Historical nectar assessment reveals the fall and rise of floral resources in Britain

Abstract

There is considerable concern over declines in insect pollinator communities and potential impacts on the pollination of crops and wildflowers1,2,3,4. Among the multiple pressures facing pollinators2,3,4, decreasing floral resources due to habitat loss and degradation has been suggested as a key contributing factor2,3,4,5,6,7,8. However, a lack of quantitative data has hampered testing for historical changes in floral resources. Here we show that overall floral rewards can be estimated at a national scale by combining vegetation surveys and direct nectar measurements. We find evidence for substantial losses in nectar resources in England and Wales between the 1930s and 1970s; however, total nectar provision in Great Britain as a whole had stabilized by 1978, and increased from 1998 to 2007. These findings concur with trends in pollinator diversity, which declined in the mid-twentieth century9 but stabilized more recently10. The diversity of nectar sources declined from 1978 to 1990 and thereafter in some habitats, with four plant species accounting for over 50% of national nectar provision in 2007. Calcareous grassland, broadleaved woodland and neutral grassland are the habitats that produce the greatest amount of nectar per unit area from the most diverse sources, whereas arable land is the poorest with respect to amount of nectar per unit area and diversity of nectar sources. Although agri-environment schemes add resources to arable landscapes, their national contribution is low. Owing to their large area, improved grasslands could add substantially to national nectar provision if they were managed to increase floral resource provision. This national-scale assessment of floral resource provision affords new insights into the links between plant and pollinator declines, and offers considerable opportunities for conservation.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Nectar productivity and diversity in Great Britain in 2007.
Figure 2: Plant species’ contributions to Great Britain nectar provision and to habitat nectar provision, based on 2007 land cover and nonlinear vegetation data.
Figure 3: Seasonal nectar productivity in Great Britain, based on 2007 land cover and nonlinear vegetation data.
Figure 4: Historical changes in nectar provision (in 1 × 106 kg of sugars per year) at the national scale in England and Wales (1930–2007) and in Great Britain (1978–2007).

References

  1. 1

    Biesmeijer, J. et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354 (2006)

    CAS  ADS  Article  Google Scholar 

  2. 2

    Potts, S. G. et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010)

    Article  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

    Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015)

    Article  Google Scholar 

  5. 5

    Carvell, C. et al. Declines in forage availability for bumblebees at a national scale. Biol. Conserv. 132, 481–489 (2006)

    Article  Google Scholar 

  6. 6

    Roulston, T. H. & Goodell, K. The role of resources and risks in regulating wild bee populations. Annu. Rev. Entomol. 56, 293–312 (2011)

    CAS  Article  Google Scholar 

  7. 7

    Scheper, J. et al. Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in The Netherlands. Proc. Natl Acad. Sci. USA 111, 17552–17557 (2014)

    CAS  ADS  Article  Google Scholar 

  8. 8

    Kleijn, D. & Raemakers, I. A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89, 1811–1823 (2008)

    Article  Google Scholar 

  9. 9

    Ollerton, J., Erenler, H., Edwards, M. & Crockett, R. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346, 1360–1362 (2014)

    CAS  ADS  Article  Google Scholar 

  10. 10

    Carvalheiro, L. G. et al. Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol. Lett. 16, 870–878 (2013)

    Article  Google Scholar 

  11. 11

    Robinson, R. A. & Sutherland, W. J. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39, 157–176 (2002)

    Article  Google Scholar 

  12. 12

    Petit, S., Stuart, R. C., Gillespie, M. K. & Barr, C. J. Field boundaries in Great Britain: stock and change between 1984, 1990 and 1998. J. Environ. Manage. 67, 229–238 (2003)

    CAS  Article  Google Scholar 

  13. 13

    Blackstock, T. H. et al. The extent of semi-natural grassland communities in lowland England and Wales : a review of conservation surveys 1978–96. Grass Forage Sci. 54, 1–18 (1999)

    Article  Google Scholar 

  14. 14

    Ratcliffe, D. A. Post-medieval and recent changes in British vegetation: the culmination of human influence. New Phytol. 98, 73–100 (1984)

    CAS  Article  Google Scholar 

  15. 15

    Fuller, R. M. The changing extent and conservation interest of lowland grasslands in England and Wales : A review of grassland surveys 1930–84. Biol. Conserv. 40, 281–300 (1987)

    Article  Google Scholar 

  16. 16

    Natural England. Countryside Stewardship Manualhttps://www.gov.uk/guidance/countryside-stewardship-manual (2015)

  17. 17

    Carvell, C., Meek, W. R. W., Pywell, R. F., Goulson, D. & Nowakowski, M. Comparing the efficiency 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 

  18. 18

    Willmer, P. Pollination and Floral Ecology 1–778 (Princeton Univ. Press, 2011)

  19. 19

    Carey, P. D. et al. Countryside Survey: UK Results from 2007 . 1–105 (NERC/Centre for Ecology & Hydrology, 2008)

  20. 20

    Stamp, L. D. The Land of Britain: its Use and Misuse (Longmans, Green and Co., 1948)

  21. 21

    Kirk, G. J. D., Bellamy, P. H. & Lark, R. M. Changes in soil pH across England and Wales in response to decreased acid deposition. Glob. Change Biol. 16, 3111–3119 (2006)

    Google Scholar 

  22. 22

    Reynolds, B. et al. Countryside Survey: National “Soil Change” 1978 – 2007 for Topsoils in Great Britain — Acidity, Carbon, and Total Nitrogen Status. Vadose Zone J. 12, (2013)

  23. 23

    Boatman, N. D., Jones, N. E., Conyers, S. T. & Pietravalle, S. Development of plant communities on set-aside in England. Agric. Ecosyst. Environ. 143, 8–19 (2011)

    Article  Google Scholar 

  24. 24

    Breeze, T. D., Bailey, P., Balcombe, K. G. & Potts, S. G. Pollination services in the UK: How important are honeybees? Agric. Ecosyst. Environ. 142, 137–143 (2011)

    Article  Google Scholar 

  25. 25

    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  Article  Google Scholar 

  26. 26

    Staley, J. T. et al. Changes in hedgerow floral diversity over 70 years in an English rural landscape, and the impacts of management. Biol. Conserv. 167, 97–105 (2013)

    Article  Google Scholar 

  27. 27

    Preston, C. D., Pearman, D. A. & Dines, T. D. New Atlas of the British and Irish Flora: An Atlas of the Vascular Plants of Britain, Ireland, The Isle of Man and the Channel Island 910 (Oxford Univ. Press, 2002)

  28. 28

    Fitter, A. H. & Peat, H. J. The Ecological Flora Database. J. Ecol. 82, 415–425 (1994)

    Article  Google Scholar 

  29. 29

    Corbet, S. A. et al. Native or exotic? Double or single? Evaluating plants for pollinator-friendly gardens. Ann. Bot. 87, 219 (2001)

    Article  Google Scholar 

  30. 30

    Carvalheiro, L. G., Barbosa, E. R. M. & Memmott, J. Pollinator networks, alien species and the conservation of rare plants: Trinia glauca as a case study. J. Appl. Ecol. 45, 1419–1427 (2008)

    Article  Google Scholar 

  31. 31

    Botanical Society of the British Isles. http://www.botanicalkeys.co.uk/flora/ (2011)

  32. 32

    Kirk, W. D. J. & Howes, F. N. Plants for Bees: a Guide to the Plants that Benefit the Bees of the British Isles 1–311 (International Bee Res. Assoc., 2012)

  33. 33

    Klotz, S., Kühn, I. & Durka, W. BIOLFLOR - Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. http://www2.ufz.de/biolflor/index.jsp (2002)

  34. 34

    Wood, C. M., Howard, D. C., Henrys, P. A. & Smart, S. M. Countryside Survey: Measuring Habitat Change over 30 years 1978 Data Rescue - Final Report, 1–18 (2012)

  35. 35

    Countryside Survey: England Results from 2007. NERC/Centre for Ecology & Hydrology, Department for Environment, Food and Rural Affairs, Natural England, 1–119 (2009)

  36. 36

    R Development Core Team. R: A Language and Environment for Statistical Computing. http://www.R-project.org (2013)

  37. 37

    Morton, R. D. et al. Final Report for LCM2007 - the new UK land cover map. Countryside Survey Technical Report No 11/07 NERC/Centre for Ecology & Hydrology (CEH Project Number: C03259), 112 (2011)

  38. 38

    Department for Environment Food and Rural Affairs. Entry Level Stewardship Handbook Terms and conditions and how to apply PB10355. 116 (2005)

  39. 39

    Department for Environment Food and Rural Affairs. Higher Level Stewardship Handbook Terms and conditions and how to apply PB10382. 123 (2005)

  40. 40

    Raine, N. R. & Chittka, L. Nectar production rates of 75 bumblebee-visited flower species in a German flora (Hymenoptera: Apidae: Bombus terrestris). Entomol. Gen. 30, 191–192 (2007)

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the UK Insect Pollinators Initiative (IPI) ‘AgriLand: Linking agriculture and land use change to pollinator populations’ project, funded by the Biotechnology and Biological Sciences Research Council (BBSRC), Wellcome Trust, Scottish Government, Department of Environment, Food and Rural Affairs (DEFRA) and Natural Environment Research Council (NERC) under the auspices of the Living with Environmental Change partnership: grant BB/H014934/1 (http://www.agriland.leeds.ac.uk). Land Cover and Countryside Survey data are owned by NERC – Centre for Ecology & Hydrology (http://www.countrysidesurvey.org.uk).

Author information

Affiliations

Authors

Contributions

The study was conceived by W.E.K. and J.M. The field survey was carried out by M.B. and N.D. with the help of J.M. The data were compiled and analysed by M.B. with suggestions from W.E.K., J.M., S.M.S., R.D.M. and M.A.K.G. Vegetation data from the Countryside Survey database were extracted by S.M.S. Agri-environment scheme data were provided and analysed by N.D.B. and S.C. The national maps were generated by R.D.M. All authors discussed the results and contributed during manuscript writing.

Corresponding author

Correspondence to Mathilde Baude.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

The floral resource database will be made available from the NERC Environmental Information Data Centre (http://dx.doi.org/10.5285/69402002-1676-4de9-a04e-d17e827db93c and http://dx.doi.org/10.5285/6c6d3844-e95a-4f84-a12e-65be4731e934).

Extended data figures and tables

Extended Data Figure 1 Annual nectar productivity and diversity in linear features in 2007.

a, Box plots of log10 (x + 1) nectar productivity according to the location of the vegetation surveyed (area (nonlinear) versus linear features) in each habitat. b, Box plots of species nectar diversity according to the location of the vegetation surveyed (area versus linear features) in each habitat. c, Box plots of functional nectar diversity according to the location of the vegetation surveyed (area versus linear features) in each habitat. Significant differences of locations (area versus linear features) in habitats are indicated by asterisks as follows: *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001. Statistical models were re-run without calcareous grassland habitat (to meet residuals homoscedasticity constraint) in order to check that significant effects remained. See Extended Data Table 1 for ANOVA results. See ‘Statistical analyses’ section of the Methods for detailed statistical methods and definition of box plot elements. Source data

Extended Data Figure 2 Historical changes in nectar productivity and diversity per habitat over recent decades (1978 to 2007).

a, Box plots of log10 (x + 1) nectar productivity per habitat, based on vegetation data for 1978, 1990, 1998 and 2007. b, Box plots of species nectar diversity per habitat, based on vegetation data for 1978, 1990, 1998 and 2007. c, Box plots of functional nectar diversity per habitat, based on vegetation data for 1978, 1990, 1998 and 2007. Significant differences of time periods per habitats are indicated by asterisks (*P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001). See Extended Data Table 1 for ANOVA results and Supplementary Table 3 for sample sizes. See ‘Statistical analyses’ section of the Methods for detailed statistical methods and definition of box plot elements. Source data

Extended Data Figure 3 Habitat contributions to the national nectar provision shifts and species contributions to habitats over recent decades (1978 to 2007).

ac, Habitat contributions to the national nectar provision changes from a, 1978 to 1990, b, 1990 to 1998, and c, 1998 to 2007. All bar plots represent the absolute changes (in 1 × 106 kg of sugars) for each habitat during the time period considered. Numbers in brackets indicate the relative changes (in %). dn, Species contributions to nectar provision in 1978, 1990, 1998 and 2007 per habitat type. Only species that contribute to the first 90% are shown. See Supplementary Table 10 for main contributing species to the national changes from 1978 to 2007. Source data

Extended Data Figure 4 Sensitivity analyses of historical trends from 1978 to 2007 in nectar productivity and species diversity with alternative data sets.

a, b, Box plots of log10 (x + 1) nectar productivity (a) and box plots of species nectar diversity per habitat (b) based on vegetation data for 1978, 1990, 1998 and 2007 discounting the contribution of grazed white clover in improved grassland. c, d, Box plots of log10 (x + 1) nectar productivity (c) and box plots of species nectar diversity per habitat (d), based on vegetation data for 1978, 1990, 1998 and 2007 and computed with the alternative rectangular phenology function. e, f, Box plots of log10 (x + 1) nectar productivity (e) and box plots of species nectar diversity per habitat (f), based on vegetation data for 1978, 1990, 1998 and 2007 and computed considering only the species with empirical nectar values. Significant differences of time periods per habitat are indicated by asterisks (*P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001). See Supplementary Table 3 for sample sizes and Supplementary Information for details. See ‘Statistical analyses’ section of the Methods for detailed statistical methods and definition of box plot elements. Source data

Extended Data Figure 5 Historical timeline in changes in nectar resources and flower-visiting insects in Great Britain.

Historical periods with the greatest negative changes in nectar resources (in percentage change in England and Wales (E&W) and Great Britain (GB)) and flower-visiting insects (in percentage change or in species extinction per decade (sp./dec.)) are indicated in red, those with intermediate changes are in orange, and those with the lowest (or even reversing) changes are in green. Main historical trends from this study (Baude et al.) are presented in regard to those described in Carvalheiro et al.10 and Ollerton et al.9 studies. The white chevron indicates a provisional extinction rate that needs to be confirmed on a 20 year period of time (see Supplementary Information from Ollerton et al.9).

Extended Data Figure 6 Validity of the data sets.

a, Major axis linear regression of log10 (x + 1) nectar values per flower obtained in the second location against those obtained in the first one. b, Major axis linear regression of log10 (x + 1) flower density values obtained in the second location against those obtained in the first one. c, Major axis linear regression of log10 (x + 1) peak flower density values obtained in the second location against those obtained in the first one. d, Standardized major axis regression of the log10 (x + 1) length of the flowering period used for analyses with those derived from IPI AgriLand floral transects (unpublished data). e, Standardized major axis regression of peak date of flowering season used for analyses with those derived from IPI AgriLand floral transects (unpublished data). f, Major axis linear regression performed on the log10 (x + 1) empirical (empirical data set) and published nectar values (literature data set from Raine and Chittka40) at the flower scale. g, Standardized major axis linear regression performed on the log10 (x + 1) empirical (empirical data set) and published nectar values (literature data set, see Supplementary Table 13 for references) at the vegetative scale. h, Standardized major axis linear regression performed on the log10 (x + 1) empirical and modelled nectar values generated by a leave-one-out approach. Estimated values and 95% confidence intervals (solid and dashed lines, respectively) of all equations are derived from (standardized) major axis regression (ma and sma function from ‘smatr’ package in R36; see Supplementary Information for details). Source data

Extended Data Figure 7 Flower number and vegetative cover relationships.

Linear regressions between the number of open flowers counted in a quadrat of 0.5 m2 according to the vegetative cover of the focus species in the quadrat (in %). Data are extracted from IPI AgriLand floral transects survey in 2012 (unpublished data) for 23 out of the 35 main nectar contributing species (panels aw). The number of flowers was analysed according to the vegetative cover (‘Cover’), the month of the survey (‘Month’) and the interaction between these two terms (‘Cover:Month’) using negative binomial generalized linear models (see Supplementary Information for details). Coloured lines represent the linear regression between flower abundance and vegetative cover for each month of the survey. Black lines represent the overall linear regression between flower abundance and vegetative cover when the ‘Month’ covariate cannot be included in the model. Line equations were derived from statistical intercept and slope estimates. Source data

Extended Data Table 1 Type III ANOVA (F-tests) results for annual nectar productivity, species nectar diversity and functional nectar diversity
Extended Data Table 2 Flower morphology and flower-visiting insects of the four main nectar-providing species
Extended Data Table 3 Agri-environment schemes and linear features: nectar productivity and provision in England in 2007

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Results, a Supplementary Discussion, Supplementary Figure 1, Supplementary Tables 1-10 and Supplementary references - see contents page for further details. (PDF 3572 kb)

Supplementary Table 11

This file contains Supplementary Table 11, which shows plant traits, flowering phenology, flower density, nectar productivity at the flower scale and nectar sugar productivity at the vegetative scale for the list of 260 species. (XLSX 74 kb)

Supplementary Table 12

This table contains a reference list for flower-visiting insects of the four main nectar providers nationally. It lists sources and data used to investigate the visiting insects of the main nectar providing plant species (Extended Data Table 2). This combines published and unpublished plant-pollinator interactions data from Memmott’s group and a review of literature of insect species visiting flowers of Trifolium repens, Calluna vulgaris, Cirsium palutre and Erica cinerea. (XLSX 26 kb)

Supplementary Table 13

This table contains a reference list for published sugar potential values in kg/ha /year. It lists sources and data used to compare our nectar values (in kg/ha cover/year) to those found in literature (Extended Data Figure 6g). Published values of sugar potential are available for 128 species at the time of writing. Where values were available from more than one source, an average was calculated. Where values were given only as honey potential in the literature, these values were multiplied by 0.8 to give sugar potential. This ratio has been reported in the majority of the published sources (References 1, 5-17). (XLSX 16 kb)

PowerPoint slides

Source data

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Baude, M., Kunin, W., Boatman, N. et al. Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530, 85–88 (2016). https://doi.org/10.1038/nature16532

Download citation

Further reading

Comments

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.

Search

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