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Complex long-term biodiversity change among invertebrates, bryophytes and lichens

Nature Ecology & Evolution volume 4, pages 384–392 (2020)Cite this article

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Abstract

Large-scale biodiversity changes are measured mainly through the responses of a few taxonomic groups. Much less is known about the trends affecting most invertebrates and other neglected taxa, and it is unclear whether well-studied taxa, such as vertebrates, reflect changes in wider biodiversity. Here, we present and analyse trends in the UK distributions of over 5,000 species of invertebrates, bryophytes and lichens, measured as changes in occupancy. Our results reveal substantial variation in the magnitude, direction and timing of changes over the last 45 years. Just one of the four major groups analysed, terrestrial non-insect invertebrates, exhibits the declining trend reported among vertebrates and butterflies. Both terrestrial insects and the bryophytes and lichens group increased in average occupancy. A striking pattern is found among freshwater species, which have undergone a strong recovery since the mid-1990s after two decades of decline. We show that, while average occupancy among most groups appears to have been stable or increasing, there has been substantial change in the relative commonness and rarity of individual species, indicating considerable turnover in community composition. Additionally, large numbers of species have experienced substantial declines. Our results suggest a more complex pattern of biodiversity change in the United Kingdom than previously reported.

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Fig. 1: Composite estimates of the average annual occupancy of four groups of species.
Fig. 2: Absolute change in geometric mean occupancy during the first (1970–1992) and second (1993–2015) halves of the time series for each major group.
Fig. 3: Composite estimates of two quantiles of annual occupancy across the four major groups.
Fig. 4: Composite estimates of average annual occupancy for each taxonomic subgroup.
Fig. 5: Heat map of the comparison between each species’ average occupancy estimate across the entire period and its average annual growth rate for each of the four major groups.

Data availability

The dataset analysed as a part of this study is publicly available from the Environmental Information Data Centre30. Additional information is supplied in the associated R package UKBiodiversity, which is available from GitHub (https://github.com/CharlieOuthwaite/UKBiodiversity), and Data Descriptor29.

Code availability

The code used to analyse the data is available from GitHub in the R package UKBiodiversity (https://github.com/CharlieOuthwaite/UKBiodiversity).

References

  1. Gregory, R. D. et al. Developing indicators for European birds. Phil. Trans. R. Soc. B 360, 269–288 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  2. McRae, L., Deinet, S. & Freeman, R. The diversity-weighted living planet index: controlling for taxonomic bias in a global biodiversity indicator. PLoS ONE 12, e0169156 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Brereton, T., Roy, D. B., Middlebrook, I., Botham, M. & Warren, M. The development of butterfly indicators in the United Kingdom and assessments in 2010. J. Insect Conserv. 15, 139–151 (2010).

    Article  Google Scholar 

  4. Van Swaay, C. A. M. et al. The EU Butterfly Indicator for Grassland species: 1990-2017: Technical Report (Butterfly Conservation Europe & ABLE/eBMS, 2015).

  5. Tittensor, D. P. et al. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–244 (2014).

    Article  CAS  PubMed  Google Scholar 

  6. Westgate, M. J., Barton, P. S., Lane, P. W. & Lindenmayer, D. B. Global meta-analysis reveals low consistency of biodiversity congruence relationships. Nat. Commun. 5, 3899 (2014).

    Article  CAS  PubMed  Google Scholar 

  7. Rodrigues, A. S. L. & Brooks, T. M. Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. Annu. Rev. Ecol. Evol. Syst. 38, 713–737 (2007).

    Article  Google Scholar 

  8. Hambler, C. & Speight, M. R. Extinction rates and butterflies. Science 305, 1563–1565 (2004).

    Article  CAS  PubMed  Google Scholar 

  9. van Strien, A. J. et al. Modest recovery of biodiversity in a western European country: the living planet index for the Netherlands. Biol. Conserv. 200, 44–50 (2016).

    Article  Google Scholar 

  10. Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: a review of its drivers. Biol. Conserv. 232, 8–27 (2019).

    Article  Google Scholar 

  12. Powney, G. D. et al. Widespread losses of pollinating insects in Britain. Nat. Commun. 10, 1018 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Simmons, B. I. et al. Worldwide insect declines: an important message, but interpret with caution. Ecol. Evol. 9, 3678–3680 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Thomas, C. D. & Jones, T. H. & Hartley, S. E. ‘Insectageddon’: a call for more robust data and rigorous analyses. Glob. Change Biol. 25, 1891–1892 (2019).

    Article  Google Scholar 

  15. Burns, F. et al. Agricultural management and climatic change are the major drivers of biodiversity change in the UK. PLoS ONE 11, e0151595 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Burns, F. et al. An assessment of the state of nature in the United Kingdom: a review of findings, methods and impact. Ecol. Indic. 94, 226–236 (2018).

    Article  Google Scholar 

  17. Hayhow, D. et al. The State of the UK’s Birds 2017 (RSPB, BTO, WWT, DAERA, JNCC, NE and NRW, 2017).

  18. Fox, R. et al. The State of the UK’s Butterflies 2015 (Butterfly Conservation and the Centre for Ecology & Hydrology, 2015).

  19. Maskell, L. C., Smart, S. M., Bullock, J. M., Thompson, K. & Stevens, C. J. Nitrogen deposition causes widespread loss of species richness in British habitats. Glob. Change Biol. 16, 671–679 (2010).

    Article  Google Scholar 

  20. Barlow, K. E. et al. Citizen science reveals trends in bat populations: the National Bat Monitoring Programme in Great Britain. Biol. Conserv. 182, 14–26 (2015).

    Article  Google Scholar 

  21. Pocock, M. J. O., Roy, H. E., Preston, C. D. & Roy, D. B. The Biological Records Centre: a pioneer of citizen science. Biol. J. Linn. Soc. 115, 475–493 (2015).

    Article  Google Scholar 

  22. Isaac, N. J. B. & Pocock, M. J. O. Bias and information in biological records. Biol. J. Linn. Soc. 115, 522–531 (2015).

    Article  Google Scholar 

  23. Boakes, E. H. et al. Distorted views of biodiversity: spatial and temporal bias in species occurrence data. PLoS Biol. 8, e1000385 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Maldonado, C. et al. Estimating species diversity and distribution in the era of Big Data: to what extent can we trust public databases? Glob. Ecol. Biogeogr. 24, 973–984 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Outhwaite, C. L. et al. Prior specification in Bayesian occupancy modelling improves analysis of species occurrence data. Ecol. Indic. 93, 333–343 (2018).

    Article  Google Scholar 

  26. Isaac, N. J. B., van Strien, A. J., August, T. A., de Zeeuw, M. P. & Roy, D. B. Statistics for citizen science: extracting signals of change from noisy ecological data. Methods Ecol. Evol. 5, 1052–1060 (2014).

    Article  Google Scholar 

  27. van Strien, A. J., van Swaay, C. A. M. & Termaat, T. Opportunistic citizen science data of animal species produce reliable estimates of distribution trends if analysed with occupancy models. J. Appl. Ecol. 50, 1450–1458 (2013).

    Article  Google Scholar 

  28. Termaat, T. et al. Distribution trends of European dragonflies under climate change. Divers. Distrib. 25, 936–950 (2019).

    Article  Google Scholar 

  29. Outhwaite, C. L. et al. Annual Estimates of Occupancy for Bryophytes, Lichens and Invertebrates in the UK (1970–2015) (NERC Environmental Information Data Centre, 2019); https://doi.org/10.5285/0ec7e549-57d4-4e2d-b2d3-2199e1578d84

  30. Dornelas, M. et al. A balance of winners and losers in the Anthropocene. Ecol. Lett. 22, 847–854 (2019).

    Article  PubMed  Google Scholar 

  31. Gregory, R. & van Strien, A. Wild bird indicators: using composite population trends of birds as measures of environmental health. Ornithol. Sci. 9, 3–22 (2010).

    Article  Google Scholar 

  32. Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).

    Article  CAS  PubMed  Google Scholar 

  33. Pescott, O. L. et al. Air pollution and its effects on lichens, bryophytes, and lichen-feeding Lepidoptera: review and evidence from biological records. Biol. J. Linn. Soc. 115, 611–635 (2015).

    Article  Google Scholar 

  34. Saal, D. S. & Parker, D. The impact of privatization and regulation on the water and sewerage industry in England and Wales: a translog cost function model. Manage. Decis. Econ. 21, 253–268 (2000).

    Article  Google Scholar 

  35. Vaughan, I. P. & Ormerod, S. J. Large-scale, long-term trends in British river macroinvertebrates. Glob. Change Biol. 18, 2184–2194 (2012).

    Article  Google Scholar 

  36. Vaughan, I. P. & Gotelli, N. J. Water quality improvements offset the climatic debt for stream macroinvertebrates over twenty years. Nat. Commun. 10, 1956 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Langford, T. E. L., Shaw, P. J., Ferguson, A. J. D. & Howard, S. R. Long-term recovery of macroinvertebrate biota in grossly polluted streams: re-colonisation as a constraint to ecological quality. Ecol. Indic. 9, 1064–1077 (2009).

    Article  CAS  Google Scholar 

  38. Balmford, A. & Knowlton, N. Why Earth Optimism? Science 356, 225 (2017).

    Article  CAS  PubMed  Google Scholar 

  39. Antrop, M. Why landscapes of the past are important for the future. Landsc. Urban Plan. 70, 21–34 (2005).

    Article  Google Scholar 

  40. 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 

  41. Mihoub, J. B. et al. Setting temporal baselines for biodiversity: the limits of available monitoring data for capturing the full impact of anthropogenic pressures. Sci. Rep. 7, 41591 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Soga, M. & Gaston, K. J. Shifting baseline syndrome: causes, consequences, and implications. Front. Ecol. Environ. 16, 222–230 (2018).

    Article  Google Scholar 

  43. Thomas, C. D. Inheritors of the Earth: How Nature Is Thriving in an Age of Extinction (Hachette UK, 2017).

  44. Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science 344, 296–299 (2014).

    Article  CAS  PubMed  Google Scholar 

  45. Lister, B. C. & Garcia, A. Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc. Natl Acad. Sci. USA 115, 201722477 (2018).

    Article  CAS  Google Scholar 

  46. Mace, G. M., Collen, B., Fuller, R. A. & Boakes, E. H. Population and geographic range dynamics: implications for conservation planning. Phil. Trans. R. Soc. B 365, 3743–3751 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Gaston, K. J. & Fuller, R. A. The sizes of species’ geographic ranges. J. Appl. Ecol. 46, 1–9 (2009).

    Article  Google Scholar 

  48. Seibold, S. et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674 (2019).

    Article  CAS  PubMed  Google Scholar 

  49. Bart, J. & Klosiewski, S. P. Use of presence-absence to measure changes in avian density. J. Wildl. Manage. 53, 847–852 (1989).

    Article  Google Scholar 

  50. Webb, T. J., Freckleton, R. P. & Gaston, K. J. Characterizing abundance–occupancy relationships: there is no artefact. Glob. Ecol. Biogeogr. 21, 952–957 (2012).

    Article  Google Scholar 

  51. Buckley, H. L. & Freckleton, R. P. Understanding the role of species dynamics in abundance–occupancy relationships. J. Ecol. 98, 645–658 (2010).

    Article  Google Scholar 

  52. van Strien, A. J., van Swaay, C. A. M., van Strien-van Liempt, W. T. F. H., Poot, M. J. M. & WallisDeVries, M. F. Over a century of data reveal more than 80% decline in butterflies in the Netherlands. Biol. Conserv. 234, 116–122 (2019).

    Article  Google Scholar 

  53. Jetz, W. et al. Essential biodiversity variables for mapping and monitoring species populations. Nat. Ecol. Evol. 3, 539–551 (2019).

    Article  PubMed  Google Scholar 

  54. Schmeller, D. S. et al. An operational definition of essential biodiversity variables. Biodivers. Conserv. 26, 2967–2972 (2017).

    Article  Google Scholar 

  55. McGill, B. J. & Dornelas, M. & Gotelli, N. J. & Magurran, A. E. Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol. Evol. 30, 104–113 (2014).

    Article  PubMed  Google Scholar 

  56. Buckland, S. T., Magurran, A. E., Green, R. E. & Fewster, R. M. Monitoring change in biodiversity through composite indices. Phil. Trans. R. Soc. B 360, 243–254 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Faraway, J. J. Linear Models with R (Chapman & Hall, CRC, 2009).

  58. Outhwaite, C. L. et al. Annual estimates of occupancy for bryophytes, lichens and invertebrates in the UK, 1970–2015. Sci. Data 6, 259 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Gelman, A. et al. Bayesian Data Analysis (CRC, 2014).

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Acknowledgements

We thank the following recording schemes and societies for contributing data to the dataset underlying this study and for their input in interpreting group-level change: the Aquatic Heteroptera Recording Scheme; the Bees, Wasps and Ants Recording Society; the British Arachnological Society, Spider Recording Scheme; the British Bryological Society; the British Dragonfly Society: Dragonfly Recording Network; the British Lichen Society; the British Myriapod and Isopod Group: Centipede Recording Scheme; the British Myriapod and Isopod Group: Millipede Recording Scheme; the Chrysomelidae Recording Scheme; the Conchological Society of Great Britain and Ireland; the Dipterists Forum: Cranefly Recording Scheme; the Dipterists Forum: Empididae, Hybotidae and Dolichopodidae Recording Scheme; the Dipterists Forum: Fungus Gnat Recording Scheme; the Dipterists Forum: Hoverfly Recording Scheme; the Gelechiid Recording Scheme; the Grasshoppers and Related Insects Recording Scheme; the Ground Beetle Recording Scheme; the Lacewings and Allies Recording Scheme; the National Moth Recording Scheme; the Riverfly Recording Schemes: Ephemeroptera; the Riverfly Recording Schemes: Plecoptera; the Riverfly Recording Schemes: Trichoptera; the Soldier Beetles, Jewel Beetles and Glow-worms Recording Scheme; the Soldierflies and Allies Recording Scheme; the Staphylinidae Recording Scheme; the Terrestrial Heteroptera Recording Scheme—Plant bugs and allied species; the Terrestrial Heteroptera Recording Scheme—Shield bugs and allied species; the UK Ladybird Survey; and the Weevil and Bark Beetle Recording Scheme. We thank G. Mace, whose advice and comments on previous versions of this manuscript greatly improved the study. We thank T. August, G. Powney, J. Silvertown and R. Pearson for advice and comments on the draft manuscripts. We also thank J. Cranston for supplying a list of recent colonist species in the United Kingdom. This work was funded by NERC, award number NE/L008823/1, and was supported by NERC, award number NE/R016429/1, as part of the UK-SCAPE programme delivering National Capability.

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Author notes

  1. Deceased: Ben Collen.

Authors and Affiliations

  1. Centre for Ecology & Hydrology, Wallingford, UK

    Charlotte L. Outhwaite & Nick J. B. Isaac

  2. Centre for Biodiversity and Environment Research, University College London, London, UK

    Charlotte L. Outhwaite, Richard D. Gregory & Ben Collen

  3. RSPB Centre for Conservation Science, RSPB, Sandy, UK

    Charlotte L. Outhwaite & Richard D. Gregory

  4. Department of Statistical Science, University College London, London, UK

    Richard E. Chandler

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  1. Charlotte L. Outhwaite
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  2. Richard D. Gregory
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  3. Richard E. Chandler
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Contributions

N.J.B.I., B.C. and R.D.G. conceived the study. C.L.O. extracted and analysed the data and drafted the manuscript. R.E.C. determined the composite indicator method. All authors contributed to the writing and editing of the manuscript.

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Correspondence to Charlotte L. Outhwaite.

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Extended data

Extended Data Fig. 1 Figure 1 of the main text, repeated using different thresholds for the number of records that contribute to a species’ estimate.

Five thresholds were tested: a minimum of 50 records, 75, 100, 150 and 200 records. Each facet presents composite trends in average occupancy of four groups of species. Values are scaled to 100 in 1970. Coloured lines show the average response as the geometric mean occupancy and the shaded area represents the 95% credible intervals of the posterior distribution of the geometric mean.

Extended Data Fig. 2 Figure 1 of the main text, repeated 12 times whist randomising the species within each group.

The colours and number of species within each group are maintained as in Fig. 1 of the main text, however the species have been randomly reassigned across the groups. Red = freshwater (n = 318), green = insects (n = 3089), blue = invertebrates (n = 536) and purple = bryophytes & lichens (n = 1269). Values are scaled to 100 in 1970. Coloured lines show the average response as the geometric mean occupancy and the shaded area represents the 95% credible intervals of the posterior distribution of the geometric mean.

Extended Data Fig. 3 Mean across years of the species’ mean proportion of sites with records for each of 26 taxonomic groups.

The black line shows the 1:1 relationship, error bars delimit the 95% credible intervals.

Extended Data Fig. 4 Variance across years in the species’ mean proportion of sites with records for each of 26 taxonomic groups.

The black line shows the 1:1 relationship, error bars delimit the 95% credible intervals.

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Supplementary Information

Supplementary Tables 1–3 and Fig. 1.

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Outhwaite, C.L., Gregory, R.D., Chandler, R.E. et al. Complex long-term biodiversity change among invertebrates, bryophytes and lichens. Nat Ecol Evol 4, 384–392 (2020). https://doi.org/10.1038/s41559-020-1111-z

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