Elsevier

Ecological Indicators

Volume 66, July 2016, Pages 65-75
Ecological Indicators

Functional diversity of macrobenthic assemblages decreases in response to sewage discharges

https://doi.org/10.1016/j.ecolind.2016.01.003Get rights and content

Abstract

We analyzed the effects of sewage discharge on a subtropical estuary by comparing the functional diversity of intertidal macroinvertebrate assemblages in contaminated with non-contaminated reference areas. Functional structure was assessed using biological traits analysis (BTA) and four multivariate indices (FRic, FEve, FDis and Rao's Q) of functional diversity. Our results showed clear and temporally consistent changes in macrobenthic functional structure in contaminated areas. However, these results depended on whether abundance- or biomass-based measurements were used, with abundance-based analyses distinguishing most clearly between sewage contamination conditions. Differences between contaminated and non-contaminated conditions were also displayed by BTA for all the functional trait categories. FDis (functional divergence) and Rao's Q (functional dispersion) were higher in the non-contaminated condition and increased with higher benthic environmental health, as measured by the AMBI index. These patterns of higher functional divergence and dispersion were driven by the numerical dominance of opportunistic annelids in the contaminated condition. We suggest that abundance-based BTA, and the FDis and/or Rao's Q indices are reliable approaches to detect changes in functional structure with respect to sewage pollution. They have a great potential for environmental assessment and monitoring of subtropical estuarine ecosystems.

Introduction

Functional diversity is the component of biodiversity that describes the variety of functions developed by organisms in an assemblage, community or ecosystem (Tilman, 2001). It can be quantified by estimating the extent, dispersion and relative abundance of species functional traits (Mason et al., 2005) and provides an informative complement to studies addressing the interrelationship between community structure, environmental heterogeneity and ecosystem functioning (Gagic et al., 2015). Functional traits are defined as any organismal characteristics related to individual performance that can directly or indirectly affect one or more ecosystem properties and processes (Mlambo, 2014, Violle et al., 2007). Studies focusing on functional diversity usually assess how organisms affect ecosystem properties/processes (Gagic et al., 2015) and which environmental factors and disturbances shape assemblage functional trait diversity and distribution along space and time (Gerisch et al., 2012, Bremner et al., 2006a).

In the past two decades, many methods and techniques have been proposed to assess the functional diversity of assemblages. The most widely used are analysis of functional or trophic groups (Gusmao-Junior and Lana, 2015), biological traits analysis (BTA; Bremner, 2008) and calculation of functional diversity indices (Laliberté and Legendre, 2010, Villéger et al., 2008). BTA is based on multivariate ordinations to describe variation patterns of functional traits along spatial or temporal gradients (Chevenet et al., 1994, Dolédec and Chessel, 1994). It has been used in marine benthic systems to assess human impacts like dredging (Wan Hussin et al., 2012) and nutrient input (Paganelli et al., 2012), or spatial and temporal variability of benthic ecosystem functioning (Bremner et al., 2006a, Bremner et al., 2006b, Darr et al., 2014, Pacheco et al., 2011). On the other hand, functional diversity indices have varying abilities to reflect the different aspects of assemblage functional trait structure. Functional Richness (FRic), Functional Evenness (FEve), Functional Divergence (FDiv), and Rao's Quadratic Entropy (Rao's Q) are multi-trait measurements that encompass the multivariate aspects of the trait functional structure (Botta-Dukát, 2005, Laliberté and Legendre, 2010, Villéger et al., 2008). FRic, FEve and FDiv are interpreted as analogous to taxonomic diversity metrics. Raos’Q estimates functional dispersion by measuring how species differ regarding functional traits, also weighting their abundances. Except FEve that describes abundance distribution, higher values of these functional diversity indices are expected when species in an assemblage differ greatly in their functional traits. These indices have been used to assess the functional diversity of birds (Luck et al., 2013), fishes (Villéger et al., 2010), zooplankton (Massicotte et al., 2014), arthropods (Gerisch et al., 2012), as well as the ecology (Darr et al., 2014), paleontology (Villéger et al., 2011) and biogeography (Berke et al., 2014) of marine benthos.

Despite their high potential applicability in assessing human-driven impacts (Mouillot et al., 2013), functional diversity approaches are scant in marine benthic ecosystems. Metrics such as species diversity (Shannon-Index H′), species richness, environmental quality indices for coastal ecosystems (e.g. AMBI and M-AMBI; Borja et al., 2004, Muxika et al., 2007) and distance-based measures such as Bray–Curtis are the most widely used approaches to assess the effects of anthropogenic disturbance on benthic structure. These metrics, however, do not consider changes in functional trait structure, which are central to understand the effects of human disturbances on ecosystem functioning (Darr et al., 2014). Thus, it is necessary to assess how functional parameters relate to different environmental drivers and disturbances in the marine benthos to test the usefulness of these analytical tools as indicators of ecological status.

One of these disturbances in coastal marine systems is sewage input that is a stress source that may eliminate sensitive in favor of tolerant or opportunistic species (Borja et al., 2000). Since tolerance levels and the ability to explore environmental resources are both related to species functional traits, a contamination gradient may affect the functional structure of macroinvertebrate assemblages. Based on these assumptions we predict: (1) the functional traits composition of macrofaunal assemblages will change depending on the sewage contamination condition; (2) lower functional diversity values are expected in contaminated areas; and (3) functional diversity indices will be negatively related to indicators of bad environmental quality. To test these hypotheses, we analyzed the effects of distinct levels of sewage discharges on the functional diversity of macroinvertebrate assemblages inhabiting tidal flats of a subtropical estuary. Biological trait analysis and the calculation of four functional diversity indices were used to test our predictions.

Section snippets

Study area

This study was carried out in the Cotinga sub-estuary (25°31′47″S, 48°28′03″W) of Paranaguá Bay, Brazil. Paranaguá Bay, covering 612 km2, is one of the largest and best preserved estuarine systems of southern Brazil. The climate is strongly influenced by the semi-permanent South Atlantic anti-cyclone and by the passage of polar fronts during the winter (Lana et al., 2001). The water balance of the region differs significantly between the rainy season (late spring and summer) and the dry season

Environmental variables

The PCA ordination of the 10 environmental variables revealed gradients within the first two axes (Fig. 2). The fist axis explained 41% of the total variability and was associated to changes in sediment grain size, mud content, sorting coefficient, and C, P and N contents. The second axis explained 21% of the total variability and was associated to changes in salinity, coprostanol, P, and organic matter content. The second axis distinguished tidal flats in the contaminated condition from those

Discussion

We have shown that macrobenthic functional structure can be successfully used as a complement to describe sewage contaminated areas. However, its usefulness depends on the selected metrics to quantify the macrobenthos. Gradients in functional trait composition across contamination conditions were evident for the abundance-based BTAs but not for the biomass-based analysis. Variation in functional diversity between contamination conditions were also variable depending on the index used but the

Conclusion

This work is the first spatially and temporally replicated study that describe variation patterns of functional diversity of estuarine macrobenthic assemblages in response to sewage contamination. Temporally consistent variations in macrobenthic functional structure across different sewage contamination conditions indicate evidence of sewage pollution in a subtropical estuarine habitat. Variation patterns derived from abundance-based metrics were more evident than those based on biomass-based

Acknowledgments

This study was funded by the Federal University of Paraná (UFPR), the Post-Graduation Program in Coastal and Oceanic Systems (PGSISCO-UFPR), and the Brazilian research funding agency CAPES (Coordination for the Improvement of Higher Education Personnel). We thank Esther Chang and the anonymous referees for the valuable comments on an earlier version of this work.

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