Munn, P.A. (2005) The worldwide health status of honey bees. Bee World 86, 88–101 ● Pilling, E.D. and Jepson, P.C. (1993) Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic. Sci. 39, 293–297 ● Chen, Y.P. and Siede, R. (2007) Honeybee viruses. Adv. Virus Res. 70, 33–80 Review Trends in Ecology and Evolution Vol.25 No.6 353