in

Honey bee hives decrease wild bee abundance, species richness, and fruit count on farms regardless of wildflower strips

  • 1.

    Steffan-Dewenter, I., Potts, S. G. & Packer, L. Pollinator diversity and crop pollination services are at risk. Trends Ecol. Evol. 20, 651–652 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  • 2.

    Aizen, M. A., Garibaldi, L. A., Cunningham, S. A. & Klein, A. M. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18, 1572–1575 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 3.

    Garibaldi, L. A., Aizen, M. A., Klein, A. M., Cunningham, S. A. & Harder, L. D. Global growth and stability of agricultural yield decrease with pollinator dependence. Proc. Natl. Acad. Sci. 108, 5909–5914 (2011).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 4.

    Goulson, D. Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Evol. Syst. 34, 1–26 (2003).

    Article  Google Scholar 

  • 5.

    Paini, D. Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: A review. Aust. Ecol. 29, 399–407 (2004).

    Article  Google Scholar 

  • 6.

    Aslan, C. E., Liang, C. T., Galindo, B., Kimberly, H. & Topete, W. The role of honey bees as pollinators in natural areas. Nat. Areas J. 36, 478–489 (2016).

    Article  Google Scholar 

  • 7.

    Mallinger, R. E., Gaines-Day, H. R. & Gratton, C. Do managed bees have negative effects on wild bees? A systematic review of the literature. PLoS ONE 12, e0189268 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 8.

    Wignall, V. R. et al. Seasonal variation in exploitative competition between honeybees and bumblebees. Oecologia 192, 351–361 (2020).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 9.

    Thomson, D. M. Detecting the effects of introduced species: A case study of competition between Apis and Bombus. Oikos 114, 407–418 (2006).

    Article  Google Scholar 

  • 10.

    Franco, E. L., Aguiar, C. M. & Ferreiraz, V. S. Plant use and niche overlap between the introduced honey bee (Apis mellifera) and the native bumblebee (Bombus atratus) (Hymenoptera: Apidae) in an area of tropical mountain vegetation in northeastern Brazil. Sociobiology 53, 141–150 (2009).

    Google Scholar 

  • 11.

    Herbertsson, L., Lindström, S. A., Rundlöf, M., Bommarco, R. & Smith, H. G. Competition between managed honeybees and wild bumblebees depends on landscape context. Basic Appl. Ecol. 17, 609–616 (2016).

    Article  Google Scholar 

  • 12.

    Thomson, D. M. Local bumble bee decline linked to recovery of honey bees, drought effects on floral resources. Ecol. Lett. 19, 1247–1255 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 13.

    Greenleaf, S. S. & Kremen, C. Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc. Natl. Acad. Sci. 103, 13890–13895 (2006).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 14.

    Badano, E. I. & Vergara, C. H. Potential negative effects of exotic honey bees on the diversity of native pollinators and yield of highland coffee plantations. Agric. For. Entomol. 13, 365–372 (2011).

    Article  Google Scholar 

  • 15.

    Brittain, C., Williams, N., Kremen, C. & Klein, A.-M. Synergistic effects of non-Apis bees and honey bees for pollination services. Proc. R. Soc. B Biol. Sci. 280, 20122767 (2013).

    Article  Google Scholar 

  • 16.

    Müller, H. T. Interaction Between Bombus terrestris and Honeybees in Red Clover Fields Reduces Abundance of Other Bumblebees and Red Clover Yield and Honeybees in Red Clover Fields Reduces Abundance of Other Bumblebees and Red Clover Yield (Norwegian University of Life Sciences, Ås, 2016).

    Google Scholar 

  • 17.

    Grass, I. et al. Pollination limitation despite managed honeybees in South African macadamia orchards. Agric. Ecosyst. Environ. 260, 11–18 (2018).

    Article  Google Scholar 

  • 18.

    hUallacháin, D. Ó. (United Nations Convention to Combat Desertification, Bonn, Germany, 2017).

  • 19.

    Vaughan, M. & Skinner, M. Using 2014 farm bill programs for pollinator conservation. USDA Biol. Tech. Note 78, 2nd Ed. (2015).

  • 20.

    Vaughan, M. & Skinner, M. Using Farm Bill programs for pollinator conservation. USDA-NRCS National Plant Data Center, USDA Biol. Tech. Note 78 (2008).

  • 21.

    FSA. CP42 pollinator habitat: Establishing and supporting diverse pollinator-friendly habitat. (Farm Service Agency, U.S. Department of Agriculture, Washington, D.C., 2013).

  • 22.

    Venturini, E. M., Drummond, F. A., Hoshide, A. K., Dibble, A. C. & Stack, L. B. Pollination reservoirs for wild bee habitat enhancement in cropping systems: a review. Agroecol. Sustain. Food Syst. 41, 101–142 (2017).

    Article  Google Scholar 

  • 23.

    Wood, T. J., Holland, J. M., Hughes, W. O. & Goulson, D. Targeted agri-environment schemes significantly improve the population size of common farmland bumblebee species. Mol. Ecol. 24, 1668–1680 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  • 24.

    Haaland, C. & Gyllin, M. Butterflies and bumblebees in greenways and sown wildflower strips in southern Sweden. J. Insect Conserv. 14, 125–132 (2010).

    Article  Google Scholar 

  • 25.

    Ponisio, L. C., M’Gonigle, L. K. & Kremen, C. On-farm habitat restoration counters biotic homogenization in intensively managed agriculture. Glob. Change Biol. 22, 704–715 (2016).

    ADS  Article  Google Scholar 

  • 26.

    Dolezal, A. G., Clair, A. L. S., Zhang, G., Toth, A. L. & O’Neal, M. E. Native habitat mitigates feast–famine conditions faced by honey bees in an agricultural landscape. Proc. Natl. Acad. Sci. 116, 25147–25155 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    Venturini, E., Drummond, F., Hoshide, A., Dibble, A. & Stack, L. B. Pollination reservoirs in lowbush blueberry (Ericales: Ericaceae). J. Econ. Entomol. 110, 333–346 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 28.

    Morandin, L. A. & Kremen, C. Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecol. Appl. 23, 829–839 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  • 29.

    Blaauw, B. R. & Isaacs, R. Flower plantings increase wild bee abundance and the pollination services provided to a pollination-dependent crop. J. Appl. Ecol. 51, 890–898 (2014).

    Article  Google Scholar 

  • 30.

    Feltham, H., Park, K., Minderman, J. & Goulson, D. Experimental evidence of the benefit of wild flower strips to crop pollination. Ecol. Evolut. 5, 3523–3530 (2015).

    Article  Google Scholar 

  • 31.

    Gross, C. & Mackay, D. Honeybees reduce fitness in the pioneer shrub Melastoma affine (Melastomataceae). Biol. Cons. 86, 169–178 (1998).

    Article  Google Scholar 

  • 32.

    do Carmo, R. M., Franceschinelli, E. V. & da Silveira, F. A. Introduced honeybees (Apis mellifera) reduce pollination success without affecting the floral resource taken by native pollinators. Biotropica 36, 371–376 (2004).

    Google Scholar 

  • 33.

    Bruckman, D. & Campbell, D. R. Floral neighborhood influences pollinator assemblages and effective pollination in a native plant. Oecologia 176, 465–476 (2014).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 34.

    Garibaldi, L. A. et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611 (2013).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 35.

    Carvalheiro, L. G. et al. Natural and within-farmland biodiversity enhances crop productivity. Ecol. Lett. 14, 251–259 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 36.

    Jönsson, A. M. et al. Modelling the potential impact of global warming on Ips typographus voltinism and reproductive diapause. Clim. Change 109, 695–718 (2011).

    ADS  Article  Google Scholar 

  • 37.

    Scheper, J. et al. Local and landscape-level floral resources explain effects of wildflower strips on wild bees across four European countries. J. Appl. Ecol. 52, 1165–1175 (2015).

    Article  Google Scholar 

  • 38.

    Krimmer, E., Martin, E. A., Krauss, J., Holzschuh, A. & Steffan-Dewenter, I. Size, age and surrounding semi-natural habitats modulate the effectiveness of flower-rich agri-environment schemes to promote pollinator visitation in crop fields. Agric. Ecosyst. Environ. 284, 106590 (2019).

    Article  Google Scholar 

  • 39.

    Klein, A. M. et al. Wild pollination services to California almond rely on semi-natural habitat. J. Appl. Ecol. 49, 723–732 (2012).

    Google Scholar 

  • 40.

    Grab, H., Poveda, K., Danforth, B. & Loeb, G. Landscape context shifts the balance of costs and benefits from wildflower borders on multiple ecosystem services. Proc. R. Soc. B Biol. Sci. 285, 20181102 (2018).

    Article  Google Scholar 

  • 41.

    Prendergast, K. S., Menz, M. H., Dixon, K. W. & Bateman, P. W. The relative performance of sampling methods for native bees: An empirical test and review of the literature. Ecosphere 11, e03076 (2020).

    Article  Google Scholar 

  • 42.

    Cane, J. H., Minckley, R. L. & Kervin, L. J. Sampling bees (Hymenoptera: Apiformes) for pollinator community studies: pitfalls of pan-trapping. J. Kansas Entomol. Soc. 73, 225–231 (2000).

    Google Scholar 

  • 43.

    O’Connor, R. S. et al. Monitoring insect pollinators and flower visitation: The effectiveness and feasibility of different survey methods. Methods Ecol. Evol. 10, 2129–2140. https://doi.org/10.1111/2041-210x.13292 (2019).

    Article  Google Scholar 

  • 44.

    Graystock, P., Blane, E. J., McFrederick, Q. S., Goulson, D. & Hughes, W. O. Do managed bees drive parasite spread and emergence in wild bees?. Int. J. Parasitol. Parasites Wildlife 5, 64–75 (2016).

    Article  Google Scholar 

  • 45.

    Alger, S. A., Burnham, P. A., Boncristiani, H. F. & Brody, A. K. RNA virus spillover from managed honeybees (Apis mellifera) to wild bumblebees (Bombus spp.). PloS One 14, e0217822 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 46.

    Schaffer, W. M. et al. Competition, foraging energetics, and the cost of sociality in three species of bees. Ecology 60, 976–987 (1979).

    Article  Google Scholar 

  • 47.

    Pleasants, J. M. Bumblebee response to variation in nectar availability. Ecology 62, 1648–1661 (1981).

    Article  Google Scholar 

  • 48.

    Ginsberg, H. S. Foraging ecology of bees in an old field. Ecology 64, 165–175 (1983).

    Article  Google Scholar 

  • 49.

    Schaffer, W. M. et al. Competition for nectar between introduced honey bees and native North American bees and ants. Ecology 64, 564–577 (1983).

    Article  Google Scholar 

  • 50.

    Gross, C. L. The effect of introduced honeybees on native bee visitation and fruit-set in Dillwynia juniperina (Fabaceae) in a fragmented ecosystem. Biol. Cons. 102, 89–95 (2001).

    Article  Google Scholar 

  • 51.

    Hudewenz, A. & Klein, A.-M. Competition between honey bees and wild bees and the role of nesting resources in a nature reserve. J. Insect Conserv. 17, 1275–1283 (2013).

    Article  Google Scholar 

  • 52.

    Johnson, L. K. & Hubbell, S. P. Aggression and competition among stingless bees: Field studies. Ecology 55, 120–127 (1974).

    Article  Google Scholar 

  • 53.

    Winfree, R., Fox, J. W., Williams, N. M., Reilly, J. R. & Cariveau, D. P. Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol. Lett. 18, 626–635 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  • 54.

    Woodcock, B. A. et al. Meta-analysis reveals that pollinator functional diversity and abundance enhance crop pollination and yield. Nat. Commun. 10, 1–10 (2019).

    ADS  CAS  Article  Google Scholar 

  • 55.

    Garibaldi, L. A. et al. From research to action: enhancing crop yield through wild pollinators. Front. Ecol. Environ. 12, 439–447 (2014).

    Article  Google Scholar 

  • 56.

    Connelly, H., Poveda, K. & Loeb, G. Landscape simplification decreases wild bee pollination services to strawberry. Agric. Ecosyst. Environ. 211, 51–56 (2015).

    Article  Google Scholar 

  • 57.

    MacInnis, G. & Forrest, J. R. K. Pollination by wild bees yields larger strawberries than pollination by honey bees. J. Appl. Ecol. 56, 824–832. https://doi.org/10.1111/1365-2664.13344 (2019).

    Article  Google Scholar 

  • 58.

    Seeley, T. D. Social foraging by honeybees: how colonies allocate foragers among patches of flowers. Behav. Ecol. Sociobiol. 19, 343–354 (1986).

    Article  Google Scholar 

  • 59.

    Bänsch, S., Tscharntke, T., Gabriel, D. & Westphal, C. Crop pollination services: complementary resource use by social vs solitary bees facing crops with contrasting flower supply. J. Appl. Ecol. https://doi.org/10.1111/1365-2664.13777 (2020).

  • 60.

    Nye, W. P. & Anderson, J. L. Insect pollinators frequenting strawberry blossoms and the effect of honey bees on yield and fruit quality. J. Am. Soc. Horticult. Sci. 99, 40 (1974).

    Google Scholar 

  • 61.

    De Oliveira, D., Savoie, L. & Vincent, C. in VI International Symposium on Pollination 288, 420–424 (1990).

  • 62.

    Chagnon, M., Gingras, J. & DeOliveira, D. Complementary aspects of strawberry pollination by honey and indigenous bees (Hymenoptera). J. Econ. Entomol. 86, 416–420 (1993).

    Article  Google Scholar 

  • 63.

    Horth, L. & Campbell, L. A. Supplementing small farms with native mason bees increases strawberry size and growth rate. J. Appl. Ecol. 55, 591–599 (2018).

    Article  Google Scholar 

  • 64.

    Pfister, S. C. et al. Dominance of cropland reduces the pollen deposition from bumble bees. Sci. Rep. 8, 13873 (2018).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 65.

    Artz, D. R. & Nault, B. A. Performance of Apis mellifera, Bombus impatiens, and Peponapis pruinosa (Hymenoptera: Apidae) as pollinators of pumpkin. J. Econ. Entomol. 104, 1153–1161 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 66.

    Petersen, J., Huseth, A. & Nault, B. Evaluating pollination deficits in pumpkin production in New York. Environ. Entomol. 43, 1247–1253 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 67.

    McGrady, C., Troyer, R. & Fleischer, S. Wild bee visitation rates exceed pollination thresholds in commercial cucurbita agroecosystems. J. Econ. Entomol. 113, 562–574 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 68.

    Geslin, B. et al. Advances in Ecological Research Vol. 57, 147–199 (Elsevier, San Diego, 2017).

    Google Scholar 

  • 69.

    Steffan-Dewenter, I. & Tscharntke, T. Resource overlap and possible competition between honey bees and wild bees in central Europe. Oecologia 122, 288–296 (2000).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 70.

    Torné-Noguera, A., Rodrigo, A., Osorio, S. & Bosch, J. Collateral effects of beekeeping: Impacts on pollen-nectar resources and wild bee communities. Basic Appl. Ecol. 17, 199–209 (2016).

    Article  Google Scholar 

  • 71.

    Free, J. B. Insect Pollination of Crops (Academic Press, London, 1970).

    Google Scholar 

  • 72.

    Delaplane, K. S., Mayer, D. R. & Mayer, D. F. Crop pollination by bees. (CABI, 2000).

  • 73.

    Phillips, B. Current honey bee and bumble bee stocking information. Michigan State University, MSU Extension: Pollination (2019). https://www.canr.msu.edu/news/current_honey_bee_stocking_information_and_an_introduction_to_commercial_bu.

  • 74.

    Angelella, G. M. & O’Rourke, M. E. Pollinator habitat establishment after organic and no-till seedbed preparation methods. HortScience 52, 1349–1355 (2017).

    CAS  Article  Google Scholar 

  • 75.

    Blaauw, B. R. & Isaacs, R. Larger patches of diverse floral resources increase insect pollinator density, diversity, and their pollination of native wildflowers. Basic Appl. Ecol. 15, 701–711 (2014).

    Article  Google Scholar 

  • 76.

    Klatt, B. K. et al. Bee pollination improves crop quality, shelf life and commercial value. Proc. R. Soc. B Biol. Sci. 281, 20132440 (2014).

    Article  Google Scholar 

  • 77.

    King, S. R., Davis, A. R. & Wehner, T. C. Classical genetics and traditional breeding. In Genetics, Genomics, and Breeding of Cucurbits (eds. Wang, Y.-H. et al.) 61–92 (CRC Press, 2012).

  • 78.

    Kronenberg, H. G. Poor fruit setting in strawberries. I. Euphytica 8, 47–57 (1959).

    Article  Google Scholar 

  • 79.

    Kronenberg, H. G., Braak, J. & Zeilinga, A. Poor fruit setting in strawberries. II. Euphytica 8, 245–251 (1959).

    Article  Google Scholar 

  • 80.

    Robinson, R. W. & Decker-Walters, D. S. Cucurbits (CAB Intl., New York, 1997).

    Google Scholar 

  • 81.

    R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2019).

  • 82.

    Magnusson, A. et al. Package ‘glmmTMB’. R Package Version 0.2. 0 (2017).

  • 83.

    Bates, D., Sarkar, D., Bates, M. D. & Matrix, L. The lme4 package. R Package Version 2, 74 (2007).

    Google Scholar 

  • 84.

    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. Emmeans: Estimated marginal means, aka least-squares means. R Package Version 1, 3 (2018).

    Google Scholar 

  • 85.

    Wien, H., Stapleton, S., Maynard, D., McClurg, C. & Riggs, D. Flowering, sex expression, and fruiting of pumpkin (Cucurbita sp.) cultivars under various temperatures in greenhouse and distant field trials. HortScience 39, 239–242 (2004).

    Article  Google Scholar 


  • Source: Ecology - nature.com

    New fiber optic temperature sensing approach to keep fusion power plants running

    Reducing inequality across the globe and on campus