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A refined functional group approach reveals novel insights into effects of urbanization on river macroinvertebrate communities

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Abstract

Context

Urbanization-induced environmental changes are key causes of community disassembly in freshwater systems. Given that species’ traits are closely linked to environmental tolerances, trait-based approaches allow predicting ecological community responses to urbanization. These responses are typically mediated by a suite of traits of organisms (i.e., trait combinations). Trait combinations reflect species’ functional strategies and potential fitness, and different taxa possessing the same trait combinations could respond similarly to stressors. To date, little is known about how urbanization restructures ecological communities from the perspective focusing on trait combinations.

Objectives

We aimed to explore how urbanization restructures ecological community patterns and underlying drivers through affecting different taxa with specific trait combinations.

Methods

We first proposed a functional grouping approach that centers on assigning the whole metacommunity into several homogeneous groups with similar trait combinations. We formed the groupings using hierarchical clustering analysis. We illustrated this approach using a dataset of river macroinvertebrates and multiple-scale environmental variables (i.e., local, land-use and spatial factors). Distance-based redundancy analysis and variation partitioning were used to quantify the roles of ecological drivers in structuring different groups.

Results

A total of six functional groups were identified from the metacommunity of 190 taxa. The relative abundance of two groups increased with the urbanization level (tolerant groups), while the others decreased (sensitive groups). Furthermore, local and land-use variables explained more of community variation for the sensitive groups, while the relative importance of spatial factors was stronger for the tolerant groups.

Conclusion

Our findings suggest that examining how urbanization reshapes ecological communities benefits from assigning the entire metacommunity into different functional groups. The identified functional groups exhibited different responses to urbanization and were shaped by different ecological drivers. We expected that the proposed functional group approach would provide new insights into mechanisms underlying community disassembly caused by urbanization.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Allan JD (2004) Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu Rev Ecol Evol Syst 35(1):257–284

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26(1):32–46

    Google Scholar 

  • Anderson L, Houk P, Miller MGR et al (2021) Trait groups as management entities in a complex, multispecies reef fishery. Conserv Biol 36(3):e13866

    Article  Google Scholar 

  • Anderson GR, Clarke K (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E. Plymouth, UK

  • Arenas-Sanchez A, Doledec S, Vighi M, Rico A (2021) Effects of anthropogenic pollution and hydrological variation on macroinvertebrates in Mediterranean rivers: a case-study in the upper Tagus river basin (Spain). Sci Total Environ 766:144044

    Article  CAS  PubMed  Google Scholar 

  • Aspin TWH, Khamis K, Matthews TJ et al (2019) Extreme drought pushes stream invertebrate communities over functional thresholds. Glob Chang Biol 25(1):230–244

    Article  PubMed  Google Scholar 

  • Barnum TR, Weller DE, Williams M (2017) Urbanization reduces and homogenizes trait diversity in stream macroinvertebrate communities. Ecol Appl 27(8):2428–2442

    Article  PubMed  Google Scholar 

  • Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153(1–2):51–68

    Article  Google Scholar 

  • Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85(7):1826–1832

    Article  Google Scholar 

  • Brinkhurst RO, Fisheriesoceans CDO (2002) Guide to the freshwater aquatic microdrile Oligochaetes of North America. J N Am Benthol Soc 84:1–259

    Google Scholar 

  • Cao J, Zhou W, Wang J et al (2021) Significant increase in extreme heat events along an urban–rural gradient. Landsc Urban Plan 215:104210

    Article  Google Scholar 

  • Castro DMPd, Dolédec S, Callisto M (2018) Land cover disturbance homogenizes aquatic insect functional structure in neotropical savanna streams. Ecol Ind 84:573–582

    Article  Google Scholar 

  • Chung MG, Frank KA, Pokhrel Y, Dietz T, Liu JG (2021) Natural infrastructure in sustaining global urban freshwater ecosystem services. Nat Sustain 4(12):1068–+

  • Cummins KW (1974) Structure and function of stream ecosystems. Bioscience 24(11):631–641

    Article  Google Scholar 

  • Czeglédi I, Kern B, Tóth R, Seress G, Erős T (2020) Impacts of urbanization on stream fish assemblages: the role of the species pool and the local environment. Front Ecol Evol 8:137

    Article  Google Scholar 

  • Dolédec S, Statzner B (2008) Invertebrate traits for the biomonitoring of large European rivers: an assessment of specific types of human impact. Freshw Biol 53(3):617–634

    Article  Google Scholar 

  • Dolédec S, Phillips N, Scarsbrook M, Riley RH, Townsend CR (2006) Comparison of structural and functional approaches to determining landuse effects on grassland stream invertebrate communities. J N Am Benthol Soc 25(1):44–60

    Article  Google Scholar 

  • Dolin PS, Tarter DC (1982) Life history and ecology of Chauliodes rastricornis Rambur and C. pectinicornis (Linnaeus) (Megaloptera: Corydalidae) in Greenbottom Swamp, Cabell County, West Virginia. Brimleyana:111–120

  • Dray S, Bauman D, Blanchet G et al (2021) adespatial: multivariate multiscale spatial analysis. R package version 0.3-14. Retrieved from https://cran.rproject.org/web/packages/adespatial/index.html

  • Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67(3):345–366

    Google Scholar 

  • Edegbene AO, Odume ON, Arimoro FO, Keke UN (2021) Identifying and classifying macroinvertebrate indicator signature traits and ecological preferences along urban pollution gradient in the Niger Delta. Environ Pollut (Barking, Essex: 1987) 281:117076–117076

  • Epler JH (2001) Identification manual for the larval Chironomidae (Diptera) of North and South Carolina. Version 1.0

  • Firmiano KR, Canedo-Arguelles M, Gutierrez-Canovas C et al (2021) Land use and local environment affect macroinvertebrate metacommunity organization in Neotropical stream networks. J Biogeogr 48(3):479–491

    Article  Google Scholar 

  • Fitzgerald DB, Winemiller KO, Perez MHS, Sousa LM (2017) Seasonal changes in the assembly mechanisms structuring tropical fish communities. Ecology 98(1):21–31

    Article  PubMed  Google Scholar 

  • Gál B, Szivák I, Heino J, Schmera D (2019) The effect of urbanization on freshwater macroinvertebrates—knowledge gaps and future research directions. Ecol Ind 104:357–364

    Article  Google Scholar 

  • Gianuca AT, Engelen J, Brans KI et al (2018) Taxonomic, functional and phylogenetic metacommunity ecology of cladoceran zooplankton along urbanization gradients. Ecography 41(1):183–194

    Article  Google Scholar 

  • Green NS, Li S, Maul JD, Overmyer JP (2022) Natural and anthropogenic factors and their interactions drive stream community integrity in a North American river basin at a large spatial scale. Sci Total Environ 835:155344

    Article  CAS  PubMed  Google Scholar 

  • Heino J (2011) A macroecological perspective of diversity patterns in the freshwater realm. Freshw Biol 56(9):1703–1722

    Article  Google Scholar 

  • Heino J (2013) Does dispersal ability affect the relative importance of environmental control and spatial structuring of littoral macroinvertebrate communities? Oecologia 171(4):971–980

    Article  PubMed  Google Scholar 

  • Heino J, Koljonen S (2022) A roadmap for sustaining biodiversity and ecosystem services through joint conservation and restoration of northern drainage basins. Ecol Solut Evid 3(2):e12142

    Article  Google Scholar 

  • Heino J, Schmera D, Erős T (2013) A macroecological perspective of trait patterns in stream communities. Freshw Biol 58(8):1539–1555

    Article  Google Scholar 

  • Heino J, Melo AS, Siqueira T, Soininen J, Valanko S, Bini LM (2015) Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshw Biol 60(5):845–869

    Article  Google Scholar 

  • Heino J, Alahuhta J, Ala-Hulkko T et al (2017) Integrating dispersal proxies in ecological and environmental research in the freshwater realm. Environ Rev 25(3):334–349

    Article  Google Scholar 

  • Hennig C (2018) fpc: flexible procedures for clustering. R package version 2.1-11.1. https://CRAN.R-project.org/package=fpc

  • Herault B (2007) Reconciling niche and neutrality through the Emergent Group approach. Perspect Plant Ecol Evol Syst 9(2):71–78

    Article  Google Scholar 

  • Hsieh TC, Ma KH, Chao A, McInerny G (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7(12):1451–1456

    Article  Google Scholar 

  • Johnson RC, Carreiro MM, Jin H-S, Jack JD (2012) Within-year temporal variation and life-cycle seasonality affect stream macroinvertebrate community structure and biotic metrics. Ecol Ind 13(1):206–214

    Article  Google Scholar 

  • Lai J, Zou Y, Zhang J, Peres-Neto PR (2022) Generalizing hierarchical and variation partitioning in multiple regression and canonical analyses using the rdacca.hp R package. Methods Ecol Evol 13(4):782–788

    Article  Google Scholar 

  • Laliberté E, Legendre P, Shipley B (2014) FD: Measuring functional diversity (FD) from multiple traits, and other tools for functional ecology. http://cran.uvigo.es/web/packages/FD/.

  • Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91(1):299–305

    Article  PubMed  Google Scholar 

  • Legendre P, Legendre L (2012) Numerical ecology, 3rd English. Elsevier, Amsterdam

    Google Scholar 

  • Li Z, Heino J, Chen X et al (2021) Understanding macroinvertebrate metacommunity organization using a nested study design across a mountainous river network. Ecol Indic 121:107188

    Article  Google Scholar 

  • Liaw A, Wiener M (2015) Package ‘randomForest’: Breiman and Cutler’s random forests for classification and regression, R package version 4.6-1.1. https://cran.rproject.org/web/packages/randomForest/randomForest.pdf

  • Liu L, Yang J, Yu Z, Wilkinson DM (2015) The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J 9(9):2068–2077

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Zhou T, Cui Y et al (2021) Environmental filtering and spatial processes equally contributed to macroinvertebrate metacommunity dynamics in the highly urbanized river networks in Shenzhen, South China. Ecol Proces 10(1):Article Number 13

    Article  Google Scholar 

  • Liu Z, Heino J, Soininen J et al (2022) Different responses of incidence-weighted and abundance-weighted multiple facets of macroinvertebrate beta diversity to urbanization in a subtropical river system. Ecol Indic 143:109357

    Article  Google Scholar 

  • Liu Z, Zhou T, Heino J et al (2022) Land conversion induced by urbanization leads to taxonomic and functional homogenization of a river macroinvertebrate metacommunity. Sci Total Environ 825(15):153940

    Article  CAS  PubMed  Google Scholar 

  • Luck GW, Smallbone LT (2011) The impact of urbanization on taxonomic and functional similarity among bird communities. J Biogeogr 38(5):894–906

    Article  Google Scholar 

  • Lundquist MJ, Zhu W (2018) Aquatic insect functional diversity and nutrient content in urban streams in a medium-sized city. Ecosphere 9(5):e02284

    Article  Google Scholar 

  • Luo K, Hu X, He Q et al (2018) Impacts of rapid urbanization on the water quality and macroinvertebrate communities of streams: a case study in Liangjiang New Area, China. Sci Total Environ 621:1601–1614

    Article  CAS  PubMed  Google Scholar 

  • McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14(11):450–453

    Article  CAS  PubMed  Google Scholar 

  • McMahon G, Cuffney TF (2000) Quantifying urban intensity in drainage basins for assessing stream ecological conditions. J Am Water Resour Assoc 36(6):1247–1261

    Article  Google Scholar 

  • Mondy CP, Munoz I, Doledec S (2016) Life-history strategies constrain invertebrate community tolerance to multiple stressors: a case study in the Ebro basin. Sci Total Environ 572:196–206

    Article  CAS  PubMed  Google Scholar 

  • Mor JR, Doledec S, Acuna V, Sabater S, Munoz I (2019) Invertebrate community responses to urban wastewater effluent pollution under different hydro-morphological conditions. Environ Pollut 252(Pt A):483–492

    Article  CAS  PubMed  Google Scholar 

  • Morse JC, Yang L, Tian L (1994) Aquatic insects of China useful for monitoring water quality. Hohai University Press, Nanjing, China

    Google Scholar 

  • Mouillot D, Graham NA, Villeger S, Mason NW, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28(3):167–177

    Article  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M et al (2017) vegan: Community Ecology Package. http://vegan.r-forge.r-project.org/. Available from https://cran.r-project.org/web/packages/vegan/index.html

  • Pandit SN, Kolasa J, Cottenie K (2009) Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. Ecology 90(8):2253–2262

    Article  PubMed  Google Scholar 

  • Paul MJ, Meyer JL (2008) Streams in the urban landscape

  • Paz LE, Rodriguez M, Gullo B, Rodrigues Capitulo A (2021) Impacts of urban and industrial pollution on functional traits of benthic macroinvertebrates: are some traits advantageous for survival? Sci Total Environ 807(Pt 2):150650

    PubMed  Google Scholar 

  • Peng FJ, Pan CG, Zhang NS et al (2020) Benthic invertebrate and microbial biodiversity in sub-tropical urban rivers: Correlations with environmental variables and emerging chemicals. Sci Total Environ 709:136281

    Article  CAS  PubMed  Google Scholar 

  • Piliere AFH, Verberk W, Grawe M et al (2016) On the importance of trait interrelationships for understanding environmental responses of stream macroinvertebrates. Freshw Biol 61(2):181–194

    Article  Google Scholar 

  • Poff NL (1997) Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. J N Am Benthol Soc 16(2):391–409

    Article  Google Scholar 

  • Poff NL, Olden JD, Vieira NKM, Finn DS, Simmons MP, Kondratieff BC (2006) Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J N Am Benthol Soc 25(4):730–755

    Article  Google Scholar 

  • Qian Y, Zhou W, Pickett STA et al (2020) Integrating structure and function: mapping the hierarchical spatial heterogeneity of urban landscapes. Ecological Processes 9(1):1:(59)

  • Reid AJ, Carlson AK, Creed IF et al (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol Rev 94(3):849–873

    Article  PubMed  Google Scholar 

  • Roberts D (2016) labdsv: Ordination and Multivariate Analysis for Ecology. R Package Version 1.8-0. https://CRAN.R-project.org/package=labdsv

  • Rosenberg DM, Resh VH (1993) Freshwater biomonitoring and benthic macroinvertebrates

  • Sarremejane R, Truchy A, McKie BG et al (2021) Stochastic processes and ecological connectivity drive stream invertebrate community responses to short-term drought. J Anim Ecol 90(4):886–898

    Article  PubMed  Google Scholar 

  • Schmera D, Heino J, Podani J (2022) Characterising functional strategies and trait space of freshwater macroinvertebrates. Sci Rep 12(1):Article Number 12283

    Article  Google Scholar 

  • Southwood TRE (1977) Habitat, the templet for ecological strategies? J Anim Ecol 46(2):337–365

    Article  Google Scholar 

  • Statzner B, Beche LA (2010) Can biological invertebrate traits resolve effects of multiple stressors on running water ecosystems? Freshw Biol 55:80–119

    Article  Google Scholar 

  • Statzner B, Hoppenhaus K, Arens MF, Richoux P (1997) Reproductive traits, habitat use and templet theory: a synthesis of world-wide data on aquatic insects. Freshw Biol 38(1):109–135

    Article  Google Scholar 

  • Statzner B, Bis B, Dolédec S, Usseglio-Polatera P (2001) Perspectives for biomonitoring at large spatial scales: a unified measure for the functional composition of invertebrate communities in European running waters. Basic Appl Ecol 2(1):73–85

    Article  Google Scholar 

  • Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2010) Invertébrés d’eau Douce: Systématique, Biologie, Écologie, 3rd edn. CNRS Éditions, Paris

    Google Scholar 

  • Thornhill IA, Biggs J, Hill MJ et al (2018) The functional response and resilience in small waterbodies along land-use and environmental gradients. Glob Chang Biol 24(7):3079–3092

    Article  PubMed  Google Scholar 

  • Tolonen KE, Tokola L, Grönroos M et al (2016) Hierarchical decomposition of trait patterns of macroinvertebrate communities in subarctic streams. Freshw Sci 35(3):1032–1048

    Article  Google Scholar 

  • Tonkin JD, Stoll S, Jähnig SC, Haase P (2016) Elements of metacommunity structure of river and riparian assemblages: communities, taxonomic groups and deconstructed trait groups. Ecol Complex 25:35–43

    Article  Google Scholar 

  • Tonkin JD, Altermatt F, Finn DS et al (2018) The role of dispersal in river network metacommunities: patterns, processes, and pathways. Freshw Biol 63(1):141–163

    Article  Google Scholar 

  • Townsend CR, Hildrew AG (1994) Species traits in relation to a habitat templet for river systems. Freshw Biol 31(3):265–275

    Article  Google Scholar 

  • Urban MC, Skelly DK, Burchsted D, Price W, Lowry S (2006) Stream communities across a rural-urban landscape gradient. Divers Distrib 12(4):337–350

    Article  Google Scholar 

  • Usseglio-Polatera P, Bournaud M, Richoux P, Tachet H (2000) Biological and ecological traits of benthic freshwater macroinvertebrates: relationships and definition of groups with similar traits. Freshw Biol 43(2):175–205

    Article  Google Scholar 

  • Verberk WCEP, Siepel H, Esselink H (2008a) Applying life-history strategies for freshwater macroinvertebrates to lentic waters. Freshw Biol 53(9):1739–1753

    Article  Google Scholar 

  • Verberk WCEP, Siepel H, Esselink H (2008b) Life-history strategies in freshwater macroinvertebrates. Freshw Biol 53(9):1722–1738

    Article  Google Scholar 

  • Verberk WCEP, van Noordwijk CGE, Hildrew AG (2013) Delivering on a promise: integrating species traits to transform descriptive community ecology into a predictive science. Freshw Sci 32(2):531–547

    Article  Google Scholar 

  • Vieira NKM, Poff NL, Carlisle DM, Moulton II SR, Koski ML, Kondratieff BC (2006) A database of lotic invertebrate traits for North America

  • Wang H (2002) Studies on taxonomy, distribution and ecology of microdrile oligochaetes of china, with description of two new species from the vicinity of the great wall station of China. Higher Education Press, Beijing

    Google Scholar 

  • Wang Q, Ross-Nickoll M, Wu D et al (2018) Impervious area percentage predicated influence of rapid urbanization on macroinvertebrate communities in a southwest China river system. Sci Total Environ 627:104–117

    Article  CAS  PubMed  Google Scholar 

  • Wiggins GB (1996) Larvae of the North American caddisfly genera (Trichoptera), 2nd edn. University of Toronto Press, Toronto, pp 1–457

    Book  Google Scholar 

  • Zhou C, Gui H, Zhou K (2003) Larval key to families of Ephemeroptera from China (Insecta). Nanjing Shida Xuebao Ziran Kexue Ban 26(2):65–68

    Google Scholar 

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Acknowledgements

We acknowledge Mr. Shun Huang for drawing figures in original-drift writing. We acknowledge Mr. Lei Liang and Mrs. Fanghua Wang for their help in field sampling. We thank Mr. Xin Wang (Analytical & Testing Center, Institute of Hydrobiology, Chinese Academy of Sciences) for assistance in data analysis.

Funding

This work was supported by the program “Shenzhen City under the grant of Aquatic Ecological Monitoring and Assessment for Major rivers” (No. 2019-07-233) and “Special Foundation for National Science and Technology Basic Research Program of China” (grant No. 2019FY101903). Jani Heino was supported by Grant No. 331957 from the Academy of Finland.

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ZL and ZX conceived the ideas and designed the methodology; ZL, TZ, YJ and YM collected the data; ZL and YG led manuscript conceptualization; ZL led data analysis and the writing of the manuscript; YG and WW assisted with analysis and interpretation of the data; JH, YC, YC, JZ and ZX revised the manuscript; all authors contributed critically to the drafts and gave final approval for publication.

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Correspondence to Junqian Zhang or Zhicai Xie.

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Liu, Z., Heino, J., Ge, Y. et al. A refined functional group approach reveals novel insights into effects of urbanization on river macroinvertebrate communities. Landsc Ecol 38, 3791–3808 (2023). https://doi.org/10.1007/s10980-023-01612-2

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