Impacts of multiple stressors on freshwater biota across spatial scales and ecosystems

Abstract

Climate and land-use change drive a suite of stressors that shape ecosystems and interact to yield complex ecological responses (that is, additive, antagonistic and synergistic effects). We know little about the spatial scales relevant for the outcomes of such interactions and little about effect sizes. These knowledge gaps need to be filled to underpin future land management decisions or climate mitigation interventions for protecting and restoring freshwater ecosystems. This study combines data across scales from 33 mesocosm experiments with those from 14 river basins and 22 cross-basin studies in Europe, producing 174 combinations of paired-stressor effects on a biological response variable. Generalized linear models showed that only one of the two stressors had a significant effect in 39% of the analysed cases, 28% of the paired-stressor combinations resulted in additive effects and 33% resulted in interactive (antagonistic, synergistic, opposing or reversal) effects. For lakes, the frequencies of additive and interactive effects were similar for all spatial scales addressed, while for rivers these frequencies increased with scale. Nutrient enrichment was the overriding stressor for lakes, with effects generally exceeding those of secondary stressors. For rivers, the effects of nutrient enrichment were dependent on the specific stressor combination and biological response variable. These results vindicate the traditional focus of lake restoration and management on nutrient stress, while highlighting that river management requires more bespoke management solutions.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Location of the sampling sites and experimental sites.
Fig. 2: Stressor effect types in lakes and rivers.
Fig. 3: Explanatory power of models at different spatial scales and in different ecosystems.
Fig. 4: %AES for stressors across case studies.

Data availability

The data on the regression model outputs and the underlying paired-stressor response data are available at GitHub: https://github.com/sebastian-birk/MultiStressorImpacts.

Code availability

The R script is available at GitHub: https://github.com/sebastian-birk/MultiStressorImpacts.

References

  1. 1.

    Ormerod, S. J., Dobson, M., Hildrew, A. G. & Townsend, C. R. Multiple stressors in freshwater ecosystems. Freshw. Biol. 55, 1–4 (2010).

    Article  Google Scholar 

  2. 2.

    Côté, I. M., Darling, E. S. & Brown, C. J. Interactions among ecosystem stressors and their importance in conservation. Proc. R. Soc. B 283, 20152592 (2016).

    PubMed  Article  Google Scholar 

  3. 3.

    van Dijk, G. M., van Liere, L., Admiraal, W., Bannink, B. A. & Cappon, J. J. Present state of the water quality of European rivers and implications for management. Sci. Total Environ. 145, 187–195 (1994).

    Article  Google Scholar 

  4. 4.

    Richardson, J. et al. Effects of multiple stressors on cyanobacteria abundance varies with lake type. Glob. Change Biol. 24, 5044–5055 (2018).

    Article  Google Scholar 

  5. 5.

    Schäfer, R. B., Kühn, B., Malaj, E., König, A. & Gergs, R. Contribution of organic toxicants to multiple stress in river ecosystems. Freshw. Biol. 61, 2116–2128 (2016).

    Article  CAS  Google Scholar 

  6. 6.

    Schinegger, R., Palt, M., Segurado, P. & Schmutz, S. Untangling the effects of multiple human stressors and their impacts on fish assemblages in European running waters. Sci. Total Environ. 573, 1079–1088 (2016).

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Folt, C. L. et al. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 44, 864–877 (1999).

    Article  Google Scholar 

  8. 8.

    Nõges, P. et al. Quantified biotic and abiotic responses to multiple stress in freshwater, marine and ground waters. Sci. Total Environ. 540, 43–52 (2016).

    PubMed  Article  CAS  Google Scholar 

  9. 9.

    Piggott, J. J., Townsend, C. R. & Matthaei, C. D. Reconceptualizing synergism and antagonism among multiple stressors. Ecol. Evol. 5, 1538–1547 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Jackson, M. C., Loewen, C. J. G., Vinebrooke, R. D. & Chimimba, C. T. Net effects of multiple stressors in freshwater ecosystems: a meta-analysis. Glob. Change Biol. 22, 180–189 (2016).

    Article  Google Scholar 

  11. 11.

    De Laender, F. Community- and ecosystem-level effects of multiple environmental change drivers: beyond null model testing. Glob. Change Biol. 24, 5021–5030 (2018).

    Article  Google Scholar 

  12. 12.

    Skjelkvåle, B. L. et al. Regional scale evidence for improvements in surface water chemistry 1990–2001. Environ. Pollut. 137, 165–176 (2005).

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Reid, A. J. et al. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol. Rev. 94, 849–873 (2019).

    PubMed  Article  Google Scholar 

  14. 14.

    Palmer, M. A., Menninger, H. L. & Bernhardt, E. River restoration, habitat heterogeneity and biodiversity: a failure of theory or practice? Freshw. Biol. 55, 205–222 (2010).

    Article  Google Scholar 

  15. 15.

    Vinebrooke, R., Cottingham, K. & Norberg, M. Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co‐tolerance. Oikos 3, 451–457 (2004).

    Article  Google Scholar 

  16. 16.

    Schäfer, R. B. & Piggott, J. J. Advancing understanding and prediction in multiple stressor research through a mechanistic basis for null models. Glob. Change Biol. 24, 1817–1826 (2018).

    Article  Google Scholar 

  17. 17.

    Thorp, J. H., Thoms, M. C. & Delong, M. D. The riverine ecosystem synthesis: biocomplexity in river networks across space and time. River Res. Appl. 22, 123–147 (2006).

    Article  Google Scholar 

  18. 18.

    Brucet, S. et al. Fish diversity in European lakes: geographical factors dominate over anthropogenic pressures. Freshw. Biol. 58, 1779–1793 (2013).

    Article  Google Scholar 

  19. 19.

    Feld, C. K. et al. Disentangling the effects of land use and geo-climatic factors on diversity in European freshwater ecosystems. Ecol. Indic. 60, 71–83 (2016).

    Article  Google Scholar 

  20. 20.

    European Waters: Assessment of Status and Pressures 2018 (European Environment Agency, 2018); https://www.eea.europa.eu/publications/state-of-water/

  21. 21.

    Jeppesen, E. et al. Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw. Biol. 50, 1747–1771 (2005).

    CAS  Article  Google Scholar 

  22. 22.

    Hering, D. et al. Assessment of European rivers with diatoms, macrophytes, invertebrates and fish: a comparative metric-based analysis of organism response to stress. Freshw. Biol. 51, 1757–1785 (2006).

    Article  Google Scholar 

  23. 23.

    Griffen, B. D., Belgrad, B. A., Cannizzo, Z. J., Knotts, E. R. & Hancock, E. R. Rethinking our approach to multiple stressor studies in marine environments. Mar. Ecol. Prog. Ser. 543, 273–281 (2016).

    Article  Google Scholar 

  24. 24.

    Davies, B. R., Biggs, J., Williams, P. J., Lee, J. T. & Thompson, S. A comparison of the catchment sizes of rivers, streams, ponds, ditches and lakes: implications for protecting aquatic biodiversity in an agricultural landscape. Hydrobiologia 597, 7–17 (2008).

    Article  Google Scholar 

  25. 25.

    Fuller, I. C. & Death, R. G. The science of connected ecosystems: what is the role of catchment-scale connectivity for healthy river ecology? Land Degrad. Dev. 29, 1413–1426 (2018).

    Article  Google Scholar 

  26. 26.

    Benda, L. et al. The network dynamics hypothesis: how channel networks structure riverine habitats. Bioscience 54, 413–427 (2004).

    Article  Google Scholar 

  27. 27.

    Liess, M. et al. Effects of Pesticides in the Field (Society of Environmental Toxicology and Chemistry, 2005).

  28. 28.

    Price, K. J. & Carrick, H. J. Effects of experimental nutrient loading on phosphorus uptake by biofilms: evidence for nutrient saturation in mid-Atlantic streams. Freshw. Sci. 35, 503–517 (2016).

    Article  Google Scholar 

  29. 29.

    McCall, S. J., Hale, M. S., Smith, J. T., Read, D. S. & Bowes, M. J. Impacts of phosphorus concentration and light intensity on river periphyton biomass and community structure. Hydrobiologia 792, 315–330 (2017).

    CAS  Article  Google Scholar 

  30. 30.

    Birk, S. in Multiple Stress in River Ecosystems: Status, Impacts and Prospects for the Future (eds Sabater, S. et al.) 235–253 (Academic Press, 2019); https://doi.org/10.1016/B978-0-12-811713-2.00014-5

  31. 31.

    Birk, S. et al. Three hundred ways to assess Europe’s surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecol. Indic. 18, 31–41 (2012).

    Article  Google Scholar 

  32. 32.

    Moss, B. et al. Allied attack: climate change and eutrophication. Inland Waters 1, 101–105 (2011).

    Article  Google Scholar 

  33. 33.

    Richardson, J. et al. The response of cyanobacteria and phytoplankton abundance to warming, extreme rainfall events and nutrient enrichment. Glob. Change Biol. 25, 3365–3380 (2019).

    Article  Google Scholar 

  34. 34.

    Jeppesen, E. et al. Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646, 73–90 (2010).

    CAS  Article  Google Scholar 

  35. 35.

    Monteith, D. T. et al. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450, 537–540 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. 36.

    Graneli, W. in Encyclopedia of Lakes and Reservoirs (eds Bengtsson, L. et al.) 117–119 (Springer Netherlands, 2012); https://doi.org/10.1007/978-1-4020-4410-6_256

  37. 37.

    Segner, H., Schmitt-Jansen, M. & Sabater, S. Assessing the impact of multiple stressors on aquatic biota: the receptor’s side matters. Environ. Sci. Technol. 48, 7690–7696 (2014).

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Baattrup-Pedersen, A. & Riis, T. Macrophyte diversity and composition in relation to substratum characteristics in regulated and unregulated Danish streams. Freshw. Biol. 42, 375–385 (1999).

    Article  Google Scholar 

  39. 39.

    Schneider, S. C. et al. Unravelling the effect of flow regime on macroinvertebrates and benthic algae in regulated versus unregulated streams. Ecohydrology 11, e1996 (2018).

    Article  Google Scholar 

  40. 40.

    de Zwart, D. & Posthuma, L. Complex mixture toxicity for single and multiple species: proposed methodologies. Environ. Toxicol. Chem. 24, 2665–2676 (2005).

    PubMed  Article  Google Scholar 

  41. 41.

    Busch, W. et al. Micropollutants in European rivers: a mode of action survey to support the development of effect-based tools for water monitoring. Environ. Toxicol. Chem. 35, 1887–1899 (2016).

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Malaj, E. et al. Organic chemicals jeopardize the health of freshwater ecosystems on the continental scale. Proc. Natl Acad. Sci. USA 111, 9549–9554 (2014).

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Hering, D. et al. Managing aquatic ecosystems and water resources under multiple stress—an introduction to the MARS project. Sci. Total Environ. 503, 10–21 (2015).

    PubMed  Article  CAS  Google Scholar 

  44. 44.

    Moe, S. J., Dudley, B. & Ptacnik, R. REBECCA databases: experiences from compilation and analyses of monitoring data from 5,000 lakes in 20 European countries. Aquat. Ecol. 42, 183–201 (2008).

    CAS  Article  Google Scholar 

  45. 45.

    Moe, S. J., Schmidt-Kloiber, A., Dudley, B. J. & Hering, D. The WISER way of organising ecological data from European rivers, lakes, transitional and coastal waters. Hydrobiologia 704, 11–28 (2013).

    Article  Google Scholar 

  46. 46.

    Sabater, S., Ludwig, R. & Elosegi, A. in Multiple Stress in River Ecosystems: Status, Impacts and Prospects for the Future (eds Sabater, S. et al.) 1–22 (Academic Press, 2019); https://doi.org/10.1016/B978-0-12-811713-2.00001-7

  47. 47.

    Liess, M. & von der Ohe, P. C. Analyzing effects of pesticides on invertebrate communities in streams. Environ. Toxicol. 24, 954–965 (2005).

    CAS  Article  Google Scholar 

  48. 48.

    von der Ohe, P. C. & Goedkoop, W. Distinguishing the effects of habitat degradation and pesticide stress on benthic invertebrates using stressor-specific metrics. Sci. Total Environ. 444, 480–490 (2013).

    PubMed  Article  CAS  Google Scholar 

  49. 49.

    Lyche Solheim, A. et al. A new broad typology for rivers and lakes in Europe: development and application for large-scale environmental assessments. Sci. Total Environ. 697, 134043 (2019).

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Box, G. E. P. & Cox, D. R. An analysis of transformations. J. R. Stat. Soc. B 26, 211–252 (1964).

    Google Scholar 

  51. 51.

    R Core Team R: A Language and Environment for Statistical Computing v.3.6.1 (R Foundation for Statistical Computing, 2019); http://www.r-project.org/index.html

  52. 52.

    Dormann, C. F. et al. Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography (Cop.) 30, 609–628 (2007).

    Article  Google Scholar 

  53. 53.

    Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the MARS project (Managing Aquatic Ecosystems and Water Resources under Multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), contract no. 603378 (http://www.mars-project.eu). Further support was received through the ILES (SAW-2015-IGB-1) and BIBS (BMBF 01LC1501G) projects. Partner organizations provided 25% cofunding through their institutional budgets. We thank J. Strackbein, J. Lorenz and L. Mack for their support.

Author information

Affiliations

Authors

Contributions

D.C., L.C., B.M.S., S.B., L.B., S.J.T. and D.H. conceptualized the study. D.C. and S.B. curated the data. D.H., L.C. and S.B. acquired the funding and administered the project. A.B., A.G., A.S., B.M.S., C.A., C.G.-C., C.P., D.d.Z., D.G., E.B.-K., F.C., G.P., J.J.R., J.R., J.T., J.U.L., K.R., K.S., L.P., L.S., M.C.U., M.J., N.K., N.W., P.B., P.S., P.C.v.d.O., R.B.S., R.-M.C., R.S., S.A., S.B., S.C.S., S.J.M., S.L., S.P., S.J.T., T.B., U.I. and U.M. provided the data and/or conducted the formal analysis. A.B.-P., A.L.S., D.G., E.B.-K., E.J., H.F., J.M.S., J.R., L.C., L.S., M.O.G., P.B., S.A., S.C.S., S.S. and W.G. conducted the experimental investigations. S.B., D.H., B.M.S., M.O.G. and D.C. wrote the manuscript. H.E.A., M.B., A.D.B., A.C.C., C.K.F., M.T.F., M.O.G., L.G., J.H., M.K., P.N., T.N., S.J.O., Y.P., B.S., M.V. and the aforementioned authors reviewed the manuscript and provided the necessary amendments.

Corresponding author

Correspondence to Sebastian Birk.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2, and references.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Birk, S., Chapman, D., Carvalho, L. et al. Impacts of multiple stressors on freshwater biota across spatial scales and ecosystems. Nat Ecol Evol (2020). https://doi.org/10.1038/s41559-020-1216-4

Download citation

Further reading