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Decline and Conservation of Bumble Bees
Open accessAbstract
Declines in bumble bee species in the past 60 years are well documented in Europe, where they are driven primarily by habitat loss and declines in floral abundance and diversity resulting from agricultural intensification. Impacts of habitat degradation and fragmentation are likely to be compounded by the social nature of bumble bees and their largely monogamous breeding system, which renders their effective population size low. Hence, populations are susceptible to stochastic extinction events and inbreeding. In North America, catastrophic declines of some bumble bee species since the 1990s are probably attributable to the accidental introduction of a nonnative parasite from Europe, a result of global trade in domesticated bumble bee colonies used for pollination of greenhouse crops. Given the importance of bumble bees as pollinators of crops and wildflowers, steps must be taken to prevent further declines. Suggested measures include tight regulation of commercial bumble bee use and targeted use of environmentally comparable schemes to enhance floristic diversity in agricultural landscapes.
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“Current data suggest an overall pattern of decline in insect diversity and abundance.”
From More than 75 percent decline over 27 years in total flying insect biomass in protected areas (2017) · cites this paper as [8]
In the citing paper
“Data for other well-studied taxa such as bees [8–14] and moths [15–18] suggest the same trend.”
From More than 75 percent decline over 27 years in total flying insect biomass in protected areas (2017) · cites this paper as [8]
In the citing paper
“Our results demonstrate that recently reported declines in several taxa such as butterflies [7, 25–27, 58], wild bees [8–14] and moths [15–18], are in parallel with a severe loss of total aerial insect biomass, suggesting that it is not only the vulnerable species, but the flying insect community as a whole, that has been decimated over the last few decades.”
From More than 75 percent decline over 27 years in total flying insect biomass in protected areas (2017) · cites this paper as [8]
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Global pollinator declines: trends, impacts and drivers
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BackgroundInfluentialSelf-citationMore than 75 percent decline over 27 years in total flying insect biomass in protected areas
Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., et al. (2017) · PLOS ONE · doi:10.1371/journal.pone.0185809 · Cited by 3,499
Self-citationREVIEW: An overview of the environmental risks posed by neonicotinoid insecticides
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Self-citationPatterns of widespread decline in North American bumble bees
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“Population genetic factors could also play a role in Bombus population decline (8).”
BackgroundResultImproving intercropping: a synthesis of research in agronomy, plant physiology and ecology
Brooker, R. W., Bennett, A. E., Cong, W., Daniell, T. J., George, T., Hallett, P. D., Hawes, C., Iannetta, P. P. M., Jones, H. G., Karley, A. J., et al. (2014) · New Phytologist · doi:10.1111/nph.13132 · Cited by 1,498
“Globally, pests are estimated to destroy more than 30% of crop yield annually (Oerke, 2006), while declining insect pollinator abundance (Goulson et al., 2008) could limit the productivity of insect-pollinated crops worldwide (Kremen et al.”
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Wagner, D. L. (2019) · Annual Review of Entomology · doi:10.1146/annurev-ento-011019-025151 · Cited by 1,442
“In Asia, Europe, and North America, several bumblebee species have already been lost to extinction or sit near its brink (20, 21, 60, 92, 100, 179, 202).”
BackgroundA meta-analysis of bees’ responses to anthropogenic disturbance
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BackgroundSocially transmitted gut microbiota protect bumble bees against an intestinal parasite
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Baldock, K. C. R., Goddard, M. A., Hicks, D. M., Kunin, W. E., Mitschunas, N., Osgathorpe, L. M., Potts, S. G., Robertson, K. M., Scott, A., Stone, G. N., et al. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2849 · Cited by 675
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InfluentialSelf-citationWorldwide occurrence records suggest a global decline in bee species richness
Zattara, E. E., & Aizen, M. A. (2021) · One Earth · doi:10.1016/j.oneear.2020.12.005 · Cited by 705
Ecological effects of invasive alien insects
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Alaux, C., Brunet, J., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., Brillard, J., Baldy, A., Belzunces, L., & Conte, Y. L. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02123.x · Cited by 572
“Therefore, multifactorial analysis should be performed in other pollinator’ species such as bumblebees, which show similar sensitivity to pesticides as honeybees (Goulson et al., 2008), also are parasitized by N.”
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Haaland, C., Naisbit, R. E., & Bersier, L. (2010) · Insect Conservation and Diversity · doi:10.1111/j.1752-4598.2010.00098.x · Cited by 560
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BackgroundInfluentialBumblebee vulnerability and conservation world-wide
Williams, P. H., & Osborne, J. L. (2009) · Apidologie · doi:10.1051/apido/2009025 · Cited by 557
“Recently it has become possible to study genetic variation within populations of the different bumblebee species in relation to their abundances and declines (Darvill et al., 2006; Ellis et al., 2006; Goulson et al., 2008).”
BackgroundInfluentialImpacts of neonicotinoid use on long-term population changes in wild bees in England
Woodcock, B. A., Isaac, N. J. B., Bullock, J. M., Roy, D. B., Garthwaite, D. G., Crowe, A., & Pywell, R. F. (2016) · Nature Communications · doi:10.1038/ncomms12459 · Cited by 550
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Bee nutrition and floral resource restoration
Vaudo, A. D., Tooker, J. F., Grozinger, C. M., & Patch, H. M. (2015) · Current Opinion in Insect Science · doi:10.1016/j.cois.2015.05.008 · Cited by 513
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Self-citationPollinator habitat enhancement: Benefits to other ecosystem services
Wratten, S. D., Gillespie, M. A. K., Decourtye, A., Mader, E., & Desneux, N. (2012) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2012.06.020 · Cited by 544
“With these factors in mind, pollinator habitat enhancement aims to provide a diverse and continuous succession of alternative food sources that ensure the persistence of bee populations throughout the year (Pywell et al., 2005; Carvell et al., 2006; Goulson et al., 2008).”
BackgroundInfluentialKaiser‐Bunbury, C. N., Muff, S., Memmott, J., MÜLLER, C. B., & Caflisch, A. (2010) · Ecology Letters · doi:10.1111/j.1461-0248.2009.01437.x · Cited by 498
Meta-analysis of multidecadal biodiversity trends in Europe
Pilotto, F., Kühn, I., Adrian, R., Alber, R., Alignier, A., Andrews, C., Bäck, J. K., Barbaro, L., Beaumont, D. A., Beenaerts, N., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17171-y · Cited by 476
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“The main driving factors of pollinator declines [20,21] are the loss and fragmentation of (semi-)natural habitats [14,22–28] and other anthropogenic disturbances such as increasing use of pesticides [29,30], environmental pollution [31], the spread of pathogens [32], introduced species (alternative plant species, comp…”
BackgroundDecline of bumble bees (Bombus) in the North American Midwest
Grixti, J. C., Wong, L. T., Cameron, S. A., & Favret, C. (2008) · Biological Conservation · doi:10.1016/j.biocon.2008.09.027 · Cited by 466
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New frontiers in competition for pollination
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“…in pollinator populations have been reported around the globe (e.g. Buchmann and Nabhan, 1996; Biesmeijer et al., 2006; Colla and Packer, 2008; Goulson et al., 2008), and may in part be the result of climate change (Allen-Wardell, 1998; Committee on the Status of Pollinators in North America,…”
BackgroundThe conservation and restoration of wild bees
Winfree, R. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05449.x · Cited by 422
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“Land-use changes can also fragment habitats, affecting both the size and connectivity of remnant habitat patches (Hadley & Betts 2012; Hooke & Mart ın-Duque 2012).”
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“Pervasive patterns are the strong importance of local habitat quality and a shift in assemblage structure with urbanization [7,31,32,33], but the effects of urbanization on pollinator abundance and diversity have varied.”
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Landscape enhancement of floral resources for honey bees in agro-ecosystems
Decourtye, A., Mader, E., & Desneux, N. (2010) · Apidologie · doi:10.1051/apido/2010024 · Cited by 337
“The biodiversity and populations of insect pollinators are in decline (Steffan-Dewenter et al., 2005; Biesmeijer et al., 2006; Goulson et al., 2008; Freitas et al., 2009).”
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FOX, R. (2013) · Insect Conservation and Diversity · doi:10.1111/j.1752-4598.2012.00186.x · Cited by 302
“In Britain (and elsewhere in north-west Europe), moderate levels of climate warming may bring opportunities for thermally constrained species such as insects and there is strong evidence, for example, that some butterflies have already expanded their ranges and flight periods in response to climate change (Roy & Spark…”
BackgroundInfluentialChronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure
Gill, R. J., & Raıne, N. E. (2014) · Functional Ecology · doi:10.1111/1365-2435.12292 · Cited by 307
Drastic historic shifts in bumble-bee community composition in Sweden
Bommarco, R., Lundin, O., Smith, H. G., & Rundlöf, M. (2012) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2011.0647 · Cited by 304
Phenology of farmland floral resources reveals seasonal gaps in nectar availability for bumblebees
Timberlake, T. P., Vaughan, I. P., & Memmott, J. (2019) · Journal of Applied Ecology · doi:10.1111/1365-2664.13403 · Cited by 292
Climatic Risk and Distribution Atlas of European Bumblebees
Rasmont, P., Franzén, M., Lecocq, T., Harpke, A., Roberts, S. P. M., Biesmeijer, J. C., Castro, L., Cederberg, B., Dvořák, L., Fitzpatrick, Ú., et al. (2015) · BIORISK – Biodiversity and Ecosystem Risk Assessment · doi:10.3897/biorisk.10.4749 · Cited by 296
“…2012; Hatten et al., 2013), (ii) shortage of flower resources (Peters, 1972; Williams, 1989; Rasmont & Mersch, 1988; Rasmont et al., 1993, 2005; Goulson et al., 2005, 2008a), (iii) killing by car traffic (Donath, 1986), (iv) overgrazing of bumblebee habitat by cattle (Özbek, 1995; Xie et al.,…”
BackgroundField realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency
Feltham, H., Park, K. J., & Goulson, D. (2014) · Ecotoxicology · doi:10.1007/s10646-014-1189-7 · Cited by 285
“Agricultural intensification has been proposed as a primary driver behind the decline of bumblebees, with habitat loss as well as increased pesticide use believed to be two important causal factors (Goulson et al. 2008).”
BackgroundSelf-citationEcological impacts of invasive alien species on bees
Stout, J. C., & Morales, C. L. (2009) · Apidologie · doi:10.1051/apido/2009023 · Cited by 303
“Habitat change, loss and fragmentation associated with agricultural intensification are thought to pose the main risks to native bees (Kremen et al., 2002; Goulson et al., 2008; Steffan-Dewenter andWestphal, 2008; Murray et al., 2009) and the impacts of these processes on native bees have been studied on a range of sc…”
BackgroundA sting in the spit: widespread cross‐infection of multiple RNA viruses across wild and managed bees
McMahon, D. P., Fürst, M. A., Caspar, J., Theodorou, P., Brown, M. J. F., & Paxton, R. J. (2015) · Journal of Animal Ecology · doi:10.1111/1365-2656.12345 · Cited by 278
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BackgroundGlobal effects of land-use intensity on local pollinator biodiversity
Millard, J. W., Outhwaite, C. L., Kinnersley, R., Freeman, R., Gregory, R. D., Adedoja, O. A., Gavini, S. S., Kioko, E. N., Kuhlmann, M. T., Ollerton, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23228-3 · Cited by 282
The same, but different: pollen foraging in honeybee and bumblebee colonies
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“…in habitat and resource availability and diversity are considered one (albeit not the only) cause of the observed bee decline (Williams 1986; Steffan-Dewenter and Tscharntke 1999; Aizen and Feinsinger 2003; Goulson and Darvill 2004; Hines and Hendrix 2005; Goulson et al. 2008; Winfree et al. 2009).”
BackgroundEffects of Invasive Parasites on Bumble Bee Declines
Meeus, I., Brown, M. J. F., de Graaf, D. C., & Smagghe, G. J. (2011) · Conservation Biology · doi:10.1111/j.1523-1739.2011.01707.x · Cited by 265
“…bees, combined with the commercialization of bumble bees as agricultural pollinators, has led to the theory that invasive and emergent parasites may play a substantial current and future role in the decline of wild bumble bee populations (Colla et al. 2006; Winter et al. 2006; Goulson et al. 2008).”
BackgroundPardee, G. L., & Philpott, S. M. (2014) · Urban Ecosystems · doi:10.1007/s11252-014-0349-0 · Cited by 290
“For example, bee diversity increases in urban sites with abandoned rodent nests that can act as nesting sites (Goulson et al. 2008; McFrederick and LeBuhn 2006).”
BackgroundLaycock, I., Lenthall, K. M., Barratt, A. T., & Cresswell, J. (2012) · Ecotoxicology · doi:10.1007/s10646-012-0927-y · Cited by 259
“Wild and managed bees are important pollinators whose populations have declined over recent years (Goulson et al. 2008; van Engelsdorp et al. 2010; De la Rúa et al. 2009) raising widespread concern (Allen-Wardell et al. 1998; Potts et al. 2010).”
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“2005), (ii) rising worries about mass declines of their natural populations (Steffan-Dewenter et al. 2005; Williams 2005; Biesmeijer et al. 2006; Fitzpatrick et al. 2007; Colla and Packer 2008; Goulson et al. 2008), and (iii) colony collapse disorder (CCD) of Apis mellifera L.”
BackgroundStoner, K. A., & Eitzer, B. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039114 · Cited by 261
“Whitehorn et al. [33] found that Bombus terrestris (a European species of bumble bee) had an 85% reduction in queen production over the season when fed imidacloprid at concentrations of 0.7 ppb in sugar water and 6 ppb in pollen for two weeks before being placed in the field.”
BackgroundInfluentialWeiner, C. N., Werner, M., Linsenmair, K. E., & Blüthgen, N. (2013) · Ecology · doi:10.1890/13-0436.1 · Cited by 245
Landscape‐scale resources promote colony growth but not reproductive performance of bumble bees
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“Declines of bumble bees in Europe have been linked to loss of preferred forage resources in changing agricultural landscapes (Carvell et al. 2006, Goulson et al. 2008, Knight et al. 2009).”
BackgroundImpact of Chronic Neonicotinoid Exposure on Honeybee Colony Performance and Queen Supersedure
Sandrock, C., Tanadini, M., Tanadini, L. G., Fauser‐Misslin, A., Potts, S. G., & Neumann, P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103592 · Cited by 259
“Recent evidence for globally paralleling declines of various pollinators [7,8,9,10], however, stands in contrast to prospects of continuously increasing demands for pollination services [4,11,12].”
Detecting Insect Pollinator Declines on Regional and Global Scales
LeBuhn, G., Droege, S., Connor, E. F., Gemmill‐Herren, B., Potts, S. G., Minckley, R. L., Griswold, T., Jean, R. P., Kula, E., Roubik, D. W., et al. (2012) · Conservation Biology · doi:10.1111/j.1523-1739.2012.01962.x · Cited by 240
“These reports were based primarily on post hoc analyses or resurveys of study sites not originally intended to yield data that would unequivocally detect a change or trend (e.g., Rasmont & Mersch 1988; National Research Council 2007; Goulson et al. 2008).”
MethodCariveau, D. P., Powell, J. E., Koch, H., Winfree, R., & Moran, N. A. (2014) · The ISME Journal · doi:10.1038/ismej.2014.68 · Cited by 234
“Some of these population declines may result from land-use change and pathogens (Goulson et al., 2008; Grixti et al., 2009; Williams and Osborne, 2009; Cameron et al., 2011), but the mechanisms underlying the declines of some Bombus species remain unknown.”
BackgroundEcotoxicity of Neonicotinoid Insecticides to Bees
Decourtye, A., & Devillers, J. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6445-8_8 · Cited by 231
Space Use of Bumblebees (Bombus spp.) Revealed by Radio-Tracking
Hagen, M., Wikelski, M. C., & Kissling, W. D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019997 · Cited by 230
“Population declines in bumblebee species, a highly important pollinator group [7,8,9], have been attributed to a reduced availability of suitable food resources in agricultural landscapes [10,11], a reduction in nesting and hibernation sites [10,12], competition from introduced species [13], and potential pathogen spi…”
BackgroundSchaafsma, A. W., Limay‐Rios, V., Baute, T. S., Smith, J. L., & Xue, Y. (2015) · PLoS ONE · doi:10.1371/journal.pone.0118139 · Cited by 238
Grundel, R., Jean, R. P., Frohnapple, K. J., Glowacki, G. A., Scott, P. E., & Pavlovic, N. B. (2010) · Ecological Applications · doi:10.1890/08-1792.1 · Cited by 226
“For bees, such studies are not yet common (Goulson et al. 2008), especially studies that evaluate the relative effect of different environmental gradients on bee community composition (Williams et al. 2001, Potts et al. 2003b, Brosi et al. 2007, Schaffers et al. 2008).”
BackgroundThe T rojan hives: pollinator pathogens, imported and distributed in bumblebee colonies
Graystock, P., Yates, K., Evison, S. E. F., Darvill, B., Goulson, D., & Hughes, W. O. H. (2013) · Journal of Applied Ecology · doi:10.1111/1365-2664.12134 · Cited by 223
Self-citationEffects of land use at a landscape scale on bumblebee nest density and survival
Goulson, D., Lepais, O., O’Connor, S., Osborne, J. L., Sanderson, R., Cussans, J. W., Goffe, L., & Darvill, B. (2010) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2010.01872.x · Cited by 220
“…feature on arable farms since they boost soil fertility, but the advent of cheap artificial fertilizers led to their abandonment; it has been argued that this change in farming may have played a significant role in driving bumblebee declines in the twentieth century (Goulson et al. 2005, 2008a).”
BackgroundSelf-citationChronic sublethal stress causes bee colony failure
Bryden, J., Gill, R. J., Mitton, R. A. A., Raıne, N. E., & Jansen, V. A. A. (2013) · Ecology Letters · doi:10.1111/ele.12188 · Cited by 219
“Reports of social bee colony losses (Oldroyd 2007; Ratnieks & Carreck 2010) and global bee population declines (Biesmeijer et al. 2006; Goulson et al. 2008; Brown & Paxton 2009; Cameron et al. 2011) are therefore of major concern.”
Goulson, D. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511778230.025 · Cited by 218
Self-citationZayed, A. (2009) · Apidologie · doi:10.1051/apido/2009026 · Cited by 215
“Over the past decade, multiple lines of evidence have shown that both native and managed pollinators are experiencing a seemingly world-wide decline (Biesmeijer et al., 2006; Fitzpatrick et al., 2006; Kosior et al., 2007; NRC, 2007; Colla and Packer, 2008; Goulson et al., 2008; Grixti et al., 2009), fueling both ecolo…”
BackgroundStevens, C. J., David, T. I., & Storkey, J. (2018) · Functional Ecology · doi:10.1111/1365-2435.13063 · Cited by 214
The invasion of southern S outh A merica by imported bumblebees and associated parasites
Schmid‐Hempel, R., Eckhardt, M., Goulson, D., Heinzmann, D., Lange, C. E., Plischuk, S., Escudero, L. R., Salathé, R. M., Scriven, J. J., & Schmid‐Hempel, P. (2013) · Journal of Animal Ecology · doi:10.1111/1365-2656.12185 · Cited by 212
Self-citationWarming, CO 2 , and nitrogen deposition interactively affect a plant‐pollinator mutualism
Hoover, S. E., Ladley, J. J., Shchepetkina, A. A., Tisch, M., Gieseg, S. P., & Tylianakis, J. M. (2012) · Ecology Letters · doi:10.1111/j.1461-0248.2011.01729.x · Cited by 209
“Despite the importance of bumble bees as generalist pollinators, many wild populations are facing decline (Goulson et al. 2008).”
Allotment gardens and parks: Provision of ecosystem services with an emphasis on biodiversity
Speak, A. F., Mizgajski, A., & Borysiak, J. (2015) · Urban forestry & urban greening · doi:10.1016/j.ufug.2015.07.007 · Cited by 234
“Support of pollinators is increasingly important given the reported decline of pollinators such as bees, and the potentially disastrous consequences this will have upon crops (Goulson et al., 2008).”
Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success
Sandrock, C., Tanadini, L. G., Pettis, J. S., Biesmeijer, J. C., Potts, S. G., & Neumann, P. (2013) · Agricultural and Forest Entomology · doi:10.1111/afe.12041 · Cited by 221
Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants
Hanley, M. E., Franco, M., Pichon, S., Darvill, B., & Goulson, D. (2008) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01415.x · Cited by 207
“While it is impossible at present to determine whether pollinator decline results in reduced reproductive potential for obligate insect-pollinated plants, or vice versa, it is clear that both specialist pollinators and obligate zoophilous plants have declined markedly in diversity and abundance over recent decades (Go…”
BackgroundSelf-citationThe identity of crop pollinators helps target conservation for improved ecosystem services
Garratt, M. P. D., Coston, D. J., Truslove, C. L., Lappage, M. G., Polce, C., Dean, R. R., Biesmeijer, J. C., & Potts, S. G. (2013) · Biological Conservation · doi:10.1016/j.biocon.2013.11.001 · Cited by 195
“Driven by habitat loss and falling floral abundance and diversity, Europe and the US have seen significant declines in many bumblebee species (Goulson et al., 2008).”
Do managed bees drive parasite spread and emergence in wild bees?
Graystock, P., Blane, E. J., McFrederick, Q. S., Goulson, D., & Hughes, W. O. H. (2015) · International Journal for Parasitology Parasites and Wildlife · doi:10.1016/j.ijppaw.2015.10.001 · Cited by 213
Self-citationNeonicotinoids in excretion product of phloem-feeding insects kill beneficial insects
Calvo‐Agudo, M., González‐Cabrera, J., Picó, Y., Calatayud-Vernich, P., Urbaneja, A., Dicke, M., & Tena, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904298116 · Cited by 202
Pervasiveness of Parasites in Pollinators
Evison, S. E. F., Roberts, K., Laurenson, L., Pietravalle, S., Hui, J., Biesmeijer, J. C., Smith, J. E., Budge, G. E., & Hughes, W. O. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030641 · Cited by 187
“recent years [10], while North American bumblebees are also”
BackgroundPollen and nectar quality drive the major and minor floral choices of bumble bees
Somme, L., Vanderplanck, M., Michez, D., Lombaerde, I., Moerman, R., Wathelet, B., Wattiez, R., Lognay, G. C., & Jacquemart, A. (2014) · Apidologie · doi:10.1007/s13592-014-0307-0 · Cited by 180
“For decades, a decline in bumble bee populations has been documented; this decline is triggered by the fragmentation and quality shift of the bees' habitats, which might induce a floral resources shift (Carvalheiro et al. 2013; Goulson et al. 2008).”
BackgroundExperimental evidence that wildflower strips increase pollinator visits to crops
Feltham, H., Park, K. J., Minderman, J., & Goulson, D. (2015) · Ecology and Evolution · doi:10.1002/ece3.1444 · Cited by 191
“Agricultural intensification is believed to be one of the key drivers of these declines (Goulson et al. 2008), but while modern agriculture may represent a hostile environment for pollinators, the number and extent of crops requiring pollina- tion have increased.”
BackgroundSelf-citationStraub, L., Williams, G. R., Pettis, J. S., Fries, I., & Neumann, P. (2015) · Current Opinion in Insect Science · doi:10.1016/j.cois.2015.10.010 · Cited by 176
“Consequently, major declines of wild insects providing such ecosystem services, in combination with elevated losses of managed honey bees, throughout the northern hemisphere are of widespread concern [3,5].”
BackgroundA depauperate immune repertoire precedes evolution of sociality in bees
Barribeau, S. M., Sadd, B. M., du Plessis, L., Brown, M. J. F., Buechel, S. D., Cappelle, K., Carolan, J. C., Christiaens, O., Colgan, T. J., Erler, S., et al. (2015) · Genome biology · doi:10.1186/s13059-015-0628-y · Cited by 178
“Given the recent and dramatic declines in populations of important bee pollinators [22-24] and the role”
BackgroundHoneybee Colony Disorder in Crop Areas: The Role of Pesticides and Viruses
Simon‐Delso, N., Martin, G. S., Bruneau, É., Minsart, L.-A., Mouret, C., & Hautier, L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103073 · Cited by 173
“The evolution of pollinator populations has been the subject of an increasing number of studies, most of them showing worrying negative trends [1–4].”
BackgroundBumblebee Vulnerability: Common Correlates of Winners and Losers across Three Continents
Williams, P. H., Colla, S. R., & Xie, Z. (2009) · Conservation Biology · doi:10.1111/j.1523-1739.2009.01176.x · Cited by 172
Emerging dangers: Deadly effects of an emergent parasite in a new pollinator host
Graystock, P., Yates, K., Darvill, B., Goulson, D., & Hughes, W. O. H. (2013) · Journal of Invertebrate Pathology · doi:10.1016/j.jip.2013.06.005 · Cited by 166
Self-citationEstimation of bumblebee queen dispersal distances using sibship reconstruction method
Lepais, O., Darvill, B., O’Connor, S., Osborne, J. L., Sanderson, R., Cussans, J. W., Goffe, L., & Goulson, D. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04500.x · Cited by 166
“Many bumblebee species have exhibited range contractions and regional extinctions in recent decades (Goulson et al. 2008; Williams & Osborne 2009).”
BackgroundSelf-citationUrban land use limits regional bumble bee gene flow
Jha, S., & Kremen, C. (2013) · Molecular Ecology · doi:10.1111/mec.12275 · Cited by 175
“Unfortunately, bumble bees are often the first bee species to be extirpated with human land use intensification (Larsen et al. 2005) and have exhibited population declines across a wide range of geographic regions (reviewed in Goulson et al. 2008).”
BackgroundInfluentialEvidence for competition between honeybees and bumblebees; effects on bumblebee worker size
Goulson, D., & Sparrow, K. R. (2008) · Journal of Insect Conservation · doi:10.1007/s10841-008-9140-y · Cited by 162
Self-citationBacterial Communities in Central European Bumblebees: Low Diversity and High Specificity
Koch, H., & Schmid‐Hempel, P. (2011) · Microbial Ecology · doi:10.1007/s00248-011-9854-3 · Cited by 160
“Over recent years, a decline in the abundance and range of bumblebee species has been noted in several parts of the world [ 24 , 70].”
BackgroundMerckx, T., & Slade, E. M. (2014) · Insect Conservation and Diversity · doi:10.1111/icad.12068 · Cited by 158
“These trends may form part of a wider insect biodiversity crisis (e.g. Conrad et al., 2006; Goulson et al., 2008; Brooks et al., 2012).”
Alien parasite hitchhikes to Patagonia on invasive bumblebee
Arbetman, M. P., Meeus, I., Morales, C. L., Aizen, M. A., & Smagghe, G. J. (2012) · Biological Invasions · doi:10.1007/s10530-012-0311-0 · Cited by 156
“Emergent infectious diseases are increasingly recognized as a potential driver of bumblebee decline (Goulson et al. 2008 and references therein; Meeus et al. 2011; Williams and Osborne 2009).”
BackgroundTest of the invasive pathogen hypothesis of bumble bee decline in North America
Cameron, S. A., Lim, H. C., Lozier, J. D., Duennes, M. A., & Thorp, R. W. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525266113 · Cited by 157
“Finally, these declines were occurring in the absence of a general decline among all bumble bee species, suggesting a targeted cause rather than more general environmental causes (8).”
BackgroundLocal bumble bee decline linked to recovery of honey bees, drought effects on floral resources
Thomson, D. M. (2016) · Ecology Letters · doi:10.1111/ele.12659 · Cited by 154
Wilson, C. J., & Jamieson, M. A. (2019) · PLoS ONE · doi:10.1371/journal.pone.0225852 · Cited by 158
Redhead, J. W., Dreier, S., Bourke, A. F. G., Heard, M. S., Jordan, W. C., Sumner, S., Wang, J., & Carvell, C. (2016) · Ecological Applications · doi:10.1890/15-0546 · Cited by 154
Current knowledge of detoxification mechanisms of xenobiotic in honey bees
Gong, Y., & Diao, Q. (2016) · Ecotoxicology · doi:10.1007/s10646-016-1742-7 · Cited by 154
Hülsmann, M., von Wehrden, H., Klein, A., & Leonhardt, S. D. (2015) · Apidologie · doi:10.1007/s13592-015-0366-x · Cited by 152
“Another reason for the high abundance of bumble bees at these sites could be the comparatively high abundance of Fabaceae and Lamiaceae (see Tables SI and SII), which are known to be preferentially visited by bumble bees (Goulson et al. 2008a; Sikora and Kelm 2012).”
BackgroundResultInfluentialOrchid conservation: from theory to practice
Phillips, R. D., Reiter, N., & Peakall, R. (2020) · Annals of Botany · doi:10.1093/aob/mcaa093 · Cited by 164
Kendall, L., Mola, J. M., Portman, Z. M., Cariveau, D. P., Smith, H. G., & Bartomeus, Í. (2022) · Ecology · doi:10.1002/ecy.3809 · Cited by 152
“As a result, among bees, small-bodied primitively eusocial and solitary taxa are likely to be most vulnerable to habitat loss and fragmentation, although assessments should also consider other known causes of decline (e.g., specialization, Goulson et al., 2008).”
Do linear landscape elements in farmland act as biological corridors for pollen dispersal?
Geert, A. V., Rossum, F. V., & Triest, L. (2009) · Journal of Ecology · doi:10.1111/j.1365-2745.2009.01600.x · Cited by 147
Neonicotinoid insecticides can serve as inadvertent insect contraceptives
Straub, L., Villamar‐Bouza, L., Bruckner, S., Chantawannakul, P., Gauthier, L., Khongphinitbunjong, K., Retschnig, G., Troxler, A., Vidondo, B., Neumann, P., et al. (2016) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2016.0506 · Cited by 147
Janousek, W. M., Douglas, M. R., Cannings, S., Clément, M. A., Delphia, C. M., Everett, J. G., Hatfield, R. G., Keinath, D. A., Koch, J. B. U., McCabe, L. M., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2211223120 · Cited by 147
What do we know about the effects of landscape changes on plant–pollinator interaction networks?
Ferreira, P. A., Bôscolo, D., & Viana, B. F. (2012) · Ecological Indicators · doi:10.1016/j.ecolind.2012.07.025 · Cited by 143
Floral abundance and resource quality influence pollinator choice
Fowler, R., Rotheray, E. L., & Goulson, D. (2016) · Insect Conservation and Diversity · doi:10.1111/icad.12197 · Cited by 145
“, 2010), bumblebees (Goulson et al., 2008) and solitary bees (Ollerton et al.”
BackgroundSelf-citationRecently identified bee viruses and their impact on bee pollinators
McMenamin, A. J., & Flenniken, M. L. (2018) · Current Opinion in Insect Science · doi:10.1016/j.cois.2018.02.009 · Cited by 143
Metadata
- Authors
- Goulson, D., Lye, G. C., & Darvill, B.
- Affiliations
- University of Stirling (GB)
- ORCID
- Goulson, D.
- Venue
- Annual Review of Entomology
- Publisher
- Annual Reviews
- Published
- 2008-01-01
- Volume
- 53
- Issue
- 1
- Pages
- 191-208
- ISSN
- 0066-4170 (ISSN-L)
- 1545-4487
- OpenAlex
- W2100945295
- Cited by
- 1,183
- References
- 104
- Citations by year
- 2026: 45 · 2025: 81 · 2024: 54 · 2023: 82 · 2022: 74 · 2021: 95 · 2020: 94 · 2019: 80 · 2018: 66 · 2017: 66 · 2016: 66 · 2015: 65 · 2014: 72 · 2013: 68 · 2012: 40
- FWCI
- 3.00
- Type
- journal article
- Language
- en
- Open access
- green
- figshare.com
- Licence
- cc-by
- Locations
- Annual Review of Entomology (publishedVersion)
- PubMed (publishedVersion)
- Stirling Online Research Repository (University of Stirling) (submittedVersion, public-domain)
- Figshare (submittedVersion, cc-by)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and animal studies
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect and Pesticide Research
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect and Arachnid Ecology and Behavior
- Keywords
- bumblebees, population decline (ecology), habitat loss, agricultural intensification, floral diversity, habitat fragmentation, inbreeding, stochastic extinction, pollination, conservation, pollinator decline, North America, Europe
- MeSH terms
- Agriculture, Animals, Bees, Conservation of Natural Resources, Environment, Pesticides, Population Dynamics, Flowers, Biodiversity
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