Abstract
Bee declines have received much attention of late, but there is considerable debate and confusion as to the extent, significance and causes of declines. In part, this reflects conflation of data for domestic honeybees, numbers of which are largely driven by economic factors, with those for wild bees, many of which have undergone marked range contractions but for the majority of which we have no good data on population size. There is no doubt that bees are subject to numerous pressures in the modern world. The abundance and diversity of flowers has declined along with availability of suitable nest sites, bees are chronically exposed to cocktails of agrochemicals, and they are simultaneously exposed to novel parasites and pathogens accidentally spread by humans. Climate change is likely to exacerbate these problems in the future, particularly for cool-climate specialists such as bumblebees. Stressors do not act in isolation; for example pesticide exposure can impair both detoxification mechanisms and immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple, interacting stressors is driving honeybee colony losses and declines of wild pollinators. Bees have a high profile and so their travails attract attention, but these same stressors undoubtedly bear upon other wild organisms, many of which are not monitored and have few champions. Those wild insects for which we do have population data (notably butterflies and moths) are overwhelmingly also in decline. We argue that bee declines are indicators of pervasive and ongoing environmental damage that is likely to impact broadly on biodiversity and the ecosystem services it provides.
Keywords: Apoidea, pollution, pathogens, pesticides, habitat loss, indicator species
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5. References
- 1.Klein A.-M., Steffan-Dewenter I., and Tscharntke T. (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc. Biol. Sci., 270, 955–961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Gallai N., Salles J.-M., Settele J., and Vaissière B.E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ., 68, 810–821. [Google Scholar]
- 3.Holden C. (2006) Report warns of looming pollination crisis in North America. Science, 314, 397. [DOI] [PubMed] [Google Scholar]
- 4.Gross M. (2008) Bee gloom deepens. Curr. Biol., 18, 1073. [Google Scholar]
- 5.Verissimo D., MacMillan D.C., Smith R.J. et al. (2014) Has climate change taken prominence over biodiversity conservation? Bioscience, 64, 625–629. [Google Scholar]
- 6.Dahlgreen W. (2014) Decline of bees seen as more serious than climate change. YouGov Surv. https://yougov.co.uk/news/2014/06/27/bees-dying-most-serious-environmental-issue/ [accessed 12 April 2016].
- 7.Breeze T.D., Bailey A.P., Balcombe K.G., and Potts S.G. (2011) Pollination services in the UK: How important are honeybees? Agric. Ecosyst. Environ., 142, 137–143. [Google Scholar]
- 8.Garibaldi L.A., Steffan-Dewenter I., Winfree R. et al. (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339, 1608–1611. [DOI] [PubMed] [Google Scholar]
- 9.Mallinger R.E., and Gratton C. (2014) Species richness of wild bees, but not the use of managed honey bees, increases fruit set of a pollinator-dependent crop. J. Appl. Ecol., 323–330. [Google Scholar]
- 10.Garibaldi L.A., Steffan-Dewenter I., Kremen C. et al. (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett., 14, 1062–1072. [DOI] [PubMed] [Google Scholar]
- 11.Garibaldi L.A., Aizen M.A., Klein A.M. et al. (2011) Global growth and stability of agricultural yield decrease with pollinator dependence. Proc. Natl. Acad. Sci. USA, 108, 5909–5914. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Potts S.G., Roberts S.P.M., Dean R. et al. (2010) Declines of managed honey bees and beekeepers in Europe. J. Apic. Res., 15–22. [Google Scholar]
- 13.National Resource Council (2007) Status of pollinators in North America. National Academies Press, Washington DC. [Google Scholar]
- 14.van Engelsdorp D., Hayes J., Underwood R.M., and Pettis J. (2008) A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS One, 3, e4071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.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, 915–918. [DOI] [PubMed] [Google Scholar]
- 16.van Engelsdorp D., Evans J.D., Saegerman C. et al. (2009) Colony collapse disorder: A descriptive study. PLoS One, 4, e6481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.The Bee Informed Partnership (2016) Colony loss 2015–2016: preliminary results. https://beeinformed.org/results/colony-loss-2015-2016-preliminary-results/ [accessed 4 July 2016].
- 18.Ghazoul J. (2015) Qualifying pollinator decline evidence. Science, 348, 981–982. [DOI] [PubMed] [Google Scholar]
- 19.Smith K.M., Loh E.H., Rostal M.K. et al. (2013) Pathogens, pests, and economics: drivers of honey bee colony declines and losses. Ecohealth, 10, 434–445. [DOI] [PubMed] [Google Scholar]
- 20.Goulson D., Lye G.C., and Darvill B. (2008) Decline and conservation of bumble bees. Annu. Rev. Entomol., 53, 191–208. [DOI] [PubMed] [Google Scholar]
- 21.Kosior A., Celary W., Olejniczak P. et al. (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx, 41, 79–88. [Google Scholar]
- 22.Williams P.H., and Osborne J.L. (2009) Bumblebee vulnerability and conservation world-wide. Apidologie, 40, 367–387. [Google Scholar]
- 23.Williams P.H., Thorp R.W., Richardson L.L., and Colla S.R. (2014) Bumble bees of North America: An identification guide. Princeton University Press, Princeton. [Google Scholar]
- 24.Carvalheiro L.G., Kunin W.E., Keil P. et al. (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol. Lett., 16, 870–878. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Biesmeijer J.C., Roberts S.P.M., Reemer M. et al. (2006) Parallel declines in pollinators and insect pollinated plants in Britain and the Netherlands. Science, 313, 351–354. [DOI] [PubMed] [Google Scholar]
- 26.Casey L.M., Rebelo H., Rotheray E., and Goulson D. (2015) Evidence for habitat and climatic specializations driving the long-term distribution trends of UK and Irish bumblebees. Divers. Distrib., 21, 864–875. [Google Scholar]
- 27.Ollerton J., Erenler H., Edwards M., and Crockett R. (2014) Pollinator declines. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science, 346, 1360–1362. [DOI] [PubMed] [Google Scholar]
- 28.Scheper J., Holzschuh A., Kuussaari M. et al. (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss–a metaanalysis. Ecol. Lett., 16, 912–920. [DOI] [PubMed] [Google Scholar]
- 29.Kleijn D., Winfree R., Bartomeus I. et al. (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat. Commun., 6, 7414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Goulson D., Nicholls E., Botías C., and Rotheray E.L. (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347, 1255957. [DOI] [PubMed] [Google Scholar]
- 31.Forup M.L., and Memmott J. (2005) The relationship between the abundance of bumblebees and honeybees in a native habitat. Ecol. Entomol., 30, 47–57. [Google Scholar]
- 32.Walther-Hellwig K., Fokul G., Frankl R. et al. (2006) Increased density of honeybee colonies affects foraging bumblebees. Apidologie, 37, 517–532. [Google Scholar]
- 33.Goulson D., and Sparrow K.R. (2008) Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size. J. Insect Conserv., 13, 177–181. [Google Scholar]
- 34.Thomson D.M. (2006) Detecting the effects of introduced species: A case study of competition between Apis and Bombus. Oikos, 114, 407–418. [Google Scholar]
- 35.Rosenkranz P., Aumeier P., and Ziegelmann B. (2010) Biology and control of Varroa destructor. J. Invertebr. Pathol., 103, 96–119. [DOI] [PubMed] [Google Scholar]
- 36.Nazzi F., Brown S.P., Annoscia D. et al. (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog., 8, e1002735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Wilfert L., Long G., Leggett H.C. et al. (2016) Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science, 351, 594–597. [DOI] [PubMed] [Google Scholar]
- 38.Goulson D., and Hughes W.O.H. (2015) Mitigating the anthropogenic spread of bee parasites to protect wild pollinators. Biol. Conserv., 191, 10–19. [Google Scholar]
- 39.Graystock P., Yates K., Darvill B., Goulson D., and Hughes W.O.H. (2013) Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. J. Invertebr. Pathol., 114, 114–119. [DOI] [PubMed] [Google Scholar]
- 40.Cameron S.A., Lozier J.D., Strange J.P. et al. (2011) Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. USA, 108, 662–667. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Meeus I., Brown M.J.F., De Graaf D.C., and Smagghe G. (2011) Effects of invasive parasites on bumble bee declines. Conserv. Biol., 25, 662–671. [DOI] [PubMed] [Google Scholar]
- 42.Schmid-Hempel R., Eckhardt M., Goulson D. et al. (2014) The invasion of southern South America by imported bumblebees and associated parasites. J. Anim. Ecol., 83, 823–837. [DOI] [PubMed] [Google Scholar]
- 43.Arbetman M.P., Meeus I., Morales C.L., Aizen M.A., and Smagghe G. (2013) Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biol. Invasions, 15, 489–494. [Google Scholar]
- 44.Ravoet J., De Smet L., Meeus I. et al. (2014) Widespread occurrence of honey bee pathogens in solitary bees. J. Invertebr. Pathol., 122, 55–58. [DOI] [PubMed] [Google Scholar]
- 45.Goulson D. (2003) Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Evol. Syst., 34, 1–26. [Google Scholar]
- 46.Sanchez-Bayo F., and Goka K. (2014) Pesticide residues and bees–a risk assessment. PLoS One, 9, e94482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Mullin C.A., Frazier M., Frazier J.L. et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One, 5, e9754. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Krupke C.H., Hunt G.J., Eitzer B.D. et al. (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One, 7, e29268. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Paradis D., Bérail G., Bonmatin J.M., and Belzunces L.P. (2014) Sensitive analytical methods for 22 relevant insecticides of 3 chemical families in honey by GC-MS/MS and LC-MS/MS. Anal. Bioanal. Chem., 406, 621–633. [DOI] [PubMed] [Google Scholar]
- 50.Chauzat A.M., Faucon J., Martel A. et al. (2006) A survey of pesticide residues in pollen loads collected by honey bees in France. J. Econ. Entomol., 99, 253–262. [DOI] [PubMed] [Google Scholar]
- 51.David A., Botías C., Abdul-Sada A. et al. (2016) Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ. Int., 88, 169–178. [DOI] [PubMed] [Google Scholar]
- 52.Pisa L.W., Amaral-Rogers V., Belzunces L.P. et al. (2014) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ. Sci. Pollut. Res. Int., 22, 1–35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Goulson D. (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol., 50, 977–987. [Google Scholar]
- 54.Tomizawa M., and Casida J.E. (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol., 45, 247–268. [DOI] [PubMed] [Google Scholar]
- 55.Botías C., David A., Horwood J. et al. (2015) Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environ. Sci. Technol., 49, 12731–12740. [DOI] [PubMed] [Google Scholar]
- 56.Suchail S., Guez D., and Belzunces L.P. (2000) Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environ. Toxicol. Chem., 19, 1901–1905. [DOI] [PubMed] [Google Scholar]
- 57.Rondeau G., Sánchez-Bayo F., Tennekes H.A. et al. (2014) Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci. Rep., 4, 5566. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Yang E.C., Chuang Y.C., Chen Y.L. et al. (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol., 101, 1743–1748. [DOI] [PubMed] [Google Scholar]
- 59.Mommaerts V., Reynders S., Boulet J. et al. (2010) Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology, 19, 207–215. [DOI] [PubMed] [Google Scholar]
- 60.Henry M., Béguin M., Requier F. et al. (2012) A common pesticide decreases foraging success and survival in honey bees. Science, 336, 348–350. [DOI] [PubMed] [Google Scholar]
- 61.Feltham H., Park K., and Goulson D. (2014) Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology, 23, 317–323. [DOI] [PubMed] [Google Scholar]
- 62.Han P., Niu C.Y., Lei C.L. et al. (2010) Quantification of toxins in a Cry1Ac + CpTI cotton cultivar and its potential effects on the honey bee Apis mellifera L. Ecotoxicology, 19, 1452–1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63.Piiroinen S., and Goulson D. (2016) Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees. Proc. Biol. Sci., 283, 20160246. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Piiroinen S., Botías C., Nicholls E., and Goulson D. (2016) No effect of low-level chronic neonicotinoid exposure on bumblebee learning and fecundity. PeerJ, 4, e1808. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Yang E.C., Chang H.C., Wu W.Y., and Chen Y.W. (2012) Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS One, 7, e49472. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Gilburn A.S., Bunnefeld N., Wilson J.M. et al. (2015) Are neonicotinoid insecticides driving declines of widespread butterflies? PeerJ, 3, e1402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 67.Kerr J.T., Pindar A., Galpern P. et al. (2015) Climate change impacts on bumblebees converge across continents. Science, 349, 177–180. [DOI] [PubMed] [Google Scholar]
- 68.Ploquin E.F., Herrera J.M., and Obeso J.R. (2013) Bumblebee community homogenization after uphill shifts in montane areas of northern Spain. Oecologia, 173, 1649–1660. [DOI] [PubMed] [Google Scholar]
- 69.Daszak P., Cunningham A.A., and Hyatt A.D. (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science, 287, 443–449. [DOI] [PubMed] [Google Scholar]
- 70.Evison S.E.F., Roberts K.E., Laurenson L. et al. (2012) Pervasiveness of parasites in pollinators. PLoS One, 7, e30641–e30641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71.Morrissey C.A., Mineau P., Devries J.H. et al. (2015) Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: A review. Environ. Int., 74, 291–303. [DOI] [PubMed] [Google Scholar]
- 72.Fox R., Brereton T.M., Asher J. et al. (2015) The State of the UK's Butterflies 2015. Butterfly Conservation and Centre for Ecology and Hydrology, Wareham. [Google Scholar]
- 73.Conrad K.F., Warren M.S., Fox R. et al. (2006) Rapid declines of common, widespread British moths provide evidence of an insect biodiversity crisis. Biol. Conserv., 132, 279–291. [Google Scholar]
- 74.Brooks D.R., Bater J.E., Clark S.J. et al. (2012) Large carabid beetle declines in a United Kingdom monitoring network increases evidence for a widespread loss in insect biodiversity. J. Appl. Ecol., 49, 1009–1019. [Google Scholar]
- 75.Van Dyck H., Van Strien A.J., Maes D., and Van Swaay C.A.M. (2009) Declines in common, widespread butterflies in a landscape under intense human use. Conserv. Biol., 23, 957–965. [DOI] [PubMed] [Google Scholar]
- 76.Van Swaay C.A.M., Nowicki P., Settele J., and Van Strien A.J. (2008) Butterfly monitoring in Europe: Methods, applications and perspectives. Biodivers. Conserv., 17, 3455–3469. [Google Scholar]
- 77.Forister M.L., Jahner J.P., Casner K.L. et al. (2011) The race is not to the swift: Long-term data reveal pervasive declines in California's low-elevation butterfly fauna. Ecology, 92, 2222–2235. [DOI] [PubMed] [Google Scholar]
- 78.Bonebrake T.C., Ponisio L.C., Boggs C.L., and Ehrlich P.R. (2010) More than just indicators: A review of tropical butterfly ecology and conservation. Biol. Conserv., 143, 1831–1841. [Google Scholar]
- 79.Koh L.P. (2007) Impacts of land use change on South-east Asian forest butterflies: a review. J. Appl. Ecol., 44, 703–713. [Google Scholar]
- 80.Pocock M.J.O., Roy H.E., Preston C.D., and Roy D.B. (2015) The Biological Records Centre: a pioneer of citizen science. Biol. J. Linn. Soc., 115, 475–493. [Google Scholar]
- 81.Dickinson J.L., Shirk J., Bonter D. et al. (2012) The current state of citizen science as a tool for ecological research and public engagement. Front. Ecol. Environ., 10, 291–297. [Google Scholar]
- 82.Silvertown J. (2009) A new dawn for citizen science. Trends Ecol. Evol., 24, 467–71. [DOI] [PubMed] [Google Scholar]
- 83.Thomas J.A., Edwards M., Simcox D.J. et al. (2015) Recent trends in UK insects that inhabit early successional stages of ecosystems. Biol. J. Linn. Soc., 115, 636–646. [Google Scholar]
- 84.Hardwick B., Kaartinen R., Koponen M., and Roslin T. (2016) A rapid assessment of a poorly known insect group. Insect Conserv. Divers., 9, 49–62. [Google Scholar]