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  • Perspective
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Ecological time lags and the journey towards conservation success

Abstract

Global conservation targets to reverse biodiversity declines and halt species extinctions are not being met despite decades of conservation action. However, a lack of measurable change in biodiversity indicators towards these targets is not necessarily a sign that conservation has failed; instead, temporal lags in species’ responses to conservation action could be masking our ability to observe progress towards conservation success. Here we present our perspective on the influence of ecological time lags on the assessment of conservation success and review the principles of time lags and their ecological drivers. We illustrate how a number of conceptual species may respond to change in a theoretical landscape and evaluate how these responses might influence our interpretation of conservation success. We then investigate a time lag in a real biodiversity indicator using empirical data and explore alternative approaches to understand the mechanisms that drive time lags. Our proposal for setting and evaluating conservation targets is to use milestones, or interim targets linked to specific ecological mechanisms at key points in time, to assess whether conservation actions are likely to be working. Accounting for ecological time lags in biodiversity targets and indicators will greatly improve the way that we evaluate conservation successes.

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Fig. 1: Habitat transformation and species–area relationships.
Fig. 2: Changes in the woodland bird index and woodland creation over time.
Fig. 3: Proportion of woodlands containing woodland bird indicator species in 2016.
Fig. 4: Bird relative abundance and species richness compared with woodland age.
Fig. 5: Schematic representing key steps in the journey towards conservation success.

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References

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

    Article  CAS  Google Scholar 

  2. Global Biodiversity Outlook 4 (Secretariat of the Convention on Biological Diversity, 2014).

  3. Mace, G. M. et al. Aiming higher to bend the curve of biodiversity loss. Nat. Sustain. 1, 448–451 (2018).

    Article  Google Scholar 

  4. Jackson, S. T. & Sax, D. F. Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol. Evol. 25, 153–160 (2010).

    Article  Google Scholar 

  5. Kuussaari, M. et al. Extinction debt: a challenge for biodiversity conservation. Trends Ecol. Evol. 24, 564–571 (2009).

    Article  Google Scholar 

  6. Hylander, K. & Ehrlén, J. The mechanisms causing extinction debts. Trends Ecol. Evol. 28, 341–346 (2013).

    Article  Google Scholar 

  7. Figueiredo, L., Krauss, J., Steffan-Dewenter, I. & Sarmento Cabral, J. Understanding extinction debts: spatio–temporal scales, mechanisms and a roadmap for future research. Ecography 42, 1973–1990 (2019).

    Article  Google Scholar 

  8. Tilman, D., May, R. M., Lehman, C. L. & Nowak, M. A. Habitat destruction and the extinction debt. Nature 371, 65–66 (1994).

    Article  Google Scholar 

  9. Krauss, J. et al. Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol. Lett. 13, 597–605 (2010).

    Article  Google Scholar 

  10. Lira, P. K., de Souza Leite, M. & Metzger, J. P. Temporal lag in ecological responses to landscape change: where are we now? Curr. Landsc. Ecol. Rep. 4, 70–82 (2019).

    Article  Google Scholar 

  11. Cristofoli, S. & Mahy, G. Colonisation credit in recent wet heathland butterfly communities. Insect Conserv. Divers. 3, 83–91 (2010).

    Article  Google Scholar 

  12. Kolk, J., Naaf, T. & Wulf, M. Paying the colonization credit: converging plant species richness in ancient and post-agricultural forests in NE Germany over five decades. Biodivers. Conserv. 26, 735–755 (2017).

    Article  Google Scholar 

  13. Hanski, I. Extinction debt and species credit in boreal forests: modelling the consequences of different approaches to biodiversity conservation. Ann. Zool. Fennici 37, 271–280 (2000).

    Google Scholar 

  14. Naaf, T. & Kolk, J. Colonization credit of post-agricultural forest patches in NE Germany remains 130–230 years after reforestation. Biol. Conserv. 182, 155–163 (2015).

    Article  Google Scholar 

  15. Essl, F. et al. Delayed biodiversity change: no time to waste. Trends Ecol. Evol. 30, 375–378 (2015).

    Article  Google Scholar 

  16. Metzger, J. P. et al. Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol. Conserv. 142, 1166–1177 (2009).

    Article  Google Scholar 

  17. Preparations for the Post-2020 Biodiversity Framework (CBD, 2019); https://www.cbd.int/conferences/post2020

  18. Brown, C., Alexander, P., Arneth, A., Holman, I. & Rounsevell, M. Achievement of Paris climate goals unlikely due to time lags in the land system. Nat. Clim. Change 9, 203–208 (2019).

    Article  Google Scholar 

  19. MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967).

  20. Hanski, I. Metapopulation dynamics. Nature 396, 41–49 (1998).

    Article  CAS  Google Scholar 

  21. Koyanagi, T. et al. Grassland plant functional groups exhibit distinct time-lags in response to historical landscape change. Plant Ecol. 213, 327–338 (2012).

    Article  Google Scholar 

  22. Whytock, R. C. et al. Bird-community responses to habitat creation in a long-term, large-scale natural experiment. Conserv. Biol. 32, 345–354 (2018).

    Article  Google Scholar 

  23. Vellend, M. et al. Extiction debt of forest plants persists for more than a century following habitat fargmentation. Ecology 87, 542–548 (2006).

    Article  Google Scholar 

  24. Cousins, S. A. O. & Vanhoenacker, D. Detection of extinction debt depends on scale and specialisation. Biol. Conserv. 144, 782–787 (2011).

    Article  Google Scholar 

  25. Hanski, I. & Ovaskainen, O. Extinction debt at extinction threshold. Conserv. Biol. 16, 666–673 (2002).

    Article  Google Scholar 

  26. Pereira, H. M. et al. Essential biodiversity variables. Science 339, 277–278 (2013).

    Article  CAS  Google Scholar 

  27. Wild Bird Populations in England, 1970 to 2017 (Defra, 2018).

  28. Loh, J. et al. The Living Planet Index: Using species population time series to track trends in biodiversity. Philos. Trans. R. Soc. B 360, 289–295 (2005).

    Article  Google Scholar 

  29. UK Biodiversity Indicators 2019 (Defra, 2019).

  30. Fuller, R. J., Noble, D. G., Smith, K. W. & Vanhinsbergh, D. Recent declines in populations of woodland birds in Britain: a review of possible causes. Brit. Birds 98, 116–143 (2005).

    Google Scholar 

  31. Bowler, D. E., Heldbjerg, H., Fox, A. D., Jong, M. & Böhning‐Gaese, K. Long‐term declines of European insectivorous bird populations and potential causes. Conserv. Biol. 33, 1120–1130 (2019).

    Article  Google Scholar 

  32. Vickery, J. A. et al. The decline of Afro-Palaearctic migrants and an assessment of potential causes. Ibis 156, 1–22 (2014).

    Article  Google Scholar 

  33. Savory, C. J. Colonisation by woodland birds at Carrifran Wildwood: the story so far. Scot. Birds 36, 135–149 (2016).

    Google Scholar 

  34. Forestry Statistics 2018 (Forestry Commission, 2018).

  35. Quine, C. P., Bailey, S. A. & Watts, K. PRACTITIONER’S PERSPECTIVE: Sustainable forest management in a time of ecosystem services frameworks: Common ground and consequences. J. Appl. Ecol. 50, 863–867 (2013).

    Article  Google Scholar 

  36. Watts, K. et al. Using historical woodland creation to construct a long-term, large-scale natural experiment: the WrEN project. Ecol. Evol. 6, 3012–3025 (2016).

    Article  Google Scholar 

  37. Lira, P. K., Ewers, R. M., Banks-Leite, C., Pardini, R. & Metzger, J. P. Evaluating the legacy of landscape history: extinction debt and species credit in bird and small mammal assemblages in the Brazilian Atlantic Forest. J. Appl. Ecol. 49, 1325–1333 (2012).

    Article  Google Scholar 

  38. Bulman, C. R. et al. Minimum viable metapopulation size, extinction debt, and the conservation of a declining species. Ecol. Appl. 17, 1460–1473 (2007).

    Article  Google Scholar 

  39. Synes, N. W. et al. A multi-species modelling approach to examine the impact of alternative climate change adaptation strategies on range shifting ability in a fragmented landscape. Ecol. Inform. 30, 222–229 (2015).

    Article  Google Scholar 

  40. Orrock, J. L. & Watling, J. I. Local community size mediates ecological drift and competition in metacommunities. Proc. R. Soc. B 277, 2185–2191 (2010).

    Article  Google Scholar 

  41. Halley, J. M. & Iwasa, Y. Neutral theory as a predictor of avifaunal extinctions after habitat loss. Proc. Natl Acad. Sci. USA 108, 2316–2321 (2011).

    Article  CAS  Google Scholar 

  42. Bocedi, G. et al. RangeShifter: a platform for modelling spatial eco-evolutionary dynamics and species’ responses to environmental changes. Methods Ecol. Evol. 5, 388–396 (2014).

    Article  Google Scholar 

  43. Synes, N. W. et al. Emerging opportunities for landscape ecological modelling. Curr. Landsc. Ecol. Rep. 1, 146–167 (2016).

    Article  Google Scholar 

  44. Shriver, R. K. et al. Transient population dynamics impede restoration and may promote ecosystem transformation after disturbance. Ecol. Lett. 22, 1357–1366 (2019).

    Article  Google Scholar 

  45. Key Elements of the Strategic Plan 2011-2020: II. VISION (CBD, 2019); https://www.cbd.int/sp/elements/#II

  46. Hoffmann, M. et al. The difference conservation makes to extinction risk of the world’s ungulates. Conserv. Biol. 29, 1303–1313 (2015).

    Article  Google Scholar 

  47. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).

  48. Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S 4th edn (Springer, 2002).

  49. Bartoń, K. A. MuMIn: Multi-Model Inference R package version 1.42.1 (May 2019); https://cran.r-project.org/package=MuMIn

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Acknowledgements

We thank all land owners who granted us permission to conduct surveys on their land, R. Whytock, P. French and P. Barbose De Andrade for assistance with data collection. This work has been developed with funding and logistical support from the Forestry Commission, University of Stirling, Natural England, Department for Environment, Food and Rural Affairs, The National Forest Company, Scottish Natural Heritage, Tarmac and the Woodland Trust. R.C.W. was funded by the Natural Research Environment Council IAPETUS Doctoral Training Partnership (grant no. NE/L002590/1) with CASE funding from Forest Research.

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K.W., K.J.P., E.F.-M. and N.A.M. conceived and designed the WrEN Project. K.W., R.C.W., N.A.M. and P.J.K.M. designed the time-lags study. K.W., R.C.W. and S.D. collated and supplied the indicator data. R.C.W. collected and analysed the bird data. K.W. and R.C.W. wrote the manuscript. All authors discussed the results and contributed to the manuscript.

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Correspondence to Kevin Watts.

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Watts, K., Whytock, R.C., Park, K.J. et al. Ecological time lags and the journey towards conservation success. Nat Ecol Evol 4, 304–311 (2020). https://doi.org/10.1038/s41559-019-1087-8

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