Abstract

Global change threatens invertebrate biodiversity and its central role in numerous ecosystem functions and services. Functional trait analyses have been advocated to uncover global mechanisms behind biodiversity responses to environmental change, but the application of this approach for invertebrates is underdeveloped relative to other organism groups. From an evaluation of 363 records comprising >1.23 million invertebrates collected from rivers across nine biogeographic regions on three continents, consistent responses of community trait composition and diversity to replicated gradients of reduced glacier cover are demonstrated. After accounting for a systematic regional effect of latitude, the processes shaping river invertebrate functional diversity are globally consistent. Analyses nested within individual regions identified an increase in functional diversity as glacier cover decreases. Community assembly models demonstrated that dispersal limitation was the dominant process underlying these patterns, although environmental filtering was also evident in highly glacierized basins. These findings indicate that predictable mechanisms govern river invertebrate community responses to decreasing glacier cover globally.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Additional information

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

References

  1. 1.

    Wilson, E. O. The little things that run the world (the importance and conservation of invertebrates). Conserv. Biol. 1, 344–346 (1987).

  2. 2.

    Lewbart, G. A. Invertebrate Medicine (Blackwell, Oxford, 2006).

  3. 3.

    Collen, B., Böhm, M., Kemp, R. & Baillie, J. E. M. Spineless: Status and Trends of the World’s Invertebrates (Zoological Society of London, London, 2012).

  4. 4.

    Stuart-Smith, R. D. et al. Integrating abundance and functional traits reveals new global hotspots of fish diversity. Nature 501, 539–542 (2013).

  5. 5.

    Díaz, S. et al. The global spectrum of plant form and function. Nature 529, 167–171 (2016).

  6. 6.

    Huang, S., Stephens, P. R. & Gittleman, J. L. Traits, trees and taxa: global dimensions of biodiversity in mammals. Proc. R. Soc. B 279, 4997–5003 (2012).

  7. 7.

    Thomas, M. K., Kremer, C. T., Klausmeier, C. A. & Litchman, E. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088 (2012).

  8. 8.

    Kunstler, G. et al. Plant functional traits have globally consistent effects on competition. Nature 529, 204–207 (2016).

  9. 9.

    Southwood, T. R. E. Tactics, strategies and templets. Oikos 52, 3–18 (1988).

  10. 10.

    Poff, N. L. Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. J. North. Am. Benthol. Soc. 16, 391–409 (1997).

  11. 11.

    Gardner, A. S. et al. A reconciled estimate of glacier contributions to sea level rise: 2003 to 2009. Science 340, 852–857 (2013).

  12. 12.

    Milner, A. M. et al. Glacier shrinkage driving global changes in downstream systems. Proc. Natl Acad. Sci. USA 114, 9770–9778 (2017).

  13. 13.

    Zemp, M. et al. Historically unprecedented global glacier decline in the early 21st century. J. Glaciol. 61, 745–762 (2015).

  14. 14.

    Milner, A. M., Brown, L. E. & Hannah, D. M. Hydroecological response of river systems to shrinking glaciers. Hydrol. Process. 23, 62–77 (2009).

  15. 15.

    Brown, L. E., Céréghino, R. & Compin, A. Endemic freshwater invertebrates from southern France: diversity, distribution and conservation implications. Biol. Conserv. 142, 2613–2619 (2009).

  16. 16.

    Jacobsen, D., Milner, A. M., Brown, L. E. & Dangles, O. Biodiversity under threat in glacier-fed river systems. Nat. Clim. Change 2, 361–364 (2012).

  17. 17.

    Kammerlander, B. et al. High diversity of protistan plankton communities in remote high mountain lakes in the European Alps and the Himalayan mountains. FEMS Microbiol. Ecol. 91, fiv010 (2015).

  18. 18.

    Statzner, B. & Bêche, L. A. Can biological invertebrate traits resolve effects of multiple stressors on running water ecosystems? Freshw. Biol. 55, 80–119 (2010).

  19. 19.

    Brown, L. E. & Milner, A. M. Rapid loss of glacial ice reveals stream community assembly processes. Glob. Change Biol. 18, 2195–2204 (2012).

  20. 20.

    Milner, A. M., Brittain, J. E., Castella, E. & Petts, G. E. Trends of macroinvertebrate community structure in glacier-fed rivers in relation to environmental conditions: a synthesis. Freshw. Biol. 46, 1833–1848 (2001).

  21. 21.

    Leibold, M. A. et al. The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7, 601–613 (2004).

  22. 22.

    Shipley, B. Measuring and interpreting trait‐based selection versus meta‐community effects during local community assembly. J. Veg. Sci. 25, 55–65 (2014).

  23. 23.

    Heino, J. et al. Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshw. Biol. 60, 845–869 (2015).

  24. 24.

    Winegardner, A. K., Jones, B. K., Ng, I. S., Siqueira, T. & Cottenie, K. The terminology of metacommunity ecology. Trends Ecol. Evol. 27, 253–254 (2012).

  25. 25.

    Karger, D. N. et al. Delineating probabilistic species pools in ecology and biogeography. Glob. Ecol. Biogeogr. 25, 489–501 (2016).

  26. 26.

    Laughlin, D. C., Joshi, C., Bodegom, P. M., Bastow, Z. A. & Fulé, P. Z. A predictive model of community assembly that incorporates intraspecific trait variation. Ecol. Lett. 15, 1291–1299 (2012).

  27. 27.

    Brown, L. E., Dickson, N. E., Carrivick, J. L. & Füreder, L. Alpine river ecosystem response to glacial and anthropogenic flow pulses. Freshw. Sci. 34, 1201–1215 (2015).

  28. 28.

    Rohde, K. Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65, 514–527 (1992).

  29. 29.

    Harrison, S. & Cornell, H. Toward a better understanding of the regional causes of local community richness. Ecol. Lett. 11, 969–979 (2008).

  30. 30.

    Verberk, W. C. E. P., van Noordwijk, C. G. E. & Hildrew, A. G. Delivering on a promise: integrating species traits to transform descriptive community ecology into a predictive science. Freshw. Sci. 32, 531–547 (2013).

  31. 31.

    Finn, D. S. & Poff, N. L. Examining spatial concordance of genetic and species diversity patterns to evaluate the role of dispersal limitation in structuring headwater metacommunities. J. North. Am. Benthol. Soc. 30, 273–283 (2011).

  32. 32.

    Robinson, C. T., Tonolla, D., Imhof, B., Vukelic, R. & Uehlinger, U. Flow intermittency, physico-chemistry and function of headwater streams in an Alpine glacial catchment. Aquat. Sci. 78, 327–341 (2016).

  33. 33.

    Thompson, P. L. & Gonzalez, A. Dispersal governs the reorganization of ecological networks under environmental change. Nat. Ecol. Evol. 1, 0162 (2017).

  34. 34.

    Bêche, L. A. & Statzner, B. Richness gradients of stream invertebrates across the USA: taxonomy- and trait-based approaches. Biodivers. Conserv. 18, 3909–3930 (2009).

  35. 35.

    Bonada, N., Dolédec, S. & Statzner, B. Taxonomic and biological trait differences of stream macroinvertebrate communities between mediterranean and temperate regions: implications for future climatic scenarios. Glob. Change Biol. 13, 1658–1671 (2007).

  36. 36.

    Jacobsen, D. & Dangles, O. Environmental harshness and global richness patterns in glacier-fed streams. Glob. Ecol. Biogeogr. 21, 647–656 (2012).

  37. 37.

    Lamanna, C. et al. Functional trait space and the latitudinal diversity gradient. Proc. Natl Acad. Sci. USA 111, 13745–13750 (2014).

  38. 38.

    Chapin, F. S. III & Körner, C. (eds) Arctic and Alpine Biodiversity: Patterns, Causes and Ecosystem Consequences (Springer-Verlag, Berlin Heidelberg, 1995).

  39. 39.

    Shugar, D. H. et al. River piracy and drainage basin regorganization led by climate-driven glacier retreat. Nat. Geosci. 10, 370–375 (2017).

  40. 40.

    Cauvy-Fraunié, S. et al. Ecological responses to experimental glacier-runoff reduction in alpine rivers. Nat. Commun. 7, 12025 (2016).

  41. 41.

    Brown, L. E., Hannah, D. M. & Milner, A. M. Vulnerability of alpine stream biodiversity to shrinking glaciers and snowpacks. Glob. Change Biol. 13, 958–966 (2007).

  42. 42.

    Woodward, G. et al. Continental-scale effects of nutrient pollution on stream ecosystem functioning. Science 336, 1438–1440 (2012).

  43. 43.

    Serra, S. R. Q., Cobo, F., Graça, M. A. S., Dolédec, S. & Feio, M. J. Synthesising the trait information of European Chironomidae (Insecta: Diptera): towards a new database. Ecol. Indic. 61, 282–292 (2016).

  44. 44.

    Tachet, H., Richoux, P., Bournaud, M. & Usseglio-Polatera, P. Invertébrés d’Eau Douce. Systématique, Biologie, Ecologie 2nd edn (CNRS, 2002).

  45. 45.

    Poff, N. L. et al. Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J. North. Am. Benthol. Soc. 25, 730–755 (2006).

  46. 46.

    Vieira, N. K. M. et al. A Database of Lotic Invertebrate Traits for North America Data Series 187 (US Department of the Interior and US Geological Survey, Reston, 2006).

  47. 47.

    Phillips, N. Stream biomonitoring using species traits. Water & Atmosphere 12, 8–9 (2004).

  48. 48.

    Ilg, C. & Castella, E. Patterns of macroinvertebrate traits along three glacial stream continuums. Freshw. Biol. 51, 840–853 (2006).

  49. 49.

    Menezes, S., Baird, D. J. & Soares, A. M. V. M. Beyond taxonomy: a review of macroinvertebrate trait based community descriptors as tools for freshwater biomonitoring. J. Appl. Ecol. 47, 711–719 (2010).

  50. 50.

    Chevenet, F., Dolédec, S. & Chessel, D. A fuzzy coding approach for analysis of long-term ecological data. Freshw. Biol. 31, 295–309 (1994).

  51. 51.

    Dray, S. & Dufour, A. B. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).

  52. 52.

    Pavoine, S., Vallet, J., Dufour, A.-B., Gachet, S. & Daniel, H. On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118, 391–402 (2009).

  53. 53.

    Darling, E. S., Alvarez-Filip, L., Oliver, T. A., McClanahan, T. R. & Côté, I. M. Evaluating life-history strategies of reef corals from species traits. Ecol. Lett. 15, 1378–1386 (2012).

  54. 54.

    Mouchet, M. A., Villéger, S., Mason, N. W. H. & Mouillot, D. Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct. Ecol. 24, 867–876 (2010).

  55. 55.

    Laliberté, E. & Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010).

  56. 56.

    Cailliez, F. The analytical solution of the additive constant problem. Psychometrika 48, 305–308 (1983).

  57. 57.

    Götzenberger, L. et al. Which randomizations detect convergence and divergence in trait-based community assembly? A test of commonly used null models. J. Veg. Sci. 27, 1275–1287 (2016).

  58. 58.

    Legendre, P., Fortin, M.-J. & Borcard, D. Should the Mantel test be used in spatial analysis? Methods Ecol. Evol. 6, 1239–1247 (2015).

  59. 59.

    Lewis, J. Turbidity-controlled suspended sediment sampling for runoff-event load estimation. Water Resour. Res. 32, 2299–2310 (1996).

Download references

Acknowledgements

This work was funded by the following organizations: the UK Natural Environment Research Council grants and studentships GR9/2913, NE/E003729/1, NE/E004539/1, NE/E004148/1, NE/G523963/1, NER/S/A/2003/11192 and NE/L002574/1; the European Union Environment and Climate Programme Arctic and Alpine Stream Ecosystem Research (AASER) project (ENV-CT95-0164); EU-FP7 Assessing Climate impacts on the Quality and quantity of WAter (ACQWA) project (212250); the Icelandic Research Council (954890095, 954890096); the University of Iceland Research Fund (GMG96, GMG97, GMG98), Wyoming Center for Environmental Hydrology and Geophysics-National Science Foundation (1208909); USA-Wyoming NASA Space Grant Faculty Research Initiation (NNX10A095H); USA-NSF Wyoming Epscor; Nationalpark Hohe Tauern, Austria; the Royal Society (International Outgoing Grant 2006/R4); the Leverhulme Trust; the Universities of Leeds, Birmingham, Iceland and Innsbruck; the European Centre for Arctic Environmental Research (ARCFAC): a Research Infrastructures Action of the European Community FP6 (026129-2008-72); the Stelvio National Park (2000–2001); the Autonomous Province of Trento (HIGHEST project, 2001–2004, del. PAT no. 1060/2001; VETTA project, 2003–2006, del. PAT no. 3402/2002); MUSE-Museo delle Scienze. We are grateful to R. Taylor and M. Winterbourn at the University of Canterbury, New Zealand, who helped to collect New Zealand invertebrate data and assisted with identification, and to H. Adalsteinsson, who contributed to data collection in Iceland. Many other people, too numerous to mention, assisted with fieldwork at all of the study locations. The European Science Foundation sponsored an exploratory workshop entitled `Glacier-fed rivers, hydroecology and climate change: current knowledge and future network of monitoring sites (GLAC-HYDROECO-NET)' that was held in Birmingham, UK in September of 2013 where some of the ideas in this paper were first discussed. We are grateful to R. Death, J. Lento, N. Phillips and M. Winterbourn for reviewing the traits database fuzzy codes. T. Baker, D. Galbraith and M. Van de Wiel provided helpful comments on an earlier version of the manuscript.

Author information

Affiliations

  1. water@leeds and School of Geography, University of Leeds, Leeds, UK

    • Lee E. Brown
    • , Jonathan L. Carrivick
    • , Sarah Fell
    • , Nikolai Friberg
    •  & William H. M. James
  2. School of Geography, Earth & Environmental Sciences, University of Birmingham, Birmingham, UK

    • Kieran Khamis
    • , Phillip Blaen
    • , David M. Hannah
    •  & Alexander M. Milner
  3. Centre for Agroecology, Water and Resilience, Coventry University, Coventry, UK

    • Martin Wilkes
  4. Natural History Museum, University of Oslo, Oslo, Norway

    • John E. Brittain
    •  & Svein J. Saltveit
  5. Norsk Institutt for Vannforskning, Oslo, Norway

    • Nikolai Friberg
  6. River Ecology and Conservation Research, Institute of Ecology, University of Innsbruck, Innsbruck, Austria

    • Leopold Füreder
  7. Institute of Life and Environmental Sciences, University of Iceland, Reykjavik, Iceland

    • Gisli M. Gislason
  8. Environment Agency, Solihull, UK

    • Sarah Hainie
  9. Invertebrate Zoology and Hydrobiology Department, MUSE-Museo delle Scienze, Trento, Italy

    • Valeria Lencioni
  10. Marine and Freshwater Research Institute, Reykjavík, Iceland

    • Jon S. Olafsson
  11. EAWAG, Dübendorf, Switzerland

    • Christopher T. Robinson
  12. Department of Environmental Science, Western Wyoming Community College, Rock Springs, WY, USA

    • Craig Thompson
  13. Institute of Arctic Biology, University of Alaska, Fairbanks, AK, USA

    • Alexander M. Milner

Authors

  1. Search for Lee E. Brown in:

  2. Search for Kieran Khamis in:

  3. Search for Martin Wilkes in:

  4. Search for Phillip Blaen in:

  5. Search for John E. Brittain in:

  6. Search for Jonathan L. Carrivick in:

  7. Search for Sarah Fell in:

  8. Search for Nikolai Friberg in:

  9. Search for Leopold Füreder in:

  10. Search for Gisli M. Gislason in:

  11. Search for Sarah Hainie in:

  12. Search for David M. Hannah in:

  13. Search for William H. M. James in:

  14. Search for Valeria Lencioni in:

  15. Search for Jon S. Olafsson in:

  16. Search for Christopher T. Robinson in:

  17. Search for Svein J. Saltveit in:

  18. Search for Craig Thompson in:

  19. Search for Alexander M. Milner in:

Contributions

Proposed the study: L.E.B., K.K., A.M.M. Collected data: L.E.B., K.K., P.B., J.E.B., J.L.C., S.F., N.F., L.F., G.M.G., D.M.H., S.H., W.H.M.J., V.L., J.S.O., C.T.R., S.J.S., C.T., A.M.M. Developed databases: L.E.B., K.K., A.M.M., M.W. Analysed data: L.E.B., K.K., M.W. Wrote paper: L.E.B., K.K., M.W., A.M.M. with input from all other authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Lee E. Brown.

Supplementary information

  1. Supplementary Information

    Supplementary Tables 1–7, Supplementary Figures 1–6, Supplementary References.

  2. Life Sciences Reporting Summary

About this article

Publication history

Received

Accepted

Published

Issue Date

DOI

https://doi.org/10.1038/s41559-017-0426-x

Further reading