Elsevier

Marine Pollution Bulletin

Volume 79, Issues 1–2, 15 February 2014, Pages 145-154
Marine Pollution Bulletin

Description of a Multimetric Phytoplankton Index (MPI) for the assessment of transitional waters

https://doi.org/10.1016/j.marpolbul.2013.12.025Get rights and content

Highlights

  • Phytoplankton dominance, diversity and biomass were used to assess water quality.

  • A multimetric index was set up to implement the European Water Framework Directive (WFD).

  • The index’s relationships with the main anthropogenic pressures were verified.

  • The index was shown to be reliable for the assessment of transitional waters.

Abstract

A Multimetric Phytoplankton Index (MPI) is proposed to support management policies for the assessment of transitional ecosystems and the implementation of the European Water Framework Directive. The MPI incorporates Hulburt’s dominance index, bloom frequency and Menhinick’s diversity index, calculated on the basis of phytoplankton species composition.

Chlorophyll a concentrations were also included, to provide biomass data and to guarantee continuity and comparison with past evaluations. The MPI was calculated by averaging the ratios of the resulting values of each metric to those of a reference site characterised by low anthropogenic impact.

The MPI was set up using data from over a 10-year period in several stations in Venice Lagoon (North-western Adriatic region), a highly valuable and heterogeneous transitional environment, subject to significant anthropogenic pressures. The dataset included physico-chemical data, nutrient and contaminant concentrations. Statistical analyses allowed us to gauge the MPI’s responses to anthropogenic pressures and to verify its reliability.

Introduction

The Clean Water Act (PL 92-500, 1972) in the USA and the Water Framework Directive (WFD, 2000/60/EC) and Marine Strategy Framework Directive (MSFD, 2008/56/EC) in Europe promoted extensive research designed to create assessment tools able to support intervention policies and recovery plans for aquatic ecosystems. The importance of fresh waters to both human beings and nature has long been recognised but wetlands are also vital to the health of wildlife and humans. Transitional systems play a key role in the regulation of river flows, water quality management, shoreline erosion control, exploitation of natural products, recreation, landscape aesthetics, and animal and plant diversity. It has been calculated that since the 16th century, in the continental United States 221 million acres of wetlands have been lost, along with 30–70% of Canada’s wetlands. In order to counteract these trends the North American Waterfowl Management Plan was adopted in 1986 and $4.5 billion was spent on protecting some 15 million acres of wetlands (U.S. Protection Environmental Agency). In Europe, attention to the quality of transitional waters has mainly been a consequence of the WFD 2000/60/EC, whose main aim is to achieve “good ecological and chemical status” for all surface waters by 2015. One of the most innovative aspects of the WFD is the significant role attributed to Biological Quality Elements (BQEs: phytoplankton, macrophytes, macrozoobenthos and fish) in the assessment of water body conditions. Implementation of Ecological Indices has thus become mandatory for EU Member States, stimulating and conducting investigations of community biodiversities and their relationships with anthropogenic pressures. In order to be compliant with the WFD, these indices must correctly represent the ecological status of water bodies and must be sensitive to anthropogenic pressures that cause waters to shift away from minimally-impacted reference conditions. In this way, common guidelines have been established in order to steer research towards shared assessment protocols. Indices for macrobenthos (Borja et al., 2000, Borja et al., 2008, Munari et al., 2009), macrophytes (Orfanidis et al., 2003, Ballesteros et al., 2007, Sfriso et al., 2009, Sfriso and Facca, 2011) and fish (Franco et al., 2009 and references therein) have been proposed for both coastal and transitional waters.

The good ecological status of transitional water ecosystems is often threatened by the presence of undesirable disturbances, defined as perturbation “that appreciably degrades or threatens the sustainable human use of that ecosystem” (Tett et al., 2007). The degradation may be driven by several factors: hydromorphological alterations, toxic chemical contamination, excess nutrient inputs, hypoxia, turbidity, suspended sediments, etc. (Borja et al., 2010). Of these stressors, eutrophication (the nutrient enrichment) has been shown to be responsible for significant deterioration of ecosystem health (Devlin et al., 2007, Brito et al., 2012a and references therein) and is one of the greatest threats to water quality in coastal areas (Coutinho et al., 2012). High nutrient availability favours the growth of algal biomass, leading to progressive shift from a seagrass-dominated system to a phytoplankton-dominated one, passing through an intermediate stage involving proliferation of bloom-forming opportunistic macroalgae (Coutinho et al., 2012 and references therein). Once the human pressures are removed or reduced, the recovery period varies significantly and it has been observed that seagrass meadows may take over 20 years to recover (Borja et al., 2010). In this context, it is of primary importance to create a network for promoting restoration measures (by means of specific laws, management policies, etc.) and to identify tools that can evaluate ecosystem status and the efficacy of the adopted measures. An a priori understanding of the interactions between anthropogenic pressures and specific biotic components is an essential precondition for planning recovery measures (Borja et al., 2010). Post-hoc measurements are then required, in order to verify the success of these measures. Biological indicators represent the main tools for completion of both of these phases.

Although, phytoplankton is known to be a sensitive biological indicator of eutrophication (Coutinho et al., 2012) and the community structure of primary producers is generally the best tool for diagnosing it, in the past interest in indicators of change tended to focus on macrobenthos (Tett et al., 2007). Thanks to the WFD, several proposals have also been made for macrophytes, as cited above.

In addition, the literature on phytoplankton within the context of the WFD is still far from complete with regard to both transitional (Sabetta et al., 2008a, Facca and Sfriso, 2009, Brito et al., 2012a, Brito et al., 2012b, Coutinho et al., 2012) and coastal waters (Sabetta et al., 2008b, Revilla et al., 2009, Spatharis and Tsirtsis, 2010), as recently noted by Garmendia et al. (2013). The latter authors focused on the difficulties inherent in the use of phytoplankton as an indicator of ecological water quality in accordance with the WFD, which requires the use of both taxonomic composition and chlorophyll a concentrations (Chl a). The importance of Chl a in eutrophication assessment is widely recognised (Lacouture et al., 2006, Devlin et al., 2007, Brito et al., 2012a, Brito et al., 2012b). However, its integration with community structure data may provide an even better understanding of environmental conditions, because the inclusion of additional metrics can render an index more sensitive (Garmendia et al., 2013). A huge effort has been made to assess Portuguese transitional and coastal waters, in which indices have been proposed using phytoplankton cell abundance and chlorophyll a concentrations (Brito et al., 2012a, Brito et al., 2012b, Coutinho et al., 2012). Due to lack of data, taxonomic composition is not an integral part of these indices but is only referenced in terms of the dominant species. Use of the entire community structure is a major challenge. Indeed, a previous study showed how diatom community structure in terms of biomass and abundance dominance curves can indicate transitional water quality (Facca and Sfriso, 2009). It was found that diatom species cell size and abundance correlated with stressed conditions, suggesting that community structure does indeed provide information on the general status of the environment. However, that index has some important disadvantages, such as the calculation of biomass by cell biovolume, which is seldom measured, and the use of Bacillariophyceae alone, although the phytoplankton community may be composed of many other classes such as Cryptophyceae, Dinophyceae, Euglenophyceae, Prasinophyceae and Prymnesiophyceae. Moreover, Chl a values are not considered.

Lugoli et al. (2012) recently proposed a new multimetric phytoplankton index combining cell size spectra, size classes, chlorophyll a and taxonomic richness thresholds. This index was found to consistently discriminate between anthropogenic and natural disturbance. However, as with Facca and Sfriso (2009) it uses cell size as a fundamental parameter for evaluation. Despite its recognised importance, this measure requires extra activity for operators and, in the context of a monitoring campaign, may result in costly action. Moreover, the laws of some European Member States, such as Italy, do not include the measurement of cell size in their monitoring protocols (ISPRA, 2011).

The aim of the present paper is to formulate a reliable assessment tool for the classification of transitional waters using phytoplankton as a BQE, in accordance with the WFD approach regarding the key role played by biodiversity. The proposed formulation integrates ecological research with the need to better understand the environmental conditions and to provide a tool that is easily applied by various types of operator, although taxonomic expertise is still required. Indeed, the “encouragement” of routine taxonomic studies will contribute significantly to the understanding of biodiversity and hence to better planning of management policies. Taking into account the observations in Garmendia et al. (2013), the following metrics were found to be sensitive to anthropogenic pressures: Hulburt’s dominance index, bloom frequency, Menhinick’s diversity index and Chl a. This new proposal, the Multimetric Phytoplankton Index (MPI), constitutes a complete tool as it includes information on taxonomic composition, cell abundance and biomass (Chl a), determined by analytical methods that have been commonly used and accepted for the last 50 years (Utermöhl, 1958, Holm-Hansen et al., 1965, Lorenzen, 1967). Moreover, the mathematical calculation of each metric is relatively easy and does not require sophisticated software. The MPI index has undergone intercalibration within the Mediterranean Geographic Group but the process has yet to be completed.

The MPI was set up using the case study of Venice Lagoon for two reasons: (i) it is a well-studied transitional water environment which allows comparison of distinct areas characterised by a range of ecological statuses (Solidoro et al., 2010 and references therein); (ii) concomitant data were collected over a 10-year period for the determination of nutrient and chlorophyll a concentrations and phytoplankton taxonomic composition. The latter is considered an essential requirement for establishing the relationship between anthropogenic pressures and biological indicators (Coutinho et al., 2012), and is one of the mandatory metrics required by the WFD for assessment of the ecological status of phytoplankton in transitional systems. In this context the MPI’s responses to anthropogenic pressures was verified along a gradient of impacts by means of multivariate statistical analyses and validated by expert judgment.

Section snippets

Study area

Venice Lagoon is a semi-enclosed water basin (mean depth ca. 1.0 m) with a surface area of ca. 550 km2. During a single tidal cycle (12 h), ca. 60% of the lagoon’s volume is exchanged with the waters of the north-western Adriatic Sea through three seaward inlets (from north to south, Lido, Malamocco and Chioggia, Fig. 1; Gačić et al., 2004). In terms of confinement, it has both choked and restricted waters (Kjerfve and Magill, 1989) and presents high spatial heterogeneity, being significantly

Data pre-treatment

Data on cell abundance were not subject to log10-transformation, which tends to flatten spatial variability, thus making it harder to discriminate between sites on the basis of community structure. In any case, the Lilliefors test for normality showed significant variability only for temperature and silicates (p < 0.05), and the Kolmogorov–Smirnov test showed significant variability (p > 0.05) for none of the considered parameters. Temperature and silicate concentrations were not in fact correlated

Discussion

The results of the present study confirm that metrics based on the phytoplankton community can provide an effective indicator of fluctuations in environmental conditions, as has been asserted (Bianchi et al., 2003, Lacouture et al., 2006, Socal et al., 2006, Facca and Sfriso, 2009, Lugoli et al., 2012). It is important that water samples are collected on a seasonal basis in order to produce a reliable ecosystem classification, going beyond phytoplankton temporal variations and hence focusing on

Acknowledgements

The authors are grateful to Mr. George Metcalf for the English editing and to the anonymous reviewer, who provided constructive comments to improve the manuscript.

References (61)

  • C. Facca et al.

    Changes in abundance and composition of phytoplankton and microphytobenthos due to increased sediment fluxes in the Venice lagoon, Italy

    Estuar. Coast. Shelf. Sci.

    (2002)
  • A. Franco et al.

    A habitat-specific fish-based approach to assess the ecological status of Mediterranean coastal lagoons

    Mar. Pollut. Bull.

    (2009)
  • M. Gačić et al.

    Temporal variations of water flow between the Venetian lagoon and the open sea

    J. Mar. Syst.

    (2004)
  • M. Garmendia et al.

    Phytoplankton composition indicators for the assessment of eutrophication in marine waters: present state and challenges within the European directives

    Mar. Pollut. Bull.

    (2013)
  • M. Ghezzo et al.

    Modeling the inter-annual variability of salinity in the lagoon of Venice in relation to the water framework directive typologies

    Ocean Coast. Manage.

    (2011)
  • G. Giordani et al.

    Simple tools for assessing water quality and trophic status in transitional water ecosystems

    Ecol. Indicat.

    (2009)
  • B. Kjerfve et al.

    Geographic and hydrodynamic characteristics of shallow coastal lagoons

    Mar. Geol.

    (1989)
  • F. Lugoli et al.

    Application of a new multi-metric phytoplankton index to the assessment of ecological status in marine and transitional waters

    Ecol. Indicat.

    (2012)
  • S. Orfanidis et al.

    An insight to the ecological evaluation index (EEI)

    Ecol. Indicat.

    (2003)
  • M. Revilla et al.

    Assessment of the phytoplankton ecological status in the Basque coast (northern Spain) according to the European Water Framework Directive

    J. Sea Res.

    (2009)
  • L. Sabetta et al.

    Marine phytoplankton size-frequency distributions: spatial patterns and decoding mechanisms

    Estuar. Coast. Shelf. Sci.

    (2008)
  • A. Sfriso et al.

    Macrophytes in the anthropic constructions of the Venice littorals and their ecological assessment by an integration of the “CARLIT” index

    Ecol. Indicat.

    (2011)
  • S. Spatharis et al.

    Ecological quality scales based on phytoplankton for the implementation of Water Framework Directive in the Eastern Mediterranean

    Ecol. Indicat.

    (2010)
  • A. Specchiulli et al.

    Environmental heterogeneity patterns and assessment of trophic levels in two Mediterranean lagoons: Orbetello and Varano, Italy

    Sci. Total Environ.

    (2008)
  • C.J.F. Ter Braak et al.

    A theory of gradient analysis

    Adv. Ecol. Res.

    (1988)
  • P. Tett et al.

    Defining and detecting undesirable disturbance in the context of marine eutrophication

    Mar. Pollut. Bull.

    (2007)
  • R. Zonta et al.

    Sediment chimica contamination of a shallow water area closet o the industrial zone of Porto Marghera (Venice Lagoon, Italy)

    Mar. Pollut. Bull.

    (2007)
  • A. Zuliani et al.

    Freshwater discharge from the drainage basin to the Venice lagoon (Italy)

    Environ. Int.

    (2005)
  • L. Airoldi et al.

    Loss, status and trends for coastal marine habitats of Europe

  • Autorità di Bacino delle Alpi Orientali. 2010. Management Plan – subunit hydrographic drainage basin, Venice lagoon and...
  • Cited by (17)

    • Large-scale testing of phytoplankton diversity indices for environmental assessment in Mediterranean sub-regions (Adriatic, Ionian and Aegean Seas)

      2021, Ecological Indicators
      Citation Excerpt :

      These differences can be attributed to several factors, but one important reason is certainly the fact that phytoplankton is listed as a key biological element in Water Framework Directive (WFD; 2000/60/EC), whereas other groups of pelagic organisms are not (Barbone et al., 2014). Nevertheless, specific, operational phytoplankton indicators that relate exclusively to the biodiversity aspect of Mediterranean Sea are rarer and their use is mainly restricted to certain areas (e.g., Facca et al., 2014; Ninčević Gladan et al., 2015; Pachés et al., 2012; Romero et al., 2013). To bridge this “never-ending” gap between the individual case studies and a common approach, there is an urgent need for a summary case study that would cover areas on a larger spatial scale with different structural and functional characteristics of the pelagic habitat.

    • Changes in marine phytoplankton diversity: Assessment under the Marine Strategy Framework Directive

      2019, Ecological Indicators
      Citation Excerpt :

      Dominance phenomena and significant changes in phytoplankton community structure can occur in impacted areas (e.g. Bužančić et al., 2016). Here, as a dominance measure, the Hulburt index (δ) was mainly selected for its ease of interpretation (as a percentage, where a high value indicates high dominance) but also for its recent applications in water quality assessments (Facca et al., 2014). Using the Principal Component Analysis, the Brillouin index (HB) was found to be the only dominance measure that explained the variations in the environment but since this metric was interrelated with D and thus likely to be redundant, the former was not retained.

    View all citing articles on Scopus
    View full text