A meta-analysis of bees’ responses to anthropogenic disturbance
Open accessAbstract
Pollinators may be declining globally, a matter of concern because animal pollination is required by most of the world's plant species, including many crop plants. Human land use and the loss of native habitats is thought to be an important driver of decline for wild, native pollinators, yet the findings of published studies on this topic have never been quantitatively synthesized. Here we use meta‐analysis to synthesize the literature on how bees, the most important group of pollinators, are affected by human disturbances such as habitat loss, grazing, logging, and agriculture. We obtained 130 effect sizes from 54 published studies recording bee abundance and/or species richness as a function of human disturbance. Both bee abundance and species richness were significantly, negatively affected by disturbance. However, the magnitude of the effects was not large. Furthermore, the only disturbance type showing a significant negative effect, habitat loss and fragmentation, was statistically significant only in systems where very little natural habitat remains. Therefore, it would be premature to draw conclusions about habitat loss having caused global pollinator decline without first assessing the extent to which the existing studies represent the status of global ecosystems. Future pollinator declines seem likely given forecasts of increasing land‐use change.
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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 [10]
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 [10]
The number of studies on insect trends with sufficient replication and spatial coverage is limited and restricted to certain well-studied taxa.
“However, the number of studies on insect trends with sufficient replication and spatial coverage are limited [10, 23–25] and restricted to certain well-studied taxa.”
From More than 75 percent decline over 27 years in total flying insect biomass in protected areas (2017) · cites this paper as [10]
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 [10]
Cites
Statistical power analysis for the behavioral sciences
Cohen, J. (1990) · Computers Environment and Urban Systems · doi:10.1016/0198-9715(90)90050-4 · Cited by 65,406 · see citing works
Wasserman, S. S., Hedges, L. V., & Olkin, I. (1988) · Journal of Educational Statistics · doi:10.2307/1164953 · Cited by 10,347 · see citing works
Global Biodiversity Scenarios for the Year 2100
Sala, O. E., Stuart Chapin, F., III, Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L. F., Jackson, R. B., et al. (2000) · Science · doi:10.1126/science.287.5459.1770 · Cited by 9,280 · see citing works
Human domination of Earth’s ecosystems
Vitousek, P. M., Mooney, H. A., Lubchenco, J., & Melillo, J. M. (1997) · Science · doi:10.1126/science.277.5325.494 · Cited by 9,086 · see citing works
The file drawer problem and tolerance for null results.
Rosenthal, R. (1979) · Psychological Bulletin · doi:10.1037/0033-2909.86.3.638 · Cited by 9,068 · see citing works
Terrestrial ecoregions of the world: a new map of life on Earth
Olson, D. M., Dinerstein, E., Wikramanayake, E. D., Burgess, N. D., Powell, G. V. N., Underwood, E. C., D'amico, J. A., Itoua, I., Strand, H. E., Morrison, J. C., et al. (2001) · BioScience · doi:10.1641/0006-3568(2001)051[0933:teotwa]2.0.co;2 · Cited by 8,488 · see citing works
Effects of Habitat Fragmentation on Biodiversity
Fahrig, L. (2003) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.34.011802.132419 · Cited by 7,879 · see citing works
Importance of pollinators in changing landscapes for world crops
Klein, A., Vaissière, B., Cane, J. H., Steffan-Dewenter, I. D., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3721 · Cited by 7,211 · see citing works
Statistical Methods for Meta-Analysis.
Freeman, P. R., Hedges, L. V., & Olkin, I. (1986) · Biometrics · doi:10.2307/2531069 · Cited by 4,832 · see citing works
Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands
Biesmeijer, J. C., Roberts, S. P. M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A. P., Potts, S. G., Kleukers, R., Thomas, C. D., et al. (2006) · Science · doi:10.1126/science.1127863 · Cited by 3,189 · see citing works
Landscape modification and habitat fragmentation: a synthesis
Fischer, J., & Lindenmayer, D. B. (2007) · Global Ecology and Biogeography · doi:10.1111/j.1466-8238.2007.00287.x · Cited by 2,447 · see citing works
ENDANGERED MUTUALISMS: The Conservation of Plant-Pollinator Interactions
Kearns, C., Inouye, D., & Waser, N. (1998) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.29.1.83 · Cited by 1,872 · see citing works
Putting people in the map: anthropogenic biomes of the world
Ellis, E. C., & Ramankutty, N. (2007) · Frontiers in Ecology and the Environment · doi:10.1890/070062 · Cited by 1,858 · see citing works
A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder
Cox-Foster, D., Conlan, S., Holmes, E. C., Palacios, G. F., Evans, J. D., Moran, N. A., Quan, P., Briese, T., Hornig, M., Geiser, D. M., et al. (2007) · Science · doi:10.1126/science.1146498 · Cited by 1,754 · see citing works
Kremen, C., Williams, N. M., Aizen, M. A., Gemmill‐Herren, B., LeBuhn, G., Minckley, R. L., Packer, L., Potts, S. G., Roulston, T. H., Steffan-Dewenter, I. D., et al. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01018.x · Cited by 1,497 · see citing works
Self-citationLandscape effects on crop pollination services: are there general patterns?
Ricketts, T. H., Regetz, J., Steffan-Dewenter, I. D., Cunningham, S. A., Kremen, C., Bogdanski, A., Gemmill‐Herren, B., Greenleaf, S. S., Klein, A., Mayfield, M. M., et al. (2008) · Ecology Letters · doi:10.1111/j.1461-0248.2008.01157.x · Cited by 1,383 · see citing works
Statistical Power Analysis for the Behavioral Sciences
Wassertheil, S., & Cohen, J. (1970) · Biometrics · doi:10.2307/2529115 · Cited by 1,383 · see citing works
POLLEN LIMITATION OF PLANT REPRODUCTION: ECOLOGICAL AND EVOLUTIONARY CAUSES AND CONSEQUENCES
Ashman, T., Knight, T. M., Steets, J. A., Amarasekare, P., Burd, M., Campbell, D. R., Dudash, M. R., Johnston, M. O., Mazer, S. J., Mitchell, R. J., et al. (2004) · Ecology · doi:10.1890/03-8024 · Cited by 1,375 · see citing works
Synthesizing Research: A Guide for Literature Reviews
Cooper, H. (1998) · Cited by 1,285 · see citing works
Rosenberg, M. S. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01004.x · Cited by 1,285 · see citing works
Decline and conservation of bumble bees
Goulson, D., Lye, G. C., & Darvill, B. (2008) · Annual Review of Entomology · doi:10.1146/annurev.ento.53.103106.093454 · Cited by 1,183 · cited 1× · 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).”
BackgroundAguilar, R., Ashworth, L., Galetto, L., & Aizen, M. A. (2006) · Ecology Letters · doi:10.1111/j.1461-0248.2006.00927.x · Cited by 1,078 · see citing works
Self-citationThe Handbook of Research Synthesis
Ziegel, E. R., Cooper, H., & Hedges, L. V. (1995) · Technometrics · doi:10.2307/1269651 · Cited by 936 · see citing works
Fruit set of highland coffee increases with the diversity of pollinating bees
Klein, A., Steffan‐Dewenter, I., & Tscharntke, T. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2306 · Cited by 857 · see citing works
Wild bees enhance honey bees’ pollination of hybrid sunflower
Greenleaf, S. S., & Kremen, C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600929103 · Cited by 721 · see citing works
Meta-analysis: Combining the Results of Independent Experiments
Gurevitch, J., & Hedges, L. V. (2001) · doi:10.1093/oso/9780195131871.003.0018 · Cited by 706 · see citing works
RESAMPLING TESTS FOR META-ANALYSIS OF ECOLOGICAL DATA
Adams, D. C., Gurevitch, J., & Rosenberg, M. S. (1997) · Ecology · doi:10.1890/0012-9658(1997)078[1277:rtfmao]2.0.co;2 · Cited by 692 · see citing works
Buchmann, S. L., & Nabhan, G. P. (2012) · Princeton University Press eBooks · doi:10.2307/jj.41003449 · Cited by 603 · see citing works
Habitat Fragmentation, Native Insect Pollinators, and Feral Honey Bees in Argentine 'Chaco Serrano'
Aizen, M. A., & Feinsinger, P. (1994) · Ecological Applications · doi:10.2307/1941941 · Cited by 475 · see citing works
Self-citationArnqvist, G. (1998) · The Quarterly Review of Biology · doi:10.1086/420179 · Cited by 474 · see citing works
Pollinator diversity and crop pollination services are at risk
Steffan‐Dewenter, I., Potts, S. G., & Packer, L. A. D. T. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.09.004 · Cited by 470 · see citing works
(1997) · Choice Reviews Online · doi:10.5860/choice.34-2735 · Cited by 469 · see citing works
Plant–pollinator Interactions: From Specialization To Generalization
del Rio, C. M. (2006) · Ornithological Applications · doi:10.1093/condor/108.4.986 · Cited by 466 · see citing works
(1994) · Cited by 463 · see citing works
Effect of Human Disturbance on Bee Communities in a Forested Ecosystem
Winfree, R., Griswold, T., & Kremen, C. (2006) · Conservation Biology · doi:10.1111/j.1523-1739.2006.00574.x · Cited by 461 · see citing works
Self-citationTscharntke, T., Steffan-Dewenter, I. D., Kruess, A., & Thies, C. (2002) · Ecological Applications · doi:10.1890/1051-0761(2002)012[0354:coshft]2.0.co;2 · Cited by 439 · see citing works
Buzziness as usual? Questioning the global pollination crisis
Ghazoul, J. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.04.026 · Cited by 410 · see citing works
Status of Pollinators in North America
National Research Council (2007) · National Academies Press eBooks · doi:10.17226/11761 · Cited by 407 · see citing works
Variation in Native Bee Faunas and its Implications for Detecting Community Changes
Williams, N. M., Minckley, R. L., & da Silveira, F. A. (2001) · Conservation Ecology · doi:10.5751/es-00259-050107 · Cited by 328 · see citing works
Quantifying and comparing bumblebee nest densities in gardens and countryside habitats
Osborne, J. L., Martin, A. P., Shortall, C. R., Todd, A. D., Goulson, D., Knight, M. E., Hale, R. J., & Sanderson, R. (2007) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2007.01359.x · Cited by 303 · see citing works
Habitat Fragmentation and Native Bees: a Premature Verdict?
Cane, J. H. (2001) · Conservation Ecology · doi:10.5751/es-00265-050103 · Cited by 273 · see citing works
Genetic rescue of remnant tropical trees by an alien pollinator
Dick, C. W. (2001) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2001.1781 · Cited by 252 · see citing works
Stokstad, E. (2007) · Science · doi:10.1126/science.316.5827.970 · Cited by 249 · see citing works
Knight, T. M., Steets, J. A., & Ashman, T. (2006) · American Journal of Botany · doi:10.3732/ajb.93.2.271 · Cited by 232 · see citing works
Chacoff, N. P., & Aizen, M. A. (2005) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2005.01116.x · Cited by 224 · see citing works
Self-citationUps and Downs in Pollinator Populations: When is there a Decline?
Roubik, D. W. (2001) · Conservation Ecology · doi:10.5751/es-00255-050102 · Cited by 211 · see citing works
Effects of UVB radiation on marine and freshwater organisms: a synthesis through meta‐analysis
Bancroft, B. A., Baker, N. J., & Blaustein, A. R. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01022.x · Cited by 205 · see citing works
Sperm ultrastructure of the wasp Agelaia vicina (Hymenoptera, Vespidae)
Mancini, K. C., Lino‐Neto, J., Campos, L. A. O., & Dolder, H. (2006) · Insectes Sociaux · doi:10.1007/s00040-006-0877-6 · Cited by 199 · see citing works
Bladder injury during transobturator sling
Minaglia, S. M., Özel, B. Z., Klutke, C. G., Ballard, C. A., & Klutke, J. J. (2004) · Urology · doi:10.1016/j.urology.2004.04.030 · Cited by 196 · see citing works
Insect pollinators and sustainable agriculture
Kevan, P. G., Clark, E. A., & Thomas, V. G. (1990) · Renewable Agriculture and Food Systems · doi:10.1017/s0889189300003179 · Cited by 159 · see citing works
Kim, J. H., Williams, N. M., & Kremen, C. (2006) · Journal of the Kansas Entomological Society · doi:10.2317/0507.11.1 · Cited by 156 · see citing works
Aizen, M. A., & Feinsinger, P. (2003) · Ecological studies · doi:10.1007/978-3-662-05238-9_7 · Cited by 145 · see citing works
Self-citationBee diversity and plant-pollinator interactions in fragmented landscapes
Steffan-Dewenter, I. D., Klein, A., Gaebele, V., Alfert, T., & Tscharntke, T. (2006) · GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) · Cited by 107 · see citing works
Morphology and the evolution of wind pollination
Linder, H. P. (1998) · Cited by 74 · see citing works
Response to Steffan-Dewenter et al.: Questioning the global pollination crisis
Ghazoul, J. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.09.006 · Cited by 29 · see citing works
Flagged first, then by citations
2 of the 57 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Global pollinator declines: trends, impacts and drivers
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E. (2010) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2010.01.007 · Cited by 6,458 · see citing works
How many flowering plants are pollinated by animals?
Ollerton, J., Winfree, R., & Tarrant, S. (2011) · Oikos · doi:10.1111/j.1600-0706.2010.18644.x · Cited by 3,874 · see citing works
Self-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 · see citing works
Vilà, M., Espinar, J. L., Hejda, M., Hulme, P. E., Jarošík, V., Maron, J. L., Pergl, J., Schaffner, U., Sun, Y., & Pyšek, P. (2011) · Ecology Letters · doi:10.1111/j.1461-0248.2011.01628.x · Cited by 3,068 · see citing works
Landscape moderation of biodiversity patterns and processes ‐ eight hypotheses
Tscharntke, T., Tylianakis, J. M., Rand, T. A., Didham, R. K., Fahrig, L., Batáry, P., Bengtsson, J., Clough, Y., Crist, T. O., Dormann, C. F., et al. (2012) · Biological Reviews · doi:10.1111/j.1469-185x.2011.00216.x · Cited by 2,134 · see citing works
Kremen, C., & Miles, A. (2012) · Ecology and Society · doi:10.5751/es-05035-170440 · Cited by 1,126 · see citing works
Aizen, M. A., & Harder, L. D. (2009) · Current Biology · doi:10.1016/j.cub.2009.03.071 · Cited by 1,116 · see citing works
Self-citationGaribaldi, L. A., Steffan-Dewenter, I., Kremen, C., Morales, J. M., Bommarco, R., Cunningham, S. A., Carvalheiro, L. G., Chacoff, N. P., Dudenhöffer, J. H., Greenleaf, S. S., et al. (2011) · Ecology Letters · doi:10.1111/j.1461-0248.2011.01669.x · Cited by 962 · see citing works
Self-citationNon-bee insects are important contributors to global crop pollination
Rader, R., Bartomeus, I., Garibaldi, L. A., Garratt, M. P. D., Howlett, B. G., Winfree, R., Cunningham, S. A., Mayfield, M. M., Arthur, A. D., Andersson, G. K. S., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1517092112 · Cited by 1,000 · see citing works
Self-citationThe worldwide importance of honey bees as pollinators in natural habitats
Hung, K. J., Kingston, J. M., Albrecht, M., Holway, D. A., & Kohn, J. R. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.2140 · Cited by 797 · see citing works
Calderone, N. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037235 · Cited by 768 · see citing works
Ecological and life-history traits predict bee species responses to environmental disturbances
Williams, N. M., Crone, E. E., Roulston, T. H., Minckley, R. L., Packer, L., & Potts, S. G. (2010) · Biological Conservation · doi:10.1016/j.biocon.2010.03.024 · Cited by 752 · see citing works
Country-specific effects of neonicotinoid pesticides on honey bees and wild bees
Woodcock, B. A., Bullock, J. M., Shore, R. F., Heard, M. S., Pereira, M. G., Redhead, J. W., Ridding, L. E., Dean, H., Sleep, D., Henrys, P. A., et al. (2017) · Science · doi:10.1126/science.aaa1190 · Cited by 746 · see citing works
The Role of Resources and Risks in Regulating Wild Bee Populations
Roulston, T. H., & Goodell, K. (2010) · Annual Review of Entomology · doi:10.1146/annurev-ento-120709-144802 · Cited by 673 · see citing works
Native Pollinators in Anthropogenic Habitats
Winfree, R., Bartomeus, Í., & Cariveau, D. P. (2011) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-102710-145042 · Cited by 621 · see citing works
Self-citationMutualisms in a changing world: an evolutionary perspective
Kiers, E. T., Palmer, T. M., Ives, A. R., Bruno, J. F., & Bronstein, J. L. (2010) · Ecology Letters · doi:10.1111/j.1461-0248.2010.01538.x · Cited by 587 · see citing works
Impacts 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
From research to action: enhancing crop yield through wild pollinators
Garibaldi, L. A., Carvalheiro, L. G., Leonhardt, S. D., Aizen, M. A., Blaauw, B. R., Isaacs, R., Kuhlmann, M. T., Kleijn, D., Klein, A., Kremen, C., et al. (2014) · Frontiers in Ecology and the Environment · doi:10.1890/130330 · Cited by 546 · 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
How urbanization is driving pollinator diversity and pollination – A systematic review
Wenzel, A., Graß, I., Belavadi, V. V., & Tscharntke, T. (2019) · Biological Conservation · doi:10.1016/j.biocon.2019.108321 · Cited by 493 · 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
Linking Landscape Connectivity and Ecosystem Service Provision: Current Knowledge and Research Gaps
Mitchell, M. G. E., Bennett, E. M., & Gonzalez, A. (2013) · Ecosystems · doi:10.1007/s10021-013-9647-2 · Cited by 435 · see citing works
Urban areas as hotspots for bees and pollination but not a panacea for all insects
Theodorou, P., Radzevičiūtė, R., Lentendu, G., Kahnt, B., Husemann, M., Bleidorn, C., Settele, J., Schweiger, O., Große, I., Wubet, T., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14496-6 · Cited by 413 · see citing works
The 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
Self-citationChanging 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
Do managed bees have negative effects on wild bees?: A systematic review of the literature
Mallinger, R. E., Gaines‐Day, H. R., & Gratton, C. (2017) · PLoS ONE · doi:10.1371/journal.pone.0189268 · Cited by 379 · see citing works
Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms
Menz, M. H. M., Phillips, R. D., Winfree, R., Kremen, C., Aizen, M. A., Johnson, S. D., & Dixon, K. W. (2010) · Trends in Plant Science · doi:10.1016/j.tplants.2010.09.006 · Cited by 372 · see citing works
Self-citationPollination services decline with distance from natural habitat even in biodiversity‐rich areas
Carvalheiro, L. G., Seymour, C. L., Veldtman, R., & Nicolson, S. W. (2010) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2010.01829.x · Cited by 365 · see citing works
Réquier, F., Odoux, J. F., Tamic, T., Moreau, N., Henry, M., Decourtye, A., & Bretagnolle, V. (2014) · Ecological Applications · doi:10.1890/14-1011.1 · Cited by 350 · see citing works
Bretagnolle, V., & Gaba, S. (2015) · Agronomy for Sustainable Development · doi:10.1007/s13593-015-0302-5 · Cited by 323 · see citing works
Diverse pollinator communities enhance plant reproductive success
Albrecht, M., Schmid, B., Hautier, Y., & MÜLLER, C. B. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1621 · Cited by 322 · see citing works
Dispersal capacity and diet breadth modify the response of wild bees to habitat loss
Bommarco, R., Biesmeijer, J. C., Meyer, B., Potts, S. G., Pöyry, J., Roberts, S. P. M., Steffan-Dewenter, I. D., & Öckinger, E. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.2221 · Cited by 296 · see citing works
Agroecology: A Review from a Global-Change Perspective
Tomich, T. P., Brodt, S. B., Ferris, H., Galt, R. E., Horwáth, W. R., Kebreab, E., Leveau, J. H. J., Liptzin, D., Lubell, M. N., Mérel, P., et al. (2011) · Annual Review of Environment and Resources · doi:10.1146/annurev-environ-012110-121302 · Cited by 298 · see citing works
A comparison of bee communities of Chicago green roofs, parks and prairies
Tonietto, R. K., Fant, J. B., Ascher, J. S., Ellis, K. E., & Larkin, D. J. (2011) · Landscape and Urban Planning · doi:10.1016/j.landurbplan.2011.07.004 · Cited by 286 · see citing works
Hadley, A. S., & Betts, M. G. (2011) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2011.00205.x · Cited by 277 · 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
Effects 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
Brittain, C., & Potts, S. G. (2011) · Basic and Applied Ecology · doi:10.1016/j.baae.2010.12.004 · Cited by 263 · see citing works
Shackelford, G. E., Steward, P., Benton, T. G., Kunin, W. E., Potts, S. G., Biesmeijer, J. C., & Sait, S. M. (2013) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12040 · Cited by 258 · see citing works
Plant Pollinator Networks along a Gradient of Urbanisation
Geslin, B., Gauzens, B., Thébault, É., & Dajoz, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063421 · Cited by 252 · see citing works
The conservation value of urban green space habitats for Australian native bee communities
Threlfall, C. G., Walker, K. L., Williams, N. S. G., Hahs, A. K., Mata, L., Stork, N. E., & Livesley, S. J. (2015) · Biological Conservation · doi:10.1016/j.biocon.2015.05.003 · Cited by 247 · see citing works
Agricultural Policies Exacerbate Honeybee Pollination Service Supply-Demand Mismatches Across Europe
Breeze, T. D., Vaissière, B., Bommarco, R., Petanidou, T., Seraphides, N., Kozák, L., Scheper, J. A., Biesmeijer, J. C., Kleijn, D., Gyldenkærne, S., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0082996 · Cited by 244 · see citing works
To mow or to mow less: Lawn mowing frequency affects bee abundance and diversity in suburban yards
Lerman, S. B., Contosta, A. R., Milam, J. C., & Bang, C. (2018) · Biological Conservation · doi:10.1016/j.biocon.2018.01.025 · Cited by 244 · 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
Negative effects of pesticides on wild bee communities can be buffered by landscape context
Park, M. G., Blitzer, E. J., Gibbs, J., Losey, J. E., & Danforth, B. N. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.0299 · Cited by 241 · see citing works
Long foraging distances impose high costs on offspring production in solitary bees
Zurbuchen, A., Cheesman, S., Klaiber, J., Müller, A., Hein, S., & Dorn, S. (2010) · Journal of Animal Ecology · doi:10.1111/j.1365-2656.2010.01675.x · Cited by 229 · see citing works
Cang, L., Wang, Y., Zhou, D., & Dong, Y. (2004) · PubMed · Cited by 224 · see citing works
Rader, R., Bartomeus, Í., Tylianakis, J. M., & Laliberté, É. (2014) · Diversity and Distributions · doi:10.1111/ddi.12221 · Cited by 220 · see citing works
Pollination services provided to small and large highbush blueberry fields by wild and managed bees
Isaacs, R., & Kirk, A. K. (2010) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2010.01823.x · Cited by 216 · see citing works
Complementary habitat use by wild bees in agro‐natural landscapes
Mandelik, Y., Winfree, R., Neeson, T. M., & Kremen, C. (2012) · Ecological Applications · doi:10.1890/11-1299.1 · Cited by 214 · see citing works
Self-citationFlowering plants under global pollinator decline
Thomann, M., Imbert, E., Devaux, C., & Cheptou, P. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.04.002 · Cited by 210 · see citing works
Pyrodiversity begets plant–pollinator community diversity
Ponisio, L. C., Wilkin, K., M’Gonigle, L. K., Kulhanek, K., Cook, L., Thorp, R. W., Griswold, T., & Kremen, C. (2016) · Global Change Biology · doi:10.1111/gcb.13236 · Cited by 205 · see citing works
Habitat fragmentation reduces plant progeny quality: a global synthesis
Aguilar, R., Cristóbal‐Pérez, E. J., Balvino‐Olvera, F. J., Aguilar‐Aguilar, M. D. J., Aguirre‐Acosta, N., Ashworth, L., Lobo, J., Martén‐Rodríguez, S., Fuchs, E. J., Sánchez‐Montoya, G., et al. (2019) · Ecology Letters · doi:10.1111/ele.13272 · Cited by 202 · see citing works
Self-citationQuantifying the impact of pesticides on learning and memory in bees
Siviter, H., Koricheva, J., Brown, M. J. F., & Leadbeater, E. (2018) · Journal of Applied Ecology · doi:10.1111/1365-2664.13193 · Cited by 205 · see citing works
Bumblebee family lineage survival is enhanced in high-quality landscapes
Carvell, C., Bourke, A. F. G., Dreier, S., Freeman, S. N., Hulmes, S., Jordan, W. C., Redhead, J. W., Sumner, S., Wang, J., & Heard, M. S. (2017) · Nature · doi:10.1038/nature21709 · Cited by 201 · see citing works
Global malnutrition overlaps with pollinator-dependent micronutrient production
Chaplin‐Kramer, R., Dombeck, E., Gerber, J., Knuth, K. A., Mueller, N. D., Mueller, M. P., Ziv, G., & Klein, A. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.1799 · Cited by 200 · see citing works
Mallinger, R. E., Gibbs, J., & Gratton, C. (2016) · Landscape Ecology · doi:10.1007/s10980-015-0332-z · Cited by 188 · see citing works
Geslin, B., Féon, V. L., Folschweiller, M., Flacher, F., Carmignac, D., Motard, E., Perret, S., & Dajoz, I. (2016) · Ecology and Evolution · doi:10.1002/ece3.2374 · Cited by 187 · see citing works
The effects of ant nests on soil fertility and plant performance: a meta‐analysis
Farji-Brener, A. G., & Werenkraut, V. (2017) · Journal of Animal Ecology · doi:10.1111/1365-2656.12672 · Cited by 185 · see citing works
Contrasting patterns in species and functional‐trait diversity of bees in an agricultural landscape
Forrest, J. R. K., Thorp, R. W., Kremen, C., & Williams, N. M. (2015) · Journal of Applied Ecology · doi:10.1111/1365-2664.12433 · Cited by 183 · see citing works
Floral adaptation and diversification under pollen limitation
Harder, L. D., & Aizen, M. A. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0226 · Cited by 183 · see citing works
Self-citationMeasuring the economic value of pollination services: Principles, evidence and knowledge gaps
Hanley, N. D., Breeze, T. D., Ellis, C., & Goulson, D. (2014) · Ecosystem Services · doi:10.1016/j.ecoser.2014.09.013 · Cited by 182 · see citing works
Supporting Bees in Cities: How Bees Are Influenced by Local and Landscape Features
Ayers, A. C., & Rehan, S. M. (2021) · Insects · doi:10.3390/insects12020128 · Cited by 178 · see citing works
Pollinator body size mediates the scale at which land use drives crop pollination services
Benjamin, F. E., Reilly, J. R., & Winfree, R. (2013) · Journal of Applied Ecology · doi:10.1111/1365-2664.12198 · Cited by 172 · see citing works
Self-citationIsaacs, R., Williams, N. M., Ellis, J. D., Pitts‐Singer, T. L., Bommarco, R., & Vaughan, M. (2017) · Basic and Applied Ecology · doi:10.1016/j.baae.2017.07.003 · Cited by 169 · see citing works
Hillebrand, H., & Kunze, C. (2020) · Ecology Letters · doi:10.1111/ele.13457 · Cited by 167 · see citing works
Theodorou, P., Albig, K., Radzevičiūtė, R., Settele, J., Schweiger, O., Murray, T. E., & Paxton, R. J. (2016) · Functional Ecology · doi:10.1111/1365-2435.12803 · Cited by 164 · see citing works
Ecosystem health assessment: A PSR analysis combining AHP and FCE methods for Jiaozhou Bay, China1
Sun, B., Tang, J., Yu, D., Song, Z., & Wang, P. (2018) · Ocean & Coastal Management · doi:10.1016/j.ocecoaman.2018.10.026 · Cited by 162 · see citing works
Spatial Heterogeneity Regulates Plant-Pollinator Networks across Multiple Landscape Scales
Moreira, E. F., Bôscolo, D., & Viana, B. F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123628 · Cited by 156 · see citing works
A global synthesis of fire effects on pollinators
Carbone, L. M., Tavella, J., Pausas, J. G., & Aguilar, R. (2019) · Global Ecology and Biogeography · doi:10.1111/geb.12939 · Cited by 164 · see citing works
Self-citationJacquemyn, H., Meester, L. D., Jongejans, E., & Honnay, O. (2011) · Journal of Ecology · doi:10.1111/j.1365-2745.2011.01919.x · Cited by 158 · see citing works
Carvell, C., Osborne, J. L., Bourke, A. F. G., Freeman, S. N., Pywell, R. F., & Heard, M. S. (2011) · Ecological Applications · doi:10.1890/10-0677.1 · Cited by 156 · see citing works
Native habitat mitigates feast–famine conditions faced by honey bees in an agricultural landscape
Dolezal, A. G., Clair, A. L. S., Zhang, G., Toth, A. L., & O’Neal, M. E. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1912801116 · Cited by 155 · see citing works
Bees in disturbed habitats use, but do not prefer, alien plants
Williams, N. M., Cariveau, D. P., Winfree, R., & Kremen, C. (2010) · Basic and Applied Ecology · doi:10.1016/j.baae.2010.11.008 · Cited by 152 · see citing works
Self-citationEffects of land management on the abundance and richness of spiders (Araneae): A meta-analysis
Prieto‐Benítez, S., & Méndez, M. (2010) · Biological Conservation · doi:10.1016/j.biocon.2010.11.024 · Cited by 152 · see citing works
Landscape elements as potential barriers and corridors for bees, wasps and parasitoids
Krewenka, K. M., Holzschuh, A., Tscharntke, T., & Dormann, C. F. (2011) · Biological Conservation · doi:10.1016/j.biocon.2011.03.014 · Cited by 146 · 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
Urban gardens promote bee foraging over natural habitats and plantations
Kaluza, B. F., Wallace, H., Heard, T. A., Klein, A., & Leonhardt, S. D. (2016) · Ecology and Evolution · doi:10.1002/ece3.1941 · Cited by 146 · see citing works
Spivak, M. S., Mader, E., Vaughan, M., & Euliss, N. H. (2010) · Environmental Science & Technology · doi:10.1021/es101468w · Cited by 141 · see citing works
Habitat restoration benefits wild bees: A meta‐analysis
Tonietto, R. K., & Larkin, D. J. (2017) · Journal of Applied Ecology · doi:10.1111/1365-2664.13012 · Cited by 139 · see citing works
A global meta-analyses of the response of multi-taxa diversity to grazing intensity in grasslands
Wang, C., & Tang, Y. (2019) · Environmental Research Letters · doi:10.1088/1748-9326/ab4932 · Cited by 138 · see citing works
Economic gain, stability of pollination and bee diversity decrease from southern to northern Europe
Leonhardt, S. D., Gallai, N., Garibaldi, L. A., Kuhlmann, M. T., & Klein, A. (2013) · Basic and Applied Ecology · doi:10.1016/j.baae.2013.06.003 · Cited by 139 · see citing works
Linking Land Cover Data and Crop Yields for Mapping and Assessment of Pollination Services in Europe
Zulian, G., Maes, J., & Paracchini, M. L. (2013) · Land · doi:10.3390/land2030472 · Cited by 138 · see citing works
Pollinator assemblages on dandelions and white clover in urban and suburban lawns
Larson, J., Kesheimer, A., & Potter, D. (2014) · Journal of Insect Conservation · doi:10.1007/s10841-014-9694-9 · Cited by 137 · see citing works
Graß, I., Jauker, B., Steffan-Dewenter, I. D., Tscharntke, T., & Jauker, F. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0631-2 · Cited by 142 · see citing works
Solitary bee abundance and species richness in dynamic agricultural landscapes
Féon, V. L., Burel, F., Chifflet, R., Henry, M., Ricroch, A., Vaissière, B., & Baudry, J. (2011) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2011.06.020 · Cited by 136 · see citing works
Harrison, T., Gibbs, J., & Winfree, R. (2017) · Global Change Biology · doi:10.1111/gcb.13921 · Cited by 134 · see citing works
Self-citationPecenka, J., Ingwell, L. L., Foster, R. E., Krupke, C. H., & Kaplan, I. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2108429118 · Cited by 134 · see citing works
Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic Rainforest
Ferreira, P. A., Bôscolo, D., Carvalheiro, L. G., Biesmeijer, J. C., da Rocha, P. L. B., & Viana, B. F. (2015) · Landscape Ecology · doi:10.1007/s10980-015-0231-3 · Cited by 134 · see citing works
Vulnerability of honey bee queens to heat-induced loss of fertility
McAfee, A., Chapman, A., Higo, H. A., Underwood, R. M., Milone, J. P., Foster, L. J., Guarna, M. M., Tarpy, D. R., & Pettis, J. S. (2020) · Nature Sustainability · doi:10.1038/s41893-020-0493-x · Cited by 132 · see citing works
Jeanneret, P., Aviron, S., Alignier, A., Lavigne, C., Helfenstein, J., Herzog, F., Kay, S., & Petit, S. (2021) · Landscape Ecology · doi:10.1007/s10980-021-01248-0 · Cited by 141 · see citing works
Archer, C. R., Pirk, C. W. W., Carvalheiro, L. G., & Nicolson, S. W. (2014) · Oikos · doi:10.1111/j.1600-0706.2013.00949.x · Cited by 129 · see citing works
Meta‐analysis: A need for well‐defined usage in ecology and conservation biology
Vetter, D., Rücker, G., & Storch, I. (2013) · Ecosphere · doi:10.1890/es13-00062.1 · Cited by 124 · see citing works
Predicting bee community responses to land-use changes: Effects of geographic and taxonomic biases
Palma, A. D., Abrahamczyk, S., Aizen, M. A., Albrecht, M., Basset, Y., Bates, A. J., Blake, R. J., Boutin, C., Bugter, R. J. F., Connop, S. P., et al. (2016) · Scientific Reports · doi:10.1038/srep31153 · Cited by 126 · see citing works
Self-citationLandscape simplification decreases wild bee pollination services to strawberry
Connelly, H. L., Poveda, K., & Loeb, G. M. (2015) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2015.05.004 · Cited by 125 · see citing works
Williams, N. M., & Winfree, R. (2013) · Biological Conservation · doi:10.1016/j.biocon.2012.12.035 · Cited by 123 · see citing works
Self-citationMurray, T. E., Coffey, M. F., Kehoe, E., & Horgan, F. G. (2013) · Biological Conservation · doi:10.1016/j.biocon.2012.10.021 · Cited by 123 · see citing works
Food in a row: urban trees offer valuable floral resources to pollinating insects
Somme, L., Moquet, L., Quinet, M., Vanderplanck, M., Michez, D., Lognay, G. C., & Jacquemart, A. (2016) · Urban Ecosystems · doi:10.1007/s11252-016-0555-z · Cited by 123 · see citing works
Impact of landscape alteration and invasions on pollinators: a meta‐analysis
Montero‐Castaño, A., & Vilà, M. (2012) · Journal of Ecology · doi:10.1111/j.1365-2745.2012.01968.x · Cited by 122 · see citing works
González‐Varo, J. P., Arroyo, J., & Aparicio, A. (2009) · Biological Conservation · doi:10.1016/j.biocon.2009.01.017 · Cited by 122 · see citing works
- Authors
- Winfree, R., Aguilar, R., Vázquez, D. P., LeBuhn, G., & Aizen, M. A.
- Affiliations
- University of California, Berkeley (US)
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- San Francisco State University (US)
- Universidad Nacional del Comahue (AR)
- Corresponding author
- Winfree, Rachael
- Venue
- Ecology
- Publisher
- Wiley
- Published
- 2009-08
- Volume
- 90
- Issue
- 8
- Pages
- 2068-2076
- ISSN
- 0012-9658 (ISSN-L)
- 1939-9170
- OpenAlex
- W2146145096
- Cited by
- 1,050
- References
- 57
- Citations by year
- 2026: 39 · 2025: 59 · 2024: 65 · 2023: 57 · 2022: 73 · 2021: 70 · 2020: 93 · 2019: 83 · 2018: 72 · 2017: 71 · 2016: 80 · 2015: 50 · 2014: 68 · 2013: 52 · 2012: 44
- FWCI
- 3.76
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Ecology (publishedVersion)
- PubMed (publishedVersion)
- CONICET Digital (CONICET) (submittedVersion, cc-by-nc-sa)
- Funders
- National Academy of Sciences
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and animal studies
- Physical Sciences › Environmental Science › Nature and Landscape Conservation › Ecology and Vegetation Dynamics Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
- Keywords
- bees, pollinator decline, human disturbance, habitat loss, habitat fragmentation, land use change, bee abundance, bee species richness, grazing, logging, pollination
- MeSH terms
- Animals, Bees, Behavior, Animal, Human Activities, Biodiversity
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