Elsevier

Ecological Indicators

Volume 10, Issue 5, September 2010, Pages 1025-1036
Ecological Indicators

From compositional to functional biodiversity metrics in bioassessment: A case study using stream macroinvertebrate communities

https://doi.org/10.1016/j.ecolind.2010.02.011Get rights and content

Abstract

While compositional diversity is a common metric for assessing human impacts on aquatic communities, functional diversity is scarcely employed, though highly desirable from the perspective of the European Water Framework Directive. Using abundance data from 99 minimally disturbed sites (i.e., no or very weak anthropogenic impact) from a national survey, we studied the spatial variability of compositional and functional biodiversity metrics across a predefined ecoregional classification. Metrics of compositional diversity comprised taxonomic and EPT richness and Simpson diversity. Functional diversity metrics were based on Rao's Quadratic Entropy (RQE), which described the differences among benthic invertebrate genera in eleven biological traits (e.g., size, life cycle, reproduction types, feeding habits). Using generalized linear models we show that taxonomic richness may vary greatly across ecoregions, contrasting with Simpson diversity and functional metrics that varied weakly in response to natural environmental variability. Functional diversity metrics, because of their stability in response to natural environmental variability, may be useful tools for assessing human impairment to ecosystem function. We further tested the response of functional diversity metrics to a specific human impact (sewage) and demonstrated significant modifications of functional diversity downstream of sewage pollution. Further investigations are required to test the ability of functional diversity metrics to precisely and accurately indicate different types of human impacts.

Introduction

According to the European Water Framework Directive (WFD), freshwater biomonitoring should be based on bioindicators that measure the deviation between an observed and an expected value of ecological quality and should enable the assessment of potential impairment to ecosystem functioning (e.g., Ghilarov, 2000). Among the various possible bioindicators (fishes, macrophytes, diatoms), benthic invertebrates have proven their efficiency and reliability for detecting human impact (Rosenberg and Resh, 1993; recently reviewed in Bonada et al., 2006). As a result, each European country currently uses benthic invertebrates in their national surveys to derive biological indices (Iversen et al., 2000) or various metrics (e.g., Böhmer et al., 2004, Furse et al., 2006) to assess stream impairment.

Among these metrics, taxonomic richness is commonly included (e.g., Hering et al., 2006) either as the total number of taxa or the number of taxa from pollution-sensitive groups such as EPT richness (Compin and Cereghino, 2003, Lenat and Penrose, 1996). Diversity indices (e.g., Simpson or Shannon index), which incorporate species abundances (or frequencies) also are common metrics used in bioassessment. Taxonomic richness is the simplest measure of biodiversity, and is generally thought to reflect ecosystem function (Statzner and Lévêque, 2007), although this idea is still debated. Compositional richness and diversity measures consider species on an equal basis. However, in terms of ecosystem function, the introduction of some invasive species may partially compensate the extinction of native species, a process that may not be detected by compositional richness or diversity metrics alone (Devin et al., 2005).

Recent proposals for measuring biodiversity aim at incorporating the biological differences among species into biological indices (e.g., Shimatani, 2001) for a more direct measurement of functional diversity (e.g., Petchey and Gaston, 2002, Petchey et al., 2004). For example, Rao's Quadratic Entropy (RQE; Rao, 1982), which measures the diversity at sites by weighting the co-occurrence of species by their biological distances, has been proposed to estimate functional diversity (Bady et al., 2005, Champely and Chessel, 2002, Izsák and Papp, 1995). Biological distances among species may be derived from taxonomy (e.g., Clarke and Warwick, 1998) or from their biological traits, i.e., attributes that are shared by all living organisms (e.g., life history, diet; see Bady et al., 2005, Usseglio-Polatera et al., 2000a). It has been shown that patterns in the biological traits of lotic invertebrates are significantly related to patterns of natural disturbance (e.g., Paillex et al., 2009, Statzner et al., 1994, Statzner et al., 1997, Townsend et al., 1997). In addition, a bulk of studies in aquatic environments have demonstrated that biological traits respond significantly to human disturbance such as landuse management (e.g., Dolédec et al., 2006, Richards et al., 1997), sewage effluent (Charvet et al., 1998, Statzner et al., 2001), cargo ship traffic (Dolédec and Statzner, 2008), or global environmental change (Dolédec et al., 1999, Gayraud et al., 2003). Trait-based diversity metrics may thus represent appropriate additional metrics for assessing changes in the functional biodiversity of ecosystems (e.g., Lepš et al., 2006).

Biomonitoring tools using invertebrate community characteristics to assess the ecological integrity of freshwater resources currently rely on the ‘reference condition approach’, i.e., comparisons of test sites with a set of minimally disturbed reference sites (e.g., Reynoldson et al., 1997, Wright et al., 2000). Ideally, to ensure the reliability of biological responses to anthropogenic disturbance, natural fluctuations of communities linked to local physical habitat, longitudinal gradient of rivers and climate conditions must be partialled out. One way to reduce the influence of natural fluctuations of communities on biological metrics relies on ecoregional partitioning, which aim at delineating homogeneous regions with specific stream types (e.g., Omernik, 1987, Omernik and Bailey, 1997). For example, in France 22 such ecoregions [called Hydroecoregions (HERs)] were defined based on geology, climate, relief, and vegetation types (Wasson et al., 2002a). By contrast, biological trait responses of invertebrate assemblages to similar reference environmental conditions were shown to converge at large spatial scales (Archaimbault et al., 2005, Charvet et al., 2000, Statzner et al., 2004).

In this paper, we use data from a national survey to examine the natural variability of 12 functional diversity metrics (using RQEs based on overall trait differences and 11 biological traits) in comparison to traditional metrics (taxonomic and EPT richness, and Simpson diversity) in the Rhône River basin. We consider (1) the natural variability of each metric at the regional scale (i.e., the entire river basin), (2) the consequences of such variability in the definition of appropriate indicators and (3) the potential of functional diversity metrics as additional metrics for indicating human disturbance.

Section snippets

Study area

The study area covers the Rhône River drainage basin (∼90,630 km2; Fig. 1) situated in the southeastern France. The catchment comprises contrasted landscapes with two large rivers (the Rhône river and its affluent the Saône river) that drain the middle axis of the catchment, various mountain types (Alps > 1500 m and Massif Central < 1500 m), as well as a latitudinal climate gradient (continental temperate to Mediterranean). Geology ranges from calcareous to more acidic substrate (granite) and includes

Correlations among metrics

Most correlations among diversity metrics were significant with 81 out of 105 with P < 0.05 (Table 3). Taxonomic and EPT richness showed the strongest correlation (0.75). Simpson D and EPT richness were significantly correlated (0.44) whereas Simpson D and total genus richness were weakly correlated (0.22). In most cases, taxonomic richness was not correlated to functional biodiversity metrics (RQEs; P > 0.05). Simpson D had the highest correlations with functional biodiversity metrics whereas EPT

Discussion

In this study, we examined the relationship between compositional and functional biodiversity metrics and ecoregion in minimally disturbed conditions with the goal of identifying candidate functional biodiversity metrics for the indication of ecosystem function. To design additional indicators linked to ecosystem functioning, we focused on two requirements for bioassessment metrics: (1) the stability of response of metrics in the absence of human disturbance (minimally disturbed sites) at a

Conclusions

Taxonomic richness and diversity indices are commonly used bioassessment metrics (Ives and Carpenter, 2007). These metrics based on the presence and relative abundance of species do not consider their ecological role (e.g., keystone species) and biological characteristics. Functional diversity metrics, using biological differences based on multiple biological traits, provide an indirect measurement of ecosystem functioning (e.g., Charvet et al., 1998, Dolédec et al., 2006, Dolédec and Statzner,

Acknowledgements

This study was funded by the French Water Agency Rhône-Méditerranée-Corse. We thank Nicolas Mengin (Cemagref, Lyon) who provided the biological and environmental data from the national database and Stéphane Stroffek from the French Water Agency Rhône-Méditerranée-Corse for thoughtful comments. We also thank Leah A. Bêche for editing the English and two anonymous referees for their constructive comments on a previous draft of the manuscript.

References (90)

  • J. Böhmer et al.

    Multimetric assessment of data provided by water managers from Germany: assessment of several different types of stressors with macrozoobenthos communities

    Hydrobiologia

    (2004)
  • N. Bonada et al.

    Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches

    Annu. Rev. Entomol.

    (2006)
  • Z. Botta-Dukát

    Rao's quadratic entropy as a measure of functional diversity based on multiple traits

    J. Veg. Sci.

    (2005)
  • J.H. Brown

    On the relationship between abundance and distribution of species

    Am. Nat.

    (1984)
  • D.M. Carlisle et al.

    Leaf litter breakdown, microbial respiration and shredder production in metal-polluted streams

    Freshw. Biol.

    (2005)
  • S. Champely et al.

    Measuring biological diversity using Euclidean metrics

    Environ. Ecol. Stat.

    (2002)
  • S. Charvet et al.

    Biomonitoring through biological traits of benthic macroinvertebrates: perspectives for a general tool in stream management

    Arch. Hydrobiol.

    (1998)
  • S. Charvet et al.

    Traits of benthic macroinvertebrates in semi-natural French streams: an initial application to biomonitoring in Europe

    Freshw. Biol.

    (2000)
  • D. Chessel et al.

    The ade4 Package—{I}: one-table methods

    R News

    (2004)
  • F. Chevenet et al.

    A fuzzy coding approach for the analysis of long-term ecological data

    Freshw. Biol.

    (1994)
  • K.R. Clarke et al.

    A taxonomic distinctness index and its statistical properties

    J. Appl. Ecol.

    (1998)
  • V. de Crespin de Billy et al.

    Biplot presentation of diet composition data: an alternative for fish stomach contents analysis

    J. Fish Biol.

    (2000)
  • S. Devin et al.

    Changes in fonctional biodiversity in an invaded freshwater ecosystem: the Moselle River

    Hydrobiologia

    (2005)
  • S. Dolédec et al.

    Comparison of structural and functional approaches to determining landuse effects on grassland stream invertebrate communities

    J. North Am. Benthol. Soc.

    (2006)
  • S. Dolédec et al.

    Invertebrate traits for the biomonitoring of large European rivers: an assessment of specific types of human impact

    Freshw. Biol.

    (2008)
  • S. Dolédec et al.

    Species traits for future biomonitoring across ecoregions: patterns along a human-impacted river

    Freshw. Biol.

    (1999)
  • S. Dray et al.

    Spatial ordination of vegetation data using a generalization of Wartenberg's multivariate spatial correlation

    J. Veg. Sci.

    (2008)
  • A. Feest

    Establishing baseline indices for the quality of the biodiversity of restored habitats using a standardized sampling process

    Restor. Ecol.

    (2006)
  • L. Füreder et al.

    Reference conditions of alpine streams: physical habitat and ecology

    Water Air Soil Pollut.

    (2002)
  • M.T. Furse et al.

    The ecological status of European rivers: evaluation and intercalibration of assessment methods

    Hydrobiologia

    (2006)
  • S. Gayraud et al.

    Invertebrate traits for the biomonitoring of large European Rivers: an initial assessment of alternative metrics

    Freshw. Biol.

    (2003)
  • A. Ghilarov

    Ecosystem functioning and intrinsic value of biodiversity

    Oikos

    (2000)
  • J.P. Grime

    Benefits of plant diversity to ecosystems: immediate, filter and founder effects

    J. Ecol.

    (1998)
  • O.J. Hardy et al.

    Interpreting and estimating measures of community phylogenetic structuring

    J. Ecol.

    (2008)
  • C.P. Hawkins et al.

    Evaluation of the use of landscape classifications for the prediction of freshwater biota: synthesis and recommendations

    J. North Am. Benthol. Soc.

    (2000)
  • C.P. Hawkins et al.

    Weak correspondence between landscape classifications and stream invertebrate assemblages: implications for bioassessment

    J. North Am. Benthol. Soc.

    (2000)
  • J. Heino et al.

    Correspondence between regional delineations and spatial patterns in macroinvertebrate assemblages of boreal headwater streams

    J. North Am. Benthol. Soc.

    (2002)
  • J. Heino et al.

    Weak relationships between landscape characteristics and multiple facets of stream macroinvertebrate biodiversity in a boreal basin

    Landsc. Ecol.

    (2008)
  • D. Hering et al.

    Cook book for the development of a Multimetric Index for biological condition of aquatic ecosystems: experiences from the European AQEM and STAR projects and related initiatives

    Hydrobiologia

    (2006)
  • D. Hering et al.

    Overview and application of the AQEM assessment system

    Hydrobiologia

    (2004)
  • M.O. Hill

    Diversity and evenness: a unifying notation and its consequences

    Ecology

    (1973)
  • D.U.F.S.C. Hooper et al.

    Effects of biodiversity on ecosystem functioning: a consensus of current knowledge

    Ecol. Monogr.

    (2005)
  • T.M. Iversen et al.

    River conservation in the European Community, including Scandinavia

  • A.R. Ives et al.

    Stability and diversity of ecosystems

    Science

    (2007)
  • J. Izsák et al.

    Application of the quadratic entropy indices for diversity studies of drosophilid assemblages

    Environ. Ecol. Stat.

    (1995)
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