Ability of benthic indicators to assess ecological quality in estuaries following management
Introduction
On a worldwide-scale, the increasing impact of human activities on marine and estuarine environments triggered attention toward the need for monitoring, assessing and managing ecological integrity (Karr, 1999) to promote the long-term sustainability of these systems (Borja et al., 2008).
The recovery process of macrobenthic communities in response to human-mediated actions to restore systems ecological quality is less well studied than their response to different types of natural and anthropogenic disturbances (Sanz-Lázaro and Marin, 2006, Wildsmith et al., 2009). Nevertheless, the detrimental effect of human activities on estuarine, coastal and marine ecosystems highlights an urgent need to remedy these impacts through the implementation of restoration measures (Elliott et al., 2007). Restoration is aimed at reversing the adverse ecological impacts of human disturbance (de Jonge et al., 2000). Degradation causes changes in both ecosystem structure and functioning, and if the recovery is successful the community should achieve a similar species composition, density, and biomass structure similar to the pre-disturbance condition (Elliott et al., 2007). To determine the effectiveness of restoration measures it is necessary, namely, (1) to identify and understand the processes that promoted the observed ecological changes, (2) to determine realistic objectives and methods to implement and incorporate them into management, and (3) to monitor the restoration in order to assess its success (Kennish, 2000).
Among the most relevant biological components selected by the European Water Framework Directive (WFD, 2000/60/EC) to assess aquatic ecosystems’ ecological status are the benthic macroinvertebrates. Their location at the sediment/water interface and their life history traits and characteristics make them highly suitable to assess environmental conditions. Indeed, most benthic taxa are relatively sedentary, long-lived and thus, unable to avoid adverse environmental conditions integrating and reflecting the history of local effects of stress over time. Moreover, macrobenthic assemblages’ taxonomy and quantitative sampling is relatively easy and they comprise species that show different tolerances to stress being, therefore, sensitive indicators of change (Dauer et al., 1993b, Warwick, 1993, Dauvin et al., 2010).
Ecological indicators are meant to provide succinct information about the state of ecosystems addressing their structure and/or functioning based on information from its components. Although presenting some drawbacks (reduction of ecosystem complexity to a single value; misleading in data interpretations when misapplied, such that their application does not follow the right criteria and does not occur in situations consistent with their intended use and scope), their usefulness particularly to communicate scientific concepts in a simple way to the general public and managers is widely recognize (Salas et al., 2006a, Borja et al., 2008, Dauvin et al., 2010).
The inherent features of macrobenthic assemblages have established them as powerful bio-indicators (Dauvin, 2007). As such, their response to several types of natural and anthropogenic disturbances has been considerably addressed in many surveys (e.g., Pearson and Rosenberg, 1978, Gray, 1979, Dauer, 1993a, Reiss and Kröncke, 2005). Disturbance effects on benthic assemblages usually comprise changes in diversity, biomass, abundance of stress tolerant and sensitive species, and at the trophic and functional level (Pearson and Rosenberg, 1978, Warwick, 1986, Warwick and Clarke, 1994, Reiss and Kröncke, 2005, Kröncke and Reiss, 2010, Elliott and Quintino, 2007). Having this knowledge, theoretically, it becomes possible to predict in advance the behavior, and consequently, the ability of an ecological indicator to measure and detect changes in ecological conditions.
As stated by Diaz et al. (2004), a parsimonious approach should rely upon the evaluation of the existing metrics prior to developing new ones. As such, comparison between different methodologies, application, and evaluation of existing indicators in various countries for different systems, helps to improve the knowledge about the suitability of such approaches. Indeed, many aspects of applying indicators and interpreting results are in continuous re-validation. Clearly, indicators that may be robust in space and time will be preferable to communicate information to environmental managers (Borja and Dauer, 2008). In this way, studies that address comparisons of performance (e.g., at several geographic areas; for different disturbance sources) among benthic indicators are imperative. As stated by Borja et al. (2009), the last decade was characterized by an explosion of indicators and the coming years should be those of consolidation and agreement. One of the challenges for the next decade is to accomplish sufficient indicator performance comparisons to reach scientific consensus on the preferred indicators approaches for macroinvertebrates (Borja et al., 2009).
The Mondego estuary (Fig. 1), a small mesotidal system located on the western coast of Portugal (40°08′N, 8°50′W), underwent several physical transformations and intense anthropogenic pressure which have strongly modified its natural environment inducing a progressive deterioration in ecological quality (Cabral et al., 1999, Lopes et al., 2000, Martins et al., 2005, Marques et al., 1997, Marques et al., 2003). In order to lessen the eutrophication symptoms recorded in the south arm of this estuary in the early 1990s and aiming to improve its ecological condition, minor experimental mitigation measures were applied in 1997/98 (Teixeira et al., 2008a, Teixeira et al., 2008b, Patrício et al., 2009, Cardoso et al., 2010, Neto et al., 2010). Following the system's observed partial recovery (Dolbeth et al., 2007, Teixeira et al., 2008a, Teixeira et al., 2008b, Patrício et al., 2009), and after much research and discussion (e.g., Marques et al., 2003, Marques et al., 2007), it was then decided to implement a more severe intervention plan in the spring of 2006 in an attempt to ameliorate this problem (Marques et al., 2007). The re-establishment of the communication between both arms of the Mondego estuary (in the spring of 2006) was chosen as an adaptive management case study.
The main goal of this study was to assess the effectiveness of this recovery action: a morphological change that altered local hydrodynamics, increasing water circulation and lowering the residence time in an estuarine section. In particular, we searched for differences in ecological condition over a five year interval, covering two periods (pre- and post-management). Firstly, we tested for temporal differences in the structure and composition of the subtidal macrobenthic assemblages of the estuary between the two periods. Secondly, we analyzed the relative performance of a set of ecological indicators to capture potential ecological changes between the two periods. Calculations of three different categories of ecological indicators were performed based on (1) diversity (Shannon–Wiener, Pielou, Margalef, Simpson and taxonomic diversity measures); (2) ecological groups (AMBI); and (3) thermodynamics (Eco-exergy and specific Eco-exergy). These ecological indicators were chosen due to their widespread use in the characterization of benthic communities, in order to capture and measure different aspects of the macrobenthic assemblages and also due to their frequent inclusion in several of the multimetric indices that are being tested under the scope of WDF implementation. Data requirements and availability were accounted for in the process of selecting the ecological indicators. This approach is consistent with the recent general trend of using multiple complementary indicators based on different ecological principles to determine the environmental quality of ecosystems (Dauer et al., 1993b, Salas et al., 2004). Lastly, we compared the ecological indicators performance with the information given by the analysis of macrofauna composition and structure in order to distinguish the actual usefulness of the tools for addressing specific management objectives.
Section snippets
Mondego estuary characterization and morphological evolution
The Mondego estuary is located in a warm-temperate region of the central Portuguese Atlantic coast (40°08′N, 8°50′W) and comprises two arms (north and south) with different hydrological characteristics, separated by an island (Fig. 1) (Marques et al., 1993, Marques et al., 2003, Marques et al., 2007). The estuary is under high urban pressure due to its location near a tourism center (Figueira da Foz), supports industrial activities, salt-works, and aquaculture farms, and receives high nutrient
Environmental variables
With regard to the PCA ordinations embracing the whole estuarine gradient (Fig. 2A and B), the first two components accounted for 65% of the variability in the data set. When the south arm area was considered alone (Fig. 2C and D), the first PCA axis (PC1) explained 45.2% of the variability in the data set, whereas both axes (PC1 and PC2) accounted for 66.4%. Therefore, the PCA 2-D plots provided a good summary of the samples relationship.
From the observation of the PCA plots coded for year (
Assessing the effectiveness of the recovery action
Concerning the environmental variables analyzed, our data showed no clear changes in the estuary water quality after the re-opening of the communication between both arms. Overall, results suggested that the management action did not produce any visible variation on the physico-chemical parameters in the post-management period. In spite of the south arm hydraulic circulation improvements, high nutrient concentrations continue to enter into the estuary mainly coming from agricultural runoff of
Conclusions
In general, the ecological indicators selected were effective in detecting the prevailing ecosystem conditions and behaved consistently with the subtidal ecological community. Most of the indicators tested (Margalef, Shannon–Wiener, Pielou, Simpson, AMBI and thermodynamic oriented indicators) were able to capture useful information about the state of the subtidal macrobenthic community as theoretically expected, although not always indicating an improvement in system ecological quality. In
Acknowledgements
The present study was carried out in the scope of the research projects RECONNECT (PTDC/MAR/64627/2006), EXTREMIS (III/36/2008), WISER (FP7-ENV2008-226273), and 3M-RECITAL (LTER/BIA-BEC/0019/2009). It was supported by the FCT (Portuguese National Board of Scientific Research) through a PhD grant (SFRH/BD/37644/2007) and by IMAR/FLAD Grants program from Luso-American Foundation for a 3-month study at Towson University, Maryland.
It was also subsidized by the European Social Fund and MCTES
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