Greater bee diversity is needed to maintain crop pollination over time
Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).CAS
PubMed
Article
Google Scholar
Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108 (2012).CAS
PubMed
Article
Google Scholar
Potts, S. G. et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010).PubMed
Article
Google Scholar
Kennedy, C. M. et al. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599 (2013).PubMed
Article
Google Scholar
Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. Proc. Natl Acad. Sci. USA 108, 662–667 (2011).CAS
PubMed
PubMed Central
Article
Google Scholar
Xu, S. et al. Species richness promotes ecosystem carbon storage: evidence from biodiversity-ecosystem functioning experiments. Proc. Biol. Sci. 287, 20202063 (2020).CAS
PubMed
PubMed Central
Google Scholar
Jochum, M. et al. The results of biodiversity–ecosystem functioning experiments are realistic. Nat. Ecol. Evol. 4, 1485–1494 (2020).PubMed
Article
Google Scholar
Isbell, F. et al. High plant diversity is needed to maintain ecosystem services. Nature 477, 199–202 (2011).CAS
PubMed
Article
Google Scholar
Barnes, A. D. et al. Species richness and biomass explain spatial turnover in ecosystem functioning across tropical and temperate ecosystems. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150279 (2016).Article
Google Scholar
Manning, P. & Cutler, G. C. Ecosystem functioning is more strongly impaired by reducing dung beetle abundance than by reducing species richness. Agric. Ecosyst. Environ. 264, 9–14 (2018).Article
Google Scholar
van der Plas, F. Biodiversity and ecosystem functioning in naturally assembled communities. Biol. Rev. Camb. Philos. Soc. 94, 1220–1245 (2019).PubMed
Google Scholar
Blüthgen, N. & Klein, A.-M. Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic Appl. Ecol. 12, 282–291 (2011).Article
Google Scholar
Loreau, M. Biodiversity and ecosystem functioning: a mechanistic model. Proc. Natl Acad. Sci. USA 95, 5632–5636 (1998).CAS
PubMed
PubMed Central
Article
Google Scholar
Loreau, M. et al. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808 (2001).CAS
PubMed
Article
Google Scholar
Tilman, D. The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80, 1455–1474 (1999).
Google Scholar
Duffy, J. E., Godwin, C. M. & Cardinale, B. J. Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549, 261–264 (2017).CAS
PubMed
Article
Google Scholar
Gonzalez, A. et al. Scaling-up biodiversity-ecosystem functioning research. Ecol. Lett. 23, 757–776 (2020).PubMed
PubMed Central
Article
Google Scholar
Garibaldi, L. A. et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 340, 1608–1611 (2013).Article
CAS
Google Scholar
Greenop, A., Woodcock, B. A., Wilby, A., Cook, S. M. & Pywell, R. F. Functional diversity positively affects prey suppression by invertebrate predators: a meta-analysis. Ecology 99, 1771–1782 (2018).PubMed
Article
Google Scholar
McGill, B. J. et al. Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol. Lett. 10, 995–1015 (2007).PubMed
Article
Google Scholar
Genung, M. A. et al. The relative importance of pollinator abundance and species richness for the temporal variance of pollination services. Ecology 98, 1807–1816 (2017).PubMed
Article
Google Scholar
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
Google Scholar
Kleijn, D. et al. Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat. Commun. 6, 7414 (2015).Smith, M. D. & Knapp, A. K. Dominant species maintain ecosystem function with non-random species loss. Ecol. Lett. 6, 509–517 (2003).Article
Google Scholar
Lohbeck, M., Bongers, F., Martinez-Ramos, M. & Poorter, L. The importance of biodiversity and dominance for multiple ecosystem functions in a human-modified tropical landscape. Ecology 97, 2772–2779 (2016).PubMed
Article
Google Scholar
Balvanera, P., Kremen, C. & Martínez-Ramos, M. Applying community structure analysis to ecosystem function: examples from pollination and carbon storage. Ecol. Appl. 15, 360–375 (2005).Article
Google Scholar
Maureaud, A. et al. Biodiversity–ecosystem functioning relationships in fish communities: biomass is related to evenness and the environment, not to species richness. Proc. Biol. Sci. 286, 20191189 (2019).PubMed
PubMed Central
Google Scholar
Genung, M. A., Fox, J. & Winfree, R. Species loss drives ecosystem function in experiments, but in nature the importance of species loss depends on dominance. Glob. Ecol. Biogeogr. 29, 1531–1541 (2020).Article
Google Scholar
Potts, S. G., Vulliamy, B., Dafni, A., Ne’eman, G. & Willmer, P. Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84, 2628–2642 (2003).Article
Google Scholar
Tilman, D., Isbell, F. & Cowles, J. M. Biodiversity and ecosystem functioning. Annu. Rev. Ecol. Evol. Syst. 45, 471–493 (2014).Article
Google Scholar
Craven, D. et al. A cross-scale assessment of productivity–diversity relationships. Glob. Ecol. Biogeogr. 29, 1940–1955 (2020).Article
Google Scholar
Thompson, P. L., Isbell, F., Loreau, M., O’Connor, M. I. & Gonzalez, A. The strength of the biodiversity–ecosystem function relationship depends on spatial scale. Proc. Biol. Sci. 285, 20180038 (2018).PubMed
PubMed Central
Google Scholar
Qiu, J. & Cardinale, B. J. Scaling up biodiversity–ecosystem function relationships across space and over time. Ecology 101, e03166 (2020).Winfree, R. et al. Species turnover promotes the importance of bee diversity for crop pollination at regional scales. Science 359, 791–793 (2018).CAS
PubMed
Article
Google Scholar
Albrecht, J. et al. Species richness is more important for ecosystem functioning than species turnover along an elevational gradient. Nat. Ecol. Evol. 5, 1582–1593 (2021).PubMed
Article
Google Scholar
Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl Acad. Sci. USA 96, 1463–1468 (1999).CAS
PubMed
PubMed Central
Article
Google Scholar
Shanafelt, D. W. et al. Biodiversity, productivity, and the spatial insurance hypothesis revisited. J. Theor. Biol. 380, 426–435 (2015).PubMed
PubMed Central
Article
Google Scholar
Naeem, S. & Li, S. Biodiversity enhances ecosystem reliability. Nature 390, 507–509 (1997).CAS
Article
Google Scholar
Tilman, D. Biodiversity: population versus ecosystem stability. Ecology 77, 350–363 (1996).Article
Google Scholar
Herrera, C. M. Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biol. J. Linn. Soc. Lond. 35, 95–125 (1988).Article
Google Scholar
McCormack, M. L., Adams, T. S., Smithwick, E. A. H. & Eissenstat, D. M. Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95, 2224–2235 (2014).PubMed
Article
Google Scholar
Wright, K. W., Vanderbilt, K. L., Inouye, D. W., Bertelsen, C. D. & Crimmins, T. M. Turnover and reliability of flower communities in extreme environments: insights from long-term phenology data sets. J. Arid Environ. 115, 27–34 (2015).Article
Google Scholar
Tylianakis, J. M. et al. Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. PLoS Biol. 6, e122 (2008).PubMed Central
Article
CAS
Google Scholar
Kremen, C. Managing ecosystem services: what do we need to know about their ecology? Ecol. Lett. 8, 468–479 (2005).PubMed
Article
Google Scholar
Iserbyt, S. & Rasmont, P. The effect of climatic variation on abundance and diversity of bumblebees: a ten years survey in a mountain hotspot. Ann. Soc. Entomol. Fr. 48, 261–273 (2012).Article
Google Scholar
Houlahan, J. E. et al. Compensatory dynamics are rare in natural ecological communities. Proc. Natl Acad. Sci. USA 104, 3273–3277 (2007).CAS
PubMed
PubMed Central
Article
Google Scholar
Ernest, S. K. M. & Brown, J. H. Homeostasis and compensation: the role of species and resources in ecosystem stability. Ecology 82, 2118–2132 (2001).Article
Google Scholar
Kremen, C., Williams, N. M. & Thorp, R. W. Crop pollination from native bees at risk from agricultural intensification. Proc. Natl Acad. Sci. USA 99, 16812–16816 (2002).CAS
PubMed
PubMed Central
Article
Google Scholar
Allan, E. et al. More diverse plant communities have higher functioning over time due to turnover in complementary dominant species. Proc. Natl Acad. Sci. USA 108, 17034–17039 (2011).CAS
PubMed
PubMed Central
Article
Google Scholar
Tilman, D., Reich, P. B. & Knops, J. M. H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).CAS
PubMed
Article
Google Scholar
Awasthi, A., Singh, M., Soni, S. K., Singh, R. & Kalra, A. Biodiversity acts as insurance of productivity of bacterial communities under abiotic perturbations. ISME J. 8, 2445–2452 (2014).PubMed
PubMed Central
Article
Google Scholar
Tuck, S. L. et al. The value of biodiversity for the functioning of tropical forests: Insurance effects during the first decade of the Sabah biodiversity experiment. Proc. Biol. Sci. 283, 20161451 (2016).PubMed
PubMed Central
Google Scholar
Isbell, F. et al. Quantifying effects of biodiversity on ecosystem functioning across times and places. Ecol. Lett. 21, 763–778 (2018).PubMed
PubMed Central
Article
Google Scholar
Reich, P. B. et al. Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592 (2012).CAS
PubMed
Article
Google Scholar
Perry, C. J., Søvik, E., Myerscough, M. R. & Barron, A. B. Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc. Natl Acad. Sci. USA 112, 3427–3432 (2015).CAS
PubMed
PubMed Central
Article
Google Scholar
Benjamin, F. E. & Winfree, R. Lack of pollinators limits fruit production in commercial blueberry (Vaccinium corymbosum). Environ. Entomol. 43, 1574–1583 (2014).PubMed
Article
Google Scholar
Isaacs, R. & Kirk, A. K. Pollination services provided to small and large highbush blueberry fields by wild and managed bees. J. Appl. Ecol. 47, 841–849 (2010).Article
Google Scholar
Zhang, Y., Chen, H. Y. H. & Reich, P. B. Forest productivity increases with evenness, species richness and trait variation: a global meta-analysis. J. Ecol. 100, 742–749 (2012).Article
Google Scholar
Baumgärtner, S. The insurance value of biodiversity in the provision of ecosystem services. Nat. Resour. Model. 20, 87–127 (2007).Article
Google Scholar
Manning, P. et al. in Advances in Ecological Research (eds Eisenhauer, N., Bohan, D. A. & Dumbrell, A. J.) 323–356 (Academic Press, 2019).Naeem, S. Species redundancy and ecosystem reliability. Conserv. Biol. 12, 39–45 (1998).Article
Google Scholar
CaraDonna, P. J. et al. Interaction rewiring and the rapid turnover of plant–pollinator networks. Ecol. Lett. 20, 385–394 (2017).PubMed
Article
Google Scholar
Gonzalez, A. & Loreau, M. The causes and consequences of compensatory dynamics in ecological communities. Annu. Rev. Ecol. Evol. Syst. 40, 393–414 (2009).Article
Google Scholar
Liu, D., Chang, P.-H. S., Power, S. A., Bell, J. N. B. & Manning, P. Changes in plant species abundance alter the multifunctionality and functional space of heathland ecosystems. New Phytol. 232, 1238–1249 (2021).CAS
PubMed
Article
Google Scholar
Buschke, F. T., Hagan, J. G., Santini, L. & Coetzee, B. W. T. Random population fluctuations bias the Living Planet Index. Nat. Ecol. Evol. 5, 1145–1152 (2021).PubMed
Article
Google Scholar
Almond, R. E. A., Grooten, M. & Peterson, T. Living Planet Report 2020: Bending the Curve of Biodiversity Loss (World Wildlife Fund, 2020).Collen, B. et al. Monitoring change in vertebrate abundance: the Living Planet Index. Conserv. Biol. 23, 317–327 (2009).PubMed
Article
Google Scholar
Wagner, D. L. Insect declines in the Anthropocene. Annu. Rev. Entomol. 65, 457–480 (2020).CAS
PubMed
Article
Google Scholar
Stanghellini, M. S., Ambrose, J. T. & Schultheis, J. R. The effects of honey bee and bumble bee pollination on fruit set and abortion of cucumber and watermelon. Am. Bee. J. 137, 386–391 (1997).
Google Scholar
Winfree, R., Williams, N. M., Dushoff, J. & Kremen, C. Native bees provide insurance against ongoing honey bee losses. Ecol. Lett. 10, 1105–1113 (2007).PubMed
Article
Google Scholar
Tamburini, G., Bommarco, R., Kleijn, D., van der Putten, W. H. & Marini, L. Pollination contribution to crop yield is often context-dependent: a review of experimental evidence. Agric. Ecosyst. Environ. 280, 16–23 (2019).Article
Google Scholar
Stanghellini, M. S., Ambrose, J. T. & Schultheis, J. R. Seed production in watermelon: a comparison between two commercially available pollinators. HortScience 33, 28–30 (1998).Article
Google Scholar
Reilly, J. R. et al. Crop production in the USA is frequently limited by a lack of pollinators. Proc. Biol. Sci. 287, 20200922 (2020).CAS
PubMed
PubMed Central
Google Scholar
Greenleaf, S. S. & Kremen, C. Wild bees enhance honey bees’ pollination of hybrid sunflower. Proc. Natl Acad. Sci. USA 103, 13890–13895 (2006).CAS
PubMed
PubMed Central
Article
Google Scholar
Sáez, A. Managed honeybees decrease pollination limitation in self-compatible but not in self-incompatible crops. Proc. Biol. Sci. 289, 20220086 (2022).PubMed
Google Scholar
Brittain, C., Williams, N., Kremen, C. & Klein, A. M. Synergistic effects of non-Apis bees and honey bees for pollination services. Proc. Biol. Sci. 280, 20122767 (2013).PubMed
PubMed Central
Google Scholar
Aizen, M. A. & Harder, L. D. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19, 915–918 (2009).CAS
PubMed
Article
Google Scholar
Houlahan, J. E. et al. Negative relationships between species richness and temporal variability are common but weak in natural systems. Ecology 99, 2592–2604 (2018).CAS
PubMed
Article
Google Scholar
Winfree, R. Global change, biodiversity, and ecosystem services: what can we learn from studies of pollination? Basic Appl. Ecol. 14, 453–460 (2013).Article
Google Scholar
Greenleaf, S. S., Williams, N. M., Winfree, R. & Kremen, C. Bee foraging ranges and their relationship to body size. Oecologia 153, 589–596 (2007).PubMed
Article
Google Scholar
Cariveau, D. P., Williams, N. M., Benjamin, F. E. & Winfree, R. Response diversity to land use occurs but does not consistently stabilise ecosystem services provided by native pollinators. Ecol. Lett. 16, 903–911 (2013).PubMed
Article
Google Scholar
Gamfeldt, L., Hillebrand, H. & Jonsson, P. R. Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology 89, 1223–1231 (2008).PubMed
Article
Google Scholar
Zavaleta, E. S., Pasari, J. R., Hulvey, K. B. & Tilman, G. D. Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Proc. Natl Acad. Sci. USA 107, 1443–1446 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
Haupt, R. L. & Haupt, S. E. Practical Genetic Algorithms (Wiley, 2004).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article
Google Scholar
Lüdecke, D., Makowski, D., Waggoner, P. & Patil, I. performance: Assessment of regression models performance. R package version 0.7.0 https://doi.org/10.5281/zenodo.3952174 (2020).Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S (Springer, 2002).Brooks, M. et al. glmmTMB: Generalized linear mixed models using template model builder. R package version 1.1.3 https://glmmtmb.github.io/glmmTMB/ (2022).R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021). More