Cited by 1,183Plant and animal studiesInsect and Pesticide ResearchInsect and Arachnid Ecology and Behavior

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Decline and Conservation of Bumble Bees

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Goulson, D., Lye, G.C., Darvill, B.·2008·Annual Review of Entomology

DOI 10.1146/annurev.ento.53.103106.093454

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Abstract

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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Background
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BackgroundInfluential
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Song, Z., & Feldman, M. W. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.2437 · Cited by 34
An assessment of bumblebee (Bombus spp) land use and floral preference in UK gardens and allotments cultivated for food
Foster, G. L., Bennett, J., & Sparks, T. H. (2016) · Urban Ecosystems · doi:10.1007/s11252-016-0604-7 · Cited by 34
“The main driver of insect pollinator decline is thought to be habitat loss, as a result of agricultural intensification and increasing urbanisation (Goulson et al. 2008; Winfree et al. 2009; Potts et al. 2010).”
Background
Habitat suitability for the invasion of Bombus terrestris in East Asian countries: A case study of spatial overlap with local Chinese bumblebees
Naeem, M., Yuan, X.-L., Huang, J., & An, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-29414-6 · Cited by 34
Seasonality and Landscape Composition Drive the Diversity of Pollen Collected by Managed Honey Bees
Malagnini, V., Cappellari, A., Marini, L., Zanotelli, L., Zorer, R., Angeli, G., Ioriatti, C., & Fontana, P. (2022) · Frontiers in Sustainable Food Systems · doi:10.3389/fsufs.2022.865368 · Cited by 33
“One of the main causes of this decline is the loss and fragmentation of natural areas, which led to a decrease in plant diversity, potentially determining insufficient nutrition for pollinators (Goulson et al., 2008).”
Background
The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis)
Erler, S., & Lattorff, H. M. G. (2010) · Insectes Sociaux · doi:10.1007/s00040-010-0093-2 · Cited by 33
“Goulson et al. (2008) asked for the development of long-term monitoring of bumblebee pop-”
Background
Determining habitat suitability for bumblebees in a mountain system: a baseline approach for testing the impact of climate change on the occurrence and abundance of species
Herrera, J. M., Ploquin, E. F., Rodríguez‐Pérez, J., & Obeso, J. R. (2013) · Journal of Biogeography · doi:10.1111/jbi.12236 · Cited by 33
“…suffered severe declines in recent decades (Williams et al., 2007; Goulson et al., 2008; Cameron et al., 2011) and research suggests that climatic variations could be driving this widespread decrease (Goulson et al., 2008; Williams et al., 2009; Iserbyt & Rasmont, 2012; Rasmont & Iserbyt, 2012).”
Background
Pollen Diet Composition Impacts Early Nesting Success in Queen Bumble Bees Bombus impatiens Cresson(Hymenoptera: Apidae)
Watrous, K. M., Duennes, M. A., & Woodard, S. H. (2019) · Environmental Entomology · doi:10.1093/ee/nvz043 · Cited by 33
Impacts of Agricultural Management Systems on Biodiversity and Ecosystem Services in Highly Simplified Dryland Landscapes
Adhikari, S., Adhikari, A., Weaver, D. K., Bekkerman, A., & Menalled, F. D. (2019) · Sustainability · doi:10.3390/su11113223 · Cited by 36
Wild Bee Toxicity Data for Pesticide Risk Assessments
Lewis, K. A., & Tzilivakis, J. (2019) · Data · doi:10.3390/data4030098 · Cited by 33
“In addition, bumblebees (and some other wild bee species) use a special technique known as ‘buzz pollination’ or sonication whereby flight muscles are contracted to produce strong vibrations that effectively shake the pollen loose from the plant [4,5].”
Background
Metatranscriptome Analysis of Sympatric Bee Species Identifies Bee Virus Variants and a New Virus, Andrena-Associated Bee Virus-1
Daughenbaugh, K. F., Kahnonitch, I., Carey, C. C., McMenamin, A. J., Wiegand, T., Erez, T., Arkin, N., Ross, B. T., Wiedenheft, B., Sadeh, A., et al. (2021) · Viruses · doi:10.3390/v13020291 · Cited by 33
“In particular, many bee populations have suffered range reductions and local extinction, in‐ cluding the rusty patched bumble bee (Bombus affinis) and the western bumble bee (Bom‐ bus occidentalis) in the US [12,13,14].”
Background
Intra-specific variation in sensitivity of Bombus terrestris and Osmia bicornis to three pesticides
Linguadoca, A., Jürison, M., Hellström, S., Straw, E. A., Šima, P., Karise, R., Costa, C., Serra, G., Colombo, R., Paxton, R. J., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-22239-4 · Cited by 33
Evidence for habitat and climatic specializations driving the long‐term distribution trends of UK and I rish bumblebees
Casey, L. M., Rebelo, H., Rotheray, E. L., & Goulson, D. (2015) · Diversity and Distributions · doi:10.1111/ddi.12344 · Cited by 33
“Distributional studies in North America, Europe and Asia reveal severe declines in a high proportion of species (Goulson et al., 2008; Williams & Osborne, 2009; Williams et al., 2009b; Cameron et al., 2011), emphasizing the need for research, monitoring and conservation.”
BackgroundMethodInfluentialSelf-citation
Current Pesticide Risk Assessment Protocols Do Not Adequately Address Differences between Honey Bees (Apis mellifera) and Bumble Bees (Bombus spp.)
Stoner, K. A. (2016) · Frontiers in Environmental Science · doi:10.3389/fenvs.2016.00079 · Cited by 32
“The importance of bumble bees to agricultural and natural systems makes the decline in range and abundance of many bumble bee species a matter of great concern (Colla and Packer, 2008; Goulson et al., 2008; Grixti et al., 2009; Williams and Osborne, 2009; Cameron et al., 2011; Colla et al., 2012).”
Background
Past, present and future distributions of bumblebees in South America: Identifying priority species and areas for conservation
Krechemer, F. D. S., & Marchioro, C. A. (2020) · Journal of Applied Ecology · doi:10.1111/1365-2664.13650 · Cited by 32
Do Viruses From Managed Honey Bees (Hymenoptera: Apidae) Endanger Wild Bees in Native Prairies?
PRITCHARD, Z. A., Hendriksma, H. P., Clair, A. L. S., Stein, D. S., Dolezal, A. G., O’Neal, M. E., & Toth, A. L. (2020) · Environmental Entomology · doi:10.1093/ee/nvaa181 · Cited by 32
Neither protogynous nor obligatory out‐crossed: pollination biology and breeding system of the European Red ListFritillaria meleagrisL. (Liliaceae)
Zych, M., & Stpiczyńska, M. (2011) · Plant Biology · doi:10.1111/j.1438-8677.2011.00510.x · Cited by 32
“This information coupled with data on bumblebee decline in Central Europe (e.g., Kosior et al. 2007; Goulson et al. 2008) suggests that the populations may be threatened with extinction due to pollen limitation and a resulting decrease in seed production.”
BackgroundResult
Experimental reduction of pollinator visitation modifies plant–plant interactions for pollination
Lázaro, A., Lundgren, R., & Totland, Ø. (2014) · Oikos · doi:10.1111/oik.01268 · Cited by 32
The Status ofBombus occidentalisandB. moderatusin Alaska with Special Focus onNosema bombiIncidence
Koch, J. B. U., & Strange, J. P. (2012) · Northwest Science · doi:10.3955/046.086.0306 · Cited by 32
Revealing the hidden niches of cryptic bumblebees in Great Britain: Implications for conservation
Scriven, J. J., Woodall, L. C., Tinsley, M. C., Knight, M. E., Williams, P. H., Carolan, J. C., Brown, M. J. F., & Goulson, D. (2014) · Biological Conservation · doi:10.1016/j.biocon.2014.11.027 · Cited by 31
“Niche-partitioning might be 169 expected between these species (Goulson et al. 2008b) and indeed some ecological differences have 170 been suggested.”
BackgroundSelf-citation
Landscape alteration and habitat modification: impacts on plant–pollinator systems
Vanbergen, A. J. (2014) · Current Opinion in Insect Science · doi:10.1016/j.cois.2014.09.004 · Cited by 31
Decline of nest site availability and nest density of underground bees along a distance gradient from human settlements
Xie, Z., Qiu, J., & Chen, X. (2013) · Entomological Science · doi:10.1111/ens.12009 · Cited by 30
“These practices principally aim to protect and/or restore food plant resources (Goulson et al. 2008; Brown & Paxton 2009; Batáry et al. 2010); however, the conservation of nest sites did not receive much attention.”
Background
Sustainable development in circular agriculture: An illustrative bee↺legume↺poultry example
Rauw, W. M., Gomez‐Raya, L., Star, L., Øverland, M., Delezie, E., Grīviņš, M., Hamann, K. T., Pietropaoli, M., Klaassen, M. T., Klemetsdal, G., et al. (2022) · Sustainable Development · doi:10.1002/sd.2435 · Cited by 31
Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae)
Wolf, S., Toev, T., Moritz, R. L. V., & Moritz, R. F. A. (2011) · Population Ecology · doi:10.1007/s10144-011-0285-2 · Cited by 31
“Only recently this issue has been addressed in various conservation genetic studies especially on social bees (Kearns et al. 1998; Packer et al. 2005; Darvill et al. 2006; Ellis et al. 2006; Goulson et al. 2008a, 2008b; Brown and Paxton 2009; Grixti et al. 2009; Murray et al. 2009; Zayed 2009; Charman et al. 2010).”
BackgroundInfluential
Mass Flowering Crops as a Conservation Resource for Wild Pollinators (Hymenoptera: Apoidea)
Todd, K. J., Gardiner, M. M., & Lindquist, E. D. (2016) · Journal of the Kansas Entomological Society · doi:10.2317/0022-8567-89.2.158 · Cited by 30
Examining the nutritional value and effects of different floral resources in pumpkin agroecosystems on Bombus impatiens worker physiology
Treanore, E. D., Vaudo, A. D., Grozinger, C. M., & Fleischer, S. J. (2019) · Apidologie · doi:10.1007/s13592-019-00668-x · Cited by 32
Effects of three flower field types on bumblebees and their pollen diets
Piko, J. I., Keller, A., Geppert, C., Batáry, P., Tscharntke, T., Westphal, C., & Hass, A. L. (2021) · Basic and Applied Ecology · doi:10.1016/j.baae.2021.02.005 · Cited by 30
Pollination Ecology: Natural History, Perspectives and Future Directions
Torezan‐Silingardi, H. M., Silberbauer-Gottsberger, I., & Gottsberger, G. (2021) · Springer eBooks · doi:10.1007/978-3-030-66877-8_6 · Cited by 30
Neonicotinoid Pesticides Cause Mass Fatalities of Native Bumble Bees: A Case Study From Wilsonville, Oregon, United States
Hatfield, R. G., Strange, J. P., Koch, J. B. U., Jepsen, S., & Stapleton, I. (2021) · Environmental Entomology · doi:10.1093/ee/nvab059 · Cited by 30
The evidence for and against competition between the European honeybee and Australian native bees
Prendergast, K. S., Dixon, K. W., & Bateman, P. W. (2022) · Pacific Conservation Biology · doi:10.1071/pc21064 · Cited by 30
“Indeed, studies have demonstrated negative competitive effects of honeybees on Bombus (Thomson 2004, 2006, 2016; Goulson et al. 2008; Elbgami et al. 2014; Torné-Noguera et al. 2016): a wellstudied genus, phylogenetically close to Apis – both Apinae, Corbiculata (Bossert et al. 2019).”
Background
Myth and reality of a global crisis for agricultural pollination
Aizen, M. A., Garibaldi, L. A., & Harder, L. D. (2022) · Ecología Austral · doi:10.25260/ea.22.32.2.1.1875 · Cited by 30
Microsatellite analysis in museum samples reveals inbreeding before the regression of Bombus veteranus
Maebe, K., Meeus, I., Maharramov, J., Grootaert, P., Michez, D., Rasmont, P., & Smagghe, G. J. (2012) · Apidologie · doi:10.1007/s13592-012-0170-9 · Cited by 30
“In their review, Goulson et al. (2008) presented the hypothesis that the genetic diversity (NA and HE) in current declined species is reduced as compared to other common Bombus species.”
BackgroundInfluential
Contextualising pollination benefits: effect of insecticide and fungicide use on fruit set and weight from bee pollination in lowbush blueberry
Melathopoulos, A. P., Tyedmers, P. H., & Cutler, G. C. (2014) · Annals of Applied Biology · doi:10.1111/aab.12143 · Cited by 30
“This might indeed be the case among many crops where other limitations have been alleviated through intensive agriculture, at the expense of wild pollinator populations (Goulson et al., 2008; Winfree, 2010; Bommarco et al., 2012).”
Background
Neonicotinoid insecticides in pollen, honey and adult bees in colonies of the European honey bee (Apis mellifera L.) in Egypt
Codling, G., Naggar, Y. A., Giesy, J. P., & Robertson, A. J. (2017) · Ecotoxicology · doi:10.1007/s10646-017-1876-2 · Cited by 30
Diversity of bumblebees, heteropteran bugs and grasshoppers maintained by both: abandonment and extensive management of mountain meadows in three regions across the Austrian and Swiss Alps
Walcher, R., Karrer, J., Sachslehner, L., Bohner, A., Pachinger, B., Brandl, D., Zaller, J. G., Arnberger, A., & Frank, T. (2017) · Landscape Ecology · doi:10.1007/s10980-017-0556-1 · Cited by 29
“Loosing suitable foraging habitats and floral resources negatively affects bumblebees (Goulson et al. 2008).”
Background
The prevalence of olfactory- versus visual-signal encounter by searching bumblebees
Sprayberry, J. D. H. (2018) · Scientific Reports · doi:10.1038/s41598-018-32897-y · Cited by 29
One‐size does not fit all: at‐risk bumble bee habitat management requires species‐specific local and landscape considerations
Liczner, A., & Colla, S. R. (2020) · Insect Conservation and Diversity · doi:10.1111/icad.12419 · Cited by 29
“include: habitat loss (Goulson et al., 2008; Williams & Osborne, 2009), pathogen spillover (Colla et al.”
Background
A century of pollen foraging by the endangered rusty patched bumble bee (Bombus affinis): inferences from molecular sequencing of museum specimens
Simanonok, M. P., Otto, C. R. V., Cornman, R. S., Iwanowicz, D. D., Strange, J. P., & Smith, T. (2020) · Biodiversity and Conservation · doi:10.1007/s10531-020-02081-8 · Cited by 29
Impacts of Neonicotinoids on the Bumble Bees Bombus terrestris and Bombus impatiens Examined through the Lens of an Adverse Outcome Pathway Framework
Camp, A. A., & Lehmann, D. M. (2020) · Environmental Toxicology and Chemistry · doi:10.1002/etc.4939 · Cited by 32
“) are critical for commercial and noncommercial pollination and also face population declines (Losey and Vaughan 2006; Colla and Packer 2008; Goulson et al. 2008; Grixti et al. 2009; Cameron et al. 2010; Lozier et al. 2011).”
Background
Biosafety of bee pollinators in genetically modified agro‐ecosystems: Current approach and further development in the EU
Arpaia, S., Smagghe, G. J., & Sweet, J. B. (2021) · Pest Management Science · doi:10.1002/ps.6287 · Cited by 31
Body mass and sex, not local climate, drive differences in chill coma recovery times in common garden reared bumble bees
Oyen, K., Jardine, L. E., Parsons, Z. M., Herndon, J. D., Strange, J. P., Lozier, J. D., & Dillon, M. E. (2021) · Journal of Comparative Physiology B · doi:10.1007/s00360-021-01385-7 · Cited by 29
Use of video surveillance to measure the influences of habitat management and landscape composition on pollinator visitation and pollen deposition in pumpkin ( Cucurbita pepo ) agroecosystems
Phillips, B. W., & Gardiner, M. M. (2015) · PeerJ · doi:10.7717/peerj.1342 · Cited by 31
Using BEEHAVE to explore pesticide protection goals for European honeybee (Apis melifera L.) worker losses at different forage qualities
Thorbek, P., Campbell, P. J., Sweeney, P. J., & Thompson, H. (2016) · Environmental Toxicology and Chemistry · doi:10.1002/etc.3504 · Cited by 29
“resulted in less and less continuous forage for pollinators [50].”
Background
Impact of honeybee (Apis mellifera L.) density on wild bee foraging behaviour
Goras, G., Tananaki, C., Dimou, M. V., Tscheulin, T., Petanidou, T., & Thrasyvoulou, A. T. (2016) · Journal of Apicultural Science · doi:10.1515/jas-2016-0007 · Cited by 29
“The decline is mainly due to changes of agricultural activities such as changes in land use, modern agricultural practices, and pesticide use (Allen-Wardell et al., 1998; Potts et al., 2006; Kremen et al., 2007; Goulson et al., 2008; Brown & Paxton, 2009).”
Background

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
DOI: 10.1146/annurev.ento.53.103106.093454
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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