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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.

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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).

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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.

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Authors and Affiliations



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.

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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

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

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