Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Bumblebee family lineage survival is enhanced in high-quality landscapes


Insect pollinators such as bumblebees (Bombus spp.) are in global decline1,2. A major cause of this decline is habitat loss due to agricultural intensification3. A range of global and national initiatives aimed at restoring pollinator habitats and populations have been developed4,5. However, the success of these initiatives depends critically upon understanding how landscape change affects key population-level parameters, such as survival between lifecycle stages6, in target species. This knowledge is lacking for bumblebees, because of the difficulty of systematically finding and monitoring colonies in the wild. We used a combination of habitat manipulation, land-use and habitat surveys, molecular genetics7 and demographic and spatial modelling to analyse between-year survival of family lineages in field populations of three bumblebee species. Here we show that the survival of family lineages from the summer worker to the spring queen stage in the following year increases significantly with the proportion of high-value foraging habitat, including spring floral resources, within 250–1,000 m of the natal colony. This provides evidence for a positive impact of habitat quality on survival and persistence between successive colony cycle stages in bumblebee populations. These findings also support the idea that conservation interventions that increase floral resources at a landscape scale and throughout the season have positive effects on wild pollinators in agricultural landscapes.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Bumblebee colony cycle stages and family lineages sampled in the study with estimated survival parameters.
Figure 2: Effects of habitat quality and land-use variables on bumblebee family lineage survival from the summer worker to spring queen stage (φ2).


  1. 1

    Williams, P. H. & Osborne, J. L. Bumblebee vulnerability and conservation world-wide. Apidologie 40, 367–387 (2009)

    Article  Google Scholar 

  2. 2

    Cameron, S. A . et al. Patterns of widespread decline in North American bumble bees. Proc. Natl Acad. Sci. USA 108, 662–667 (2011)

    CAS  Article  ADS  Google Scholar 

  3. 3

    Vanbergen, A. J. & The Insect Pollinators Initiative. Threats to an ecosystem service: pressures on pollinators. Front. Ecol. Environ 11, 251–259 (2013)

    Article  Google Scholar 

  4. 4

    Department for Environment, Food & Rural Affairs. The National Pollinator Strategy: for bees and other pollinators in England. (2014)

  5. 5

    Gill, R. J. et al. Protecting an ecosystem service: approaches to understanding and mitigating threats to wild insect pollinators. Adv. Ecol. Res 54, 135–206 (2016)

    Article  Google Scholar 

  6. 6

    Carvell, C. et al. Bumble bee species’ responses to a targeted conservation measure depend on landscape context and habitat quality. Ecol. Appl . 21, 1760–1771 (2011)

    CAS  Article  Google Scholar 

  7. 7

    Dreier, S. et al. Fine-scale spatial genetic structure of common and declining bumble bees across an agricultural landscape. Mol. Ecol . 23, 3384–3395 (2014)

    Article  Google Scholar 

  8. 8

    Baude, M. et al. Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530, 85–88 (2016)

    CAS  Article  ADS  Google Scholar 

  9. 9

    Winfree, R., Aguilar, R., Vázquez, D. P., LeBuhn, G. & Aizen, M. A. A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076 (2009)

    Article  Google Scholar 

  10. 10

    Garibaldi, L. A. et al. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett . 14, 1062–1072 (2011)

    Article  Google Scholar 

  11. 11

    Natural England. Countryside Stewardship Manual (Natural England catalogue code NE608, (2015)

  12. 12

    Carvell, C., Meek, W. R., Pywell, R. F., Goulson, D. & Nowakowski, M. Comparing the efficacy of agri-environment schemes to enhance bumble bee abundance and diversity on arable field margins. J. Appl. Ecol . 44, 29–40 (2007)

    Article  Google Scholar 

  13. 13

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

    Article  Google Scholar 

  14. 14

    Pywell, R. F . et al. Wildlife-friendly farming increases crop yield: evidence for ecological intensification. Proc. R. Soc. B 282, 20151740 (2015)

    Article  Google Scholar 

  15. 15

    M’Gonigle, L. K., Ponisio, L. C., Cutler, K. & Kremen, C. Habitat restoration promotes pollinator persistence and colonization in intensively managed agriculture. Ecol. Appl . 25, 1557–1565 (2015)

    Article  Google Scholar 

  16. 16

    Klein, A.-M . et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313 (2007)

    Article  Google Scholar 

  17. 17

    Garratt, M. P. D. et al. The identity of crop pollinators helps target conservation for improved ecosystem services. Biol. Conserv . 169, 128–135 (2014)

    CAS  Article  Google Scholar 

  18. 18

    Benton, T. Bumblebees: the Natural History & Identification of the Species found in Britain (Collins, 2006)

  19. 19

    Beekman, M ., van Stratum, P & Lingeman, R. Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entomol. Exp. Appl . 89, 207–214 (1998)

    Article  Google Scholar 

  20. 20

    Lepais, O. et al. Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol. Ecol . 19, 819–831 (2010)

    CAS  Article  Google Scholar 

  21. 21

    Williams, N. M., Regetz, J. & Kremen, C. Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93, 1049–1058 (2012)

    Article  Google Scholar 

  22. 22

    Jha, S. & Kremen, C. Urban land use limits regional bumble bee gene flow. Mol. Ecol . 22, 2483–2495 (2013)

    Article  Google Scholar 

  23. 23

    Redhead, J. W. et al. Effects of habitat composition and landscape structure on worker foraging distances of five bumble bee species. Ecol. Appl . 26, 726–739 (2016)

    Article  Google Scholar 

  24. 24

    Lebreton, J.-D., Burnham, K. P., Clobert, J. & Anderson, D. R. Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol. Monogr . 62, 67–118 (1992)

    Article  Google Scholar 

  25. 25

    Goulson, D. et al. Effects of land use at a landscape scale on bumblebee nest density and survival. J. Appl. Ecol . 47, 1207–1215 (2010)

    Article  Google Scholar 

  26. 26

    Jha, S & Kremen, C. Resource diversity and landscape-level homogeneity drive native bee foraging. Proc. Natl Acad. Sci. USA 110, 555–558 (2013)

    CAS  Article  ADS  Google Scholar 

  27. 27

    Dicks, L. V. et al. How much flower-rich habitat is enough for wild pollinators? Answering a key policy question with incomplete knowledge. Ecol. Entomol . 40, 22–35 (2015)

    Article  Google Scholar 

  28. 28

    Carvell, C., Bourke, A. F. G., Osborne, J. L. & Heard, M. S. Effects of an agri-environment scheme on bumblebee reproduction at local and landscape scales. Basic Appl. Ecol . 16, 519–530 (2015)

    Article  Google Scholar 

  29. 29

    Nieto, A. et al. European Red List of Bees (Luxembourg: Publication Office of the European Union, 2014)

  30. 30

    Redhead, J. W. et al. Map of land-use/land-cover and floral cover across an arable landscape in Buckinghamshire, UK. NERC Environmental Information Data Centre (2014)

  31. 31

    Lye, G., Park, K., Osborne, J., Holland, J. & Goulson, D. Assessing the value of Rural Stewardship schemes for providing foraging resources and nesting habitat for bumblebee queens (Hymenoptera: Apidae). Biol. Conserv . 142, 2023–2032 (2009)

    Article  Google Scholar 

  32. 32

    Lopez-Vaamonde, C. et al. Lifetime reproductive success and longevity of queens in an annual social insect. J. Evol. Biol . 22, 983–996 (2009)

    CAS  Article  Google Scholar 

  33. 33

    Goulson, D., Hughes, W. O. H., Derwent, L. C. & Stout, J. C. Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130, 267–273 (2002)

    CAS  Article  ADS  Google Scholar 

  34. 34

    Whitehorn, P. R., O’Connor, S., Wackers, F. L. & Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012)

    CAS  Article  ADS  Google Scholar 

  35. 35

    Carvell, C. et al. Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumblebee species. Oikos 121, 734–742 (2012)

    Article  Google Scholar 

  36. 36

    Holehouse, K. A., Hammond, R. L. & Bourke, A. F. G. Non-lethal sampling of DNA from bumble bees for conservation genetics. Insectes Sociaux 50, 277–285 (2003)

    Article  Google Scholar 

  37. 37

    Dreier, S. et al. Microsatellite genotype data for five species of bumblebee across an agricultural landscape in Buckinghamshire, UK. NERC Environmental Information Data Centre (2014)

  38. 38

    Wang, J. Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963–1979 (2004)

    Article  Google Scholar 

  39. 39

    Bourke, A. F. G. Sex ratios in bumble bees. Phil. Trans. R. Soc. Lond. B 352, 1921–1933 (1997)

    Article  ADS  Google Scholar 

  40. 40

    White, G. C. & Burnham, K. P. Program MARK: survival estimation from populations of marked animals. Bird Study 46, 120–139 (1999)

    Article  Google Scholar 

  41. 41

    Carvell, C. et al. Family lineage and landscape quality data for wild bumblebee colonies across an agricultural landscape in Buckinghamshire, UK. NERC Environmental Information Data Centre (2016)

  42. 42

    Carvell, C. et al. Location data of worker bumblebees across an agricultural landscape in Buckinghamshire, UK. NERC Environmental Information Data Centre (2014)

Download references


We thank the CEH field team (L. Hulmes, J. Peyton, J. Savage, S. Amy, R. Chapman, G. Baron and R. MacDonald) for sampling bumblebees and conducting habitat surveys; R. Faccenda and R. Franklin of Faccenda Farms, and other landowners, for access to the Hillesden Estate and surroundings; R. Pywell and M. Nowakowski for access to the Hillesden Experimental Platform; H. Dean for data management; C. Harrower for help with graphics; H. M. Lattorff for use of his primers for the molecular discrimination of B. terrestris and B. lucorum workers; I. Warren for assistance with laboratory work; and J. Bullock and K. Schonrogge for comments on an earlier version of the manuscript. This research was supported by the Insect Pollinators Initiative (grant BB/I000925/1). The Insect Pollinators Initiative was funded jointly by the Biotechnology and Biological Sciences Research Council, the Department for Environment, Food and Rural Affairs, the Natural Environment Research Council, The Scottish Government and The Wellcome Trust, under the Living with Environmental Change Partnership. Acquisition of remote sensing data was funded by Syngenta Plc.

Author information




C.C., M.S.H., A.F.G.B., S.S. and W.C.J. conceived the project and designed the study. C.C., M.S.H. and S.H. coordinated the fieldwork and modelling elements and C.C. prepared the manuscript. S.D. carried out the molecular genotyping and sibship assignments with guidance from J.W. J.W.R. developed and applied the spatial analyses and S.N.F. designed and undertook the statistical analyses. All authors contributed to writing and critiquing the manuscript.

Corresponding author

Correspondence to Claire Carvell.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks T. Ergon and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Figure 1 Variation and correlations between habitat and land-use variables across the study landscape.

Plots show (i) histograms to demonstrate variation within each habitat/land-use variable along the diagonal; (ii) scatter plots showing correlations between variables (top, right) with a linear model trend line fitted to the correlation data (in red, only extended to the limits of the data) and a 1:1 line (in pale grey) and (iii) correlation coefficients with their significance (bottom, left) where *P < 0.05, **P < 0.01 and ***P < 0.001. Axis values are standardised and represent proportional cover of the different habitat variables within 1,000 m of the estimated colony locations, with variable names following the same order and shortened format as presented in Extended Data Table 5. Each point on the scatter plots represents one family lineage (n = 456). Arable, arable field cover; Mixed, mixed semi-natural vegetation cover; Nest, nesting habitat cover; Spring, spring flower cover; Summer, summer flower cover; Queen, queen-visited spring flower cover; Spr + Sum, combined queen-visited and worker-preferred flower cover; Worker, worker-preferred flower cover.

Extended Data Figure 2 Simulation-based assessment of robustness of the modified CJS model.

ad, The estimated parameter values aggregate around the true values. Frequency distributions of parameter estimates are shown, from 1,000 simulated datasets, each of 2,000 families. Parameters plotted are shown for ad as indicated. a, φ1: true value = 0.6. b, φ2: true value = 0.5. c, λ1: true value = 3. d, λ2: true value = 2. To align with the real data in which some families were not detected at the founding queen (Q1) stage, if at all, data were simulated assuming a detection probability of 0.4 at the Q1 stage.

Extended Data Figure 3 Goodness of fit for the modified mark–recapture model.

See Extended Data Table 3 for estimated probabilities. ad, Frequency distributions across all species are shown. a, Observed counts of workers (W1i). b, Expected counts of workers (W1i). c, Observed counts of second-generation queens (Q2i). d, Expected counts of second-generation queens (Q2i).

Extended Data Table 1 Numbers (and percentages) of bumblebee (Bombus spp.) colonies and lineages detected within each family relationship category
Extended Data Table 2 Initial model results showing estimated survival and detection parameters for the three study bumblebee (Bombus) species
Extended Data Table 3 Estimated probabilities of survival and detection of bumblebee (Bombus spp.) family lineages using the modified mark–recapture model
Extended Data Table 4 Model results for logistic regression of apparent survival (probability of bumblebee family lineage survival from the summer colony to spring queen stage (φ2)) against habitat quality and land-use variables at four spatial scales
Extended Data Table 5 Habitat quality and land-use variables for which effects on bumblebee family lineage survival and queen dispersal distance were tested
Extended Data Table 6 Plant groups used for field survey of habitats across the study landscape

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data, Supplementary Tables 1-2 and additional references. (PDF 271 kb)

Supplementary Data

This file contains the R code. (TXT 3 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Carvell, C., Bourke, A., Dreier, S. et al. Bumblebee family lineage survival is enhanced in high-quality landscapes. Nature 543, 547–549 (2017).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing