Multi-decadal improvements in the ecological quality of European rivers are not consistently reflected in biodiversity metrics.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
26 Jan 2024
26 Jan 2024
Historique:
received:
26
06
2023
accepted:
11
12
2023
medline:
27
1
2024
pubmed:
27
1
2024
entrez:
26
1
2024
Statut:
aheadofprint
Résumé
Humans impact terrestrial, marine and freshwater ecosystems, yet many broad-scale studies have found no systematic, negative biodiversity changes (for example, decreasing abundance or taxon richness). Here we show that mixed biodiversity responses may arise because community metrics show variable responses to anthropogenic impacts across broad spatial scales. We first quantified temporal trends in anthropogenic impacts for 1,365 riverine invertebrate communities from 23 European countries, based on similarity to least-impacted reference communities. Reference comparisons provide necessary, but often missing, baselines for evaluating whether communities are negatively impacted or have improved (less or more similar, respectively). We then determined whether changing impacts were consistently reflected in metrics of community abundance, taxon richness, evenness and composition. Invertebrate communities improved, that is, became more similar to reference conditions, from 1992 until the 2010s, after which improvements plateaued. Improvements were generally reflected by higher taxon richness, providing evidence that certain community metrics can broadly indicate anthropogenic impacts. However, richness responses were highly variable among sites, and we found no consistent responses in community abundance, evenness or composition. These findings suggest that, without sufficient data and careful metric selection, many common community metrics cannot reliably reflect anthropogenic impacts, helping explain the prevalence of mixed biodiversity trends.
Identifiants
pubmed: 38278985
doi: 10.1038/s41559-023-02305-4
pii: 10.1038/s41559-023-02305-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 310030_197410
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 31003A_173074
Organisme : European Commission (EC)
ID : LIFE18 NAT/ES/000121
Organisme : European Commission (EC)
ID : LIFE18 NAT/ES/000121
Organisme : Lietuvos Mokslo Taryba (Research Council of Lithuania)
ID : S-PD-22-72
Organisme : Lietuvos Mokslo Taryba (Research Council of Lithuania)
ID : S-PD-22-72
Organisme : Ministry of Education and Science | Fundação para a Ciência e a Tecnologia (Portuguese Science and Technology Foundation)
ID : UIDB/04292/2020
Organisme : Ministry of Education and Science | Fundação para a Ciência e a Tecnologia (Portuguese Science and Technology Foundation)
ID : UIDP/04292/2020
Organisme : Ministry of Education and Science | Fundação para a Ciência e a Tecnologia (Portuguese Science and Technology Foundation)
ID : LA/P/0069/2020
Organisme : Academy of Finland (Suomen Akatemia)
ID : 331957
Organisme : Eesti Teadusagentuur (Estonian Research Council)
ID : PRG1266
Organisme : EC | Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020)
ID : 871128
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57 (2011).
pubmed: 21368823
doi: 10.1038/nature09678
Ceballos, G. et al. Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).
pubmed: 26601195
pmcid: 4640606
doi: 10.1126/sciadv.1400253
Yasuhara, M., Hunt, G., Breitburg, D., Tsujimoto, A. & Katsuki, K. Human-induced marine ecological degradation: micropaleontological perspectives. Ecol. Evol. 2, 3242–3268 (2012).
pubmed: 23301187
pmcid: 3539015
doi: 10.1002/ece3.425
Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).
pubmed: 25832402
doi: 10.1038/nature14324
Reid, A. J. et al. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol. Rev. 94, 849–873 (2019).
pubmed: 30467930
doi: 10.1111/brv.12480
Tickner, D. et al. Bending the curve of global freshwater biodiversity loss: an emergency recovery plan. BioScience 70, 330–342 (2020).
pubmed: 32284631
pmcid: 7138689
doi: 10.1093/biosci/biaa002
Vellend, M. et al. Global meta-analysis reveals no net change in local-scale plant biodiversity over time. Proc. Natl Acad. Sci. USA 110, 19456–19459 (2013).
pubmed: 24167259
pmcid: 3845118
doi: 10.1073/pnas.1312779110
Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science 344, 296–299 (2014).
pubmed: 24744374
doi: 10.1126/science.1248484
Blowes, S. A. et al. The geography of biodiversity change in marine and terrestrial assemblages. Science 366, 339–345 (2019).
pubmed: 31624208
doi: 10.1126/science.aaw1620
Millette, K. L. et al. No consistent effects of humans on animal genetic diversity worldwide. Ecol. Lett. 23, 55–67 (2020).
pubmed: 31637822
doi: 10.1111/ele.13394
Pilotto, F. et al. Meta-analysis of multidecadal biodiversity trends in Europe. Nat. Commun. 11, 3486 (2020).
pubmed: 32661354
pmcid: 7359034
doi: 10.1038/s41467-020-17171-y
van Klink, R. et al. Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 368, 417–420 (2020).
pubmed: 32327596
doi: 10.1126/science.aax9931
Outhwaite, C. L., Gregory, R. D., Chandler, R. E., Collen, B. & Isaac, N. J. B. Complex long-term biodiversity change among invertebrates, bryophytes and lichens. Nat. Ecol. Evol. 4, 384–392 (2020).
pubmed: 32066888
doi: 10.1038/s41559-020-1111-z
Wagner, D. L., Fox, R., Salcido, D. M. & Dyer, L. A. A window to the world of global insect declines: moth biodiversity trends are complex and heterogeneous. Proc. Natl Acad. Sci. USA 118, e2002549117 (2021).
pubmed: 33431565
pmcid: 7812805
doi: 10.1073/pnas.2002549117
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).
pubmed: 23692632
pmcid: 3738924
doi: 10.1111/ele.12121
Schipper, A. M. et al. Contrasting changes in the abundance and diversity of North American bird assemblages from 1971 to 2010. Glob. Change Biol. 22, 3948–3959 (2016).
doi: 10.1111/gcb.13292
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).
pubmed: 29045418
pmcid: 5646769
doi: 10.1371/journal.pone.0185809
Haase, P. et al. The recovery of European freshwater biodiversity has come to a halt. Nature 620, 582–588 (2023).
pubmed: 37558875
pmcid: 10432276
doi: 10.1038/s41586-023-06400-1
de los Santos, C. B. et al. Recent trend reversal for declining European seagrass meadows. Nat. Commun. 10, 3356 (2019).
doi: 10.1038/s41467-019-11340-4
Kuczynski, L., Ontiveros, V. J. & Hillebrand, H. Biodiversity time series are biased towards increasing species richness in changing environments. Nat. Ecol. Evol. 7, 994–1001 (2023).
pubmed: 37277495
pmcid: 10333117
doi: 10.1038/s41559-023-02078-w
Gonzalez, A. et al. Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity. Ecology 97, 1949–1960 (2016).
pubmed: 27859190
doi: 10.1890/15-1759.1
Cardinale, B. J., Gonzalez, A., Allington, G. R. H. & Loreau, M. Is local biodiversity declining or not? A summary of the debate over analysis of species richness time trends. Biol. Conserv. 219, 175–183 (2018).
doi: 10.1016/j.biocon.2017.12.021
Valdez, J. W. et al. The undetectability of global biodiversity trends using local species richness. Ecography 2023, e06604 (2023).
doi: 10.1111/ecog.06604
Catford, J. A., Wilson, J. R. U., Pyšek, P., Hulme, P. E. & Duncan, R. P. Addressing context dependence in ecology. Trends Ecol. Evol. 37, 158–170 (2022).
pubmed: 34756764
doi: 10.1016/j.tree.2021.09.007
Elahi, R. et al. Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr. Biol. 25, 1938–1943 (2015).
pubmed: 26166784
doi: 10.1016/j.cub.2015.05.030
Hillebrand, H. et al. Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J. Appl. Ecol. 55, 169–184 (2018).
doi: 10.1111/1365-2664.12959
Ludsin, S. A., Kershner, M. W., Blocksom, K. A., Knight, R. L. & Stein, R. A. Life after death in Lake Erie: nutrient controls drive fish species richness, rehabilitation. Ecol. Appl. 11, 731–746 (2001).
doi: 10.1890/1051-0761(2001)011[0731:LADILE]2.0.CO;2
Fournier, A. M. V., White, E. R. & Heard, S. B. Site-selection bias and apparent population declines in long-term studies. Conserv. Biol. 33, 1370–1379 (2019).
pubmed: 31210365
doi: 10.1111/cobi.13371
Magurran, A. E. et al. Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. Trends Ecol. Evol. 25, 574–582 (2010).
pubmed: 20656371
doi: 10.1016/j.tree.2010.06.016
Bonada, N., Prat, N., Resh, V. H. & Statzner, B. Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches. Annu. Rev. Entomol. 51, 495–523 (2006).
pubmed: 16332221
doi: 10.1146/annurev.ento.51.110104.151124
Pharaoh, E., Diamond, M., Ormerod, S. J., Rutt, G. & Vaughan, I. P. Evidence of biological recovery from gross pollution in English and Welsh rivers over three decades. Sci. Total Environ. 878, 163107 (2023).
pubmed: 36972879
doi: 10.1016/j.scitotenv.2023.163107
Water Framework Directive (WFD). Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. Off. J. Eur. Comm. 327, 1–72 (2000).
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).
doi: 10.1016/j.ecolind.2011.10.009
Bennett, C. et al. Bringing European river quality into line: an exercise to intercalibrate macro-invertebrate classification methods. Hydrobiologia 667, 31–48 (2011).
doi: 10.1007/s10750-011-0635-2
Desquilbet, M. et al. Comment on ‘Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 370, eabd8947 (2020).
pubmed: 33335036
doi: 10.1126/science.abd8947
Giakoumis, T. & Voulvoulis, N. The transition of EU water policy towards the Water Framework Directive’s Integrated River Basin Management Paradigm. Environ. Manage. 62, 819–831 (2018).
pubmed: 29987347
pmcid: 6208820
doi: 10.1007/s00267-018-1080-z
The European Environment—State and Outlook 2020 (European Environment Agency, 2020); https://www.eea.europa.eu/soer/publications/soer-2020
Gozlan, R. E., Karimov, B. K., Zadereev, E., Kuznetsova, D. & Brucet, S. Status, trends, and future dynamics of freshwater ecosystems in Europe and Central Asia. Inland Waters 9, 78–94 (2019).
doi: 10.1080/20442041.2018.1510271
O’Briain, R. Climate change and European rivers: an eco-hydromorphological perspective. Ecohydrology 12, e2099 (2019).
doi: 10.1002/eco.2099
Wolfram, J., Stehle, S., Bub, S., Petschick, L. L. & Schulz, R. Water quality and ecological risks in European surface waters—monitoring improves while water quality decreases. Environ. Int. 152, 106479 (2021).
pubmed: 33684734
doi: 10.1016/j.envint.2021.106479
Bernhardt, E. S., Rosi, E. J. & Gessner, M. O. Synthetic chemicals as agents of global change. Front. Ecol. Environ. 15, 84–90 (2017).
doi: 10.1002/fee.1450
Pereira, H. M. et al. Essential biodiversity variables. Science 339, 277–278 (2013).
pubmed: 23329036
doi: 10.1126/science.1229931
Deiner, K. et al. Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Mol. Ecol. 26, 5872–5895 (2017).
pubmed: 28921802
doi: 10.1111/mec.14350
Anderson, C. B. Biodiversity monitoring, earth observations and the ecology of scale. Ecol. Lett. 21, 1572–1585 (2018).
pubmed: 30004184
doi: 10.1111/ele.13106
Miller, S. W., Budy, P. & Schmidt, J. C. Quantifying macroinvertebrate responses to in-stream habitat restoration: applications of meta-analysis to river restoration. Restor. Ecol. 18, 8–19 (2010).
doi: 10.1111/j.1526-100X.2009.00605.x
Ferreira, W. R. et al. Importance of environmental factors for the richness and distribution of benthic macroinvertebrates in tropical headwater streams. Freshw. Sci. 33, 860–871 (2014).
doi: 10.1086/676951
Hodgson, J. A., Thomas, C. D., Wintle, B. A. & Moilanen, A. Climate change, connectivity and conservation decision making: back to basics. J. Appl. Ecol. 46, 964–969 (2009).
doi: 10.1111/j.1365-2664.2009.01695.x
Mortelliti, A., Amori, G. & Boitani, L. The role of habitat quality in fragmented landscapes: a conceptual overview and prospectus for future research. Oecologia 163, 535–547 (2010).
pubmed: 20414787
doi: 10.1007/s00442-010-1623-3
Crossley, M. S. et al. No net insect abundance and diversity declines across US Long Term Ecological Research sites. Nat. Ecol. Evol. 4, 1368–1376 (2020).
pubmed: 32778751
doi: 10.1038/s41559-020-1269-4
Johnson, R. K. & Hering, D. Spatial congruency of benthic diatom, invertebrate, macrophyte, and fish assemblages in European streams. Ecol. Appl. 20, 978–992 (2010).
pubmed: 20597284
doi: 10.1890/08-1153.1
Vellend, M. The biodiversity conservation paradox. Am. Sci. 105, 94–101 (2017).
doi: 10.1511/2017.105.2.94
Dornelas, M. et al. A balance of winners and losers in the Anthropocene. Ecol. Lett. 22, 847–854 (2019).
pubmed: 30874368
doi: 10.1111/ele.13242
Heino, J. et al. Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshw. Biol. 60, 845–869 (2015).
doi: 10.1111/fwb.12533
Heino, J. The importance of metacommunity ecology for environmental assessment research in the freshwater realm. Biol. Rev. 88, 166–178 (2013).
pubmed: 22937892
doi: 10.1111/j.1469-185X.2012.00244.x
Ruaro, R., Gubiani, É. A., Hughes, R. M. & Mormul, R. P. Global trends and challenges in multimetric indices of biological condition. Ecol. Indic. 110, 105862 (2020).
doi: 10.1016/j.ecolind.2019.105862
Hawkins, C. P. Quantifying biological integrity by taxonomic completeness: its utility in regional and global assessments. Ecol. Appl. 16, 1277–1294 (2006).
pubmed: 16937797
doi: 10.1890/1051-0761(2006)016[1277:QBIBTC]2.0.CO;2
Vandewalle, M. et al. Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodivers. Conserv. 19, 2921–2947 (2010).
doi: 10.1007/s10531-010-9798-9
Miraldo, A. et al. An Anthropocene map of genetic diversity. Science 353, 1532–1535 (2016).
pubmed: 27708102
doi: 10.1126/science.aaf4381
Violle, C., Reich, P. B., Pacala, S. W., Enquist, B. J. & Kattge, J. The emergence and promise of functional biogeography. Proc. Natl Acad. Sci. USA 111, 13690–13696 (2014).
pubmed: 25225414
pmcid: 4183284
doi: 10.1073/pnas.1415442111
Maureaud, A. et al. Biodiversity–ecosystem functioning relationships in fish communities: biomass is related to evenness and the environment, not to species richness. Proc. R. Soc. B 286, 20191189 (2019).
pubmed: 31288699
pmcid: 6650717
doi: 10.1098/rspb.2019.1189
Jarzyna, M. A. & Jetz, W. Taxonomic and functional diversity change is scale dependent. Nat. Commun. 9, 2565 (2018).
pubmed: 29967400
pmcid: 6028399
doi: 10.1038/s41467-018-04889-z
Pielou, E. C. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13, 131–144 (1966).
doi: 10.1016/0022-5193(66)90013-0
Spellerberg, I. F. & Fedor, P. J. A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon–Wiener’ Index. Glob. Ecol. Biogeogr. 12, 177–179 (2003).
doi: 10.1046/j.1466-822X.2003.00015.x
Haase, P. et al. Moderate warming over the past 25 years has already reorganized stream invertebrate communities.Sci. Total Environ. 658, 1531–1538 (2019).
pubmed: 30678011
doi: 10.1016/j.scitotenv.2018.12.234
Vitecek, S., Johnson, R. K. & Poikane, S. Assessing the ecological status of European rivers and lakes using benthic invertebrate communities: a practical catalogue of metrics and methods. Water 13, 346 (2021).
doi: 10.3390/w13030346
R Core Team. R: A Language and Environment for Statistical Computing (2022); https://www.r-project.org
Huber, P. J. Robust Statistical Procedures 2nd edn (SIAM, 1996).
EuroGeographics. Countries—Administrative Units (2020); https://ec.europa.eu/eurostat/web/gisco/geodata/reference-data/administrative-units-statistical-units/countries