Decline and conservation of bumble bees
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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.
“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]
Data for bees and moths suggest the same declining trend as for other well-studied taxa.
“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]
Recently reported declines in butterflies, wild bees and moths are in parallel with a severe loss of total aerial insect biomass, suggesting that the flying insect community as a whole has been decimated over the last few decades.
“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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“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 1,426 · see citing works
“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.”
BackgroundInsect Declines in the Anthropocene
Wagner, D. L. (2019) · Annual Review of Entomology · doi:10.1146/annurev-ento-011019-025151 · Cited by 1,360 · see citing works
“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
Winfree, R., Aguilar, R., Vázquez, D. P., LeBuhn, G., & Aizen, M. A. (2009) · Ecology · doi:10.1890/08-1245.1 · Cited by 1,050 · see citing works
“Human disturbance, particularly the loss of natural and semi-natural habitats, is regarded as a primary cause of pollinator decline (Kearns et al. 1998, Aizen and Feinsinger 2003, Goulson et al. 2008).”
BackgroundNeonicotinoids in bees: a review on concentrations, side-effects and risk assessment
Blacquière, T., Smagghe, G. J., van Gestel, C. A. M., & Mommaerts, V. (2012) · Ecotoxicology · doi:10.1007/s10646-012-0863-x · Cited by 1,039 · see citing works
“parallel decrease of plant species, or vice versa (Biesmeijer et al. 2006; National Research Council of the National Academies 2007; Goulson et al. 2008).”
BackgroundPesticide Residues and Bees – A Risk Assessment
Sánchez‐Bayo, F., & Goka, K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094482 · Cited by 904 · see citing works
“Biological factors have been responsible for many of the problems that beekeepers have with their bee hives [24], but they are unlikely to be the main cause of disappearance of a number of wild bee species, or the decline of bumble bees in North America and Europe in recent years [12,25].”
BackgroundSocially transmitted gut microbiota protect bumble bees against an intestinal parasite
Koch, H., & Schmid‐Hempel, P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110474108 · Cited by 828 · see citing works
“P are believed to play a major role in the recent worldwide decline of honey bee and bumble bee populations (1–4), raising concerns over the loss of pollination services for agricultural crops and wild flowering plants (5, 6).”
BackgroundWhere is the UK's pollinator biodiversity? The importance of urban areas for flower-visiting insects
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 · see citing works
“However, declines have been reported for all key insect pollinator groups, including honeybees, bumblebees, solitary bees and hoverflies [5–8].”
The city as a refuge for insect pollinators
Hall, D. M., Camilo, G. R., Tonietto, R. K., Ollerton, J., Ahrné, K., Arduser, M., Ascher, J. S., Baldock, K. C. R., Fowler, R., Frankie, G. W., et al. (2016) · Conservation Biology · doi:10.1111/cobi.12840 · Cited by 661 · see citing works
“In the midst of a pollination crisis, where insect pollinator populations are experiencing significant declines (Jaffe et al. 2010; Pleasants & Oberhauser 2013; Goulson et al. 2015), studies of native bee richness and abundance indicate that diverse communities of wild bees persist in cities in many parts of the world…”
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 624 · see citing works
Ecological effects of invasive alien insects
Kenis, M., Auger-Rozenberg, M.-A., Roques, A., Timms, L., Péré, C., Cock, M. J. W., Settele, J., Augustin, S., & Lopez-Vaamonde, C. (2009) · Biological Invasions · doi:10.1007/s10530-008-9318-y · Cited by 750 · see citing works
“Other undesirable effects include co-introduction of natural enemies, inadequate pollination of native flora or undesirable pollination of exotic flora (Goulson 2003; Goulson et al. 2008).”
BackgroundInteractions between Nosema microspores and a neonicotinoid weaken honeybees ( Apis mellifera )
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 · see citing works
“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.”
BackgroundSown wildflower strips for insect conservation: a review
Haaland, C., Naisbit, R. E., & Bersier, L. (2010) · Insect Conservation and Diversity · doi:10.1111/j.1752-4598.2010.00098.x · Cited by 560 · see citing works
“Like many groups, insect populations have declined rapidly in agricultural landscapes in Europe.”
BackgroundInfluentialBumblebee vulnerability and conservation world-wide
Williams, P. H., & Osborne, J. L. (2009) · Apidologie · doi:10.1051/apido/2009025 · Cited by 557 · see citing works
“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 · see citing works
“We modelled occupancy at 25km 2 resolution (that is, 5 (cid”
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 · see citing works
Neonicotinoids, bee disorders and the sustainability of pollinator services
van der Sluijs, J. P., Simon‐Delso, N., Goulson, D., Maxim, L., Bonmatin, J., & Belzunces, L. (2013) · Current Opinion in Environmental Sustainability · doi:10.1016/j.cosust.2013.05.007 · Cited by 507 · see citing works
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 504 · see citing works
“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 · see citing works
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 466 · see citing works
Spatial and Temporal Trends of Global Pollination Benefit
Lautenbach, S., Seppelt, R., Liebscher, J., & Dormann, C. F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035954 · Cited by 444 · see citing works
“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 435 · see citing works
Godfray, H. C. J., Blacquière, T., Field, L. M., Hails, R. S., Petrokofsky, G., Potts, S. G., Raıne, N. E., Vanbergen, A. J., & McLean, A. R. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.0558 · Cited by 429 · see citing works
New frontiers in competition for pollination
Mitchell, R. J., Flanagan, R. J., Brown, B. J., Waser, N. M., & Karron, J. D. (2009) · Annals of Botany · doi:10.1093/aob/mcp062 · Cited by 428 · see citing works
“…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 395 · see citing works
Kovács‐Hostyánszki, A., Espíndola, A., Vanbergen, A. J., Settele, J., Kremen, C., & Dicks, L. V. (2017) · Ecology Letters · doi:10.1111/ele.12762 · Cited by 401 · see citing works
“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).”
BackgroundChanging Bee and Hoverfly Pollinator Assemblages along an Urban-Rural Gradient
Bates, A. J., Sadler, J. P., Fairbrass, A. J., Falk, S. J., Hale, J., & Matthews, T. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023459 · Cited by 389 · see citing works
“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.”
BackgroundInfluentialFortel, L., Henry, M., Guilbaud, L., Guirao, A.-L., Kuhlmann, M. T., Mouret, H., Rollin, O., & Vaissière, B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104679 · Cited by 364 · see citing works
“soil plowing, pesticide use, crop rotation, landscape simplification) are the main causes of bee diversity loss in farmland areas [95,96].”
BackgroundVaudo, A. D., Patch, H. M., Mortensen, D. A., Tooker, J. F., & Grozinger, C. M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606101113 · Cited by 357 · see citing works
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 · see citing works
“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).”
BackgroundThe decline of moths in Great Britain: a review of possible causes
FOX, R. (2013) · Insect Conservation and Diversity · doi:10.1111/j.1752-4598.2012.00186.x · Cited by 302 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 286 · see citing works
“…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 · see citing works
“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 282 · see citing works
“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 · see citing works
“Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output.”
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 · see citing works
The same, but different: pollen foraging in honeybee and bumblebee colonies
Leonhardt, S. D., & Blüthgen, N. (2011) · Apidologie · doi:10.1007/s13592-011-0112-y · Cited by 272 · see citing works
“…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 · see citing works
“…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 264 · see citing works
“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 · see citing works
“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).”
BackgroundInfluentialDötterl, S., & Vereecken, N. J. (2010) · Canadian Journal of Zoology · doi:10.1139/z10-031 · Cited by 258 · see citing works
“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 254 · see citing works
“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 · see citing works
Landscape‐scale resources promote colony growth but not reproductive performance of bumble bees
Williams, N. M., Regetz, J., & Kremen, C. (2011) · Ecology · doi:10.1890/11-1006.1 · Cited by 241 · see citing works
“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 241 · see citing works
“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 · see citing works
“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 232 · see citing works
“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 · see citing works
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 · see citing works
“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 228 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“…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 · see citing works
“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 · see citing works
Self-citationZayed, A. (2009) · Apidologie · doi:10.1051/apido/2009026 · Cited by 215 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
“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 208 · see citing works
“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 208 · see citing works
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 · see citing works
“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 · see citing works
“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 192 · see citing works
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 192 · see citing works
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 · see citing works
“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 · see citing works
“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 176 · see citing works
“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 · see citing works
“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 176 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
“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 164 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
“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 · see citing works
“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 155 · see citing works
“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 · see citing works
Wilson, C. J., & Jamieson, M. A. (2019) · PLoS ONE · doi:10.1371/journal.pone.0225852 · Cited by 158 · see citing works
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 · see citing works
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 · see citing works
Hülsmann, M., von Wehrden, H., Klein, A., & Leonhardt, S. D. (2015) · Apidologie · doi:10.1007/s13592-015-0366-x · Cited by 152 · see citing works
“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 161 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“, 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 · see citing works
- 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 › Biochemistry, Genetics and Molecular Biology › Genetics › 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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