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Diversity of European seagrass indicators:
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Patterns within and across regions
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Núria Marbà1*, Dorte Krause-Jensen2, Teresa Alcoverro3, Sebastian Birk4, Are
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Pedersen5, Joao M Neto6, Sotiris Orfanidis7, Joxe M Garmendia8, Iñigo Muxika8,
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Angel Borja8, Kristina Dencheva9 and Carlos M. Duarte1,10
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Department of Global Change Research, IMEDEA (CSIC-UIB), Institut Mediterrani d’Estudis Avançats, Miquel Marquès 21, 07190 Esporles (Illes Balears), Spain
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National Environmental Research Institute, Department of Marine Ecology, Aarhus University, Frederiksborgvej 399, DK-4000 Roskilde, Denmark
3 Department
of Marine Ecology, Centre d’Estudis Avançats de Blanes (CEAB-CSIC).
C/Accés a la Cala St. Francesc, 14, 17300 Blanes. Girona, Spain 4 Department
of Applied Zoology/Hydrobiology, University of Duisburg-Essen,
Universitätstraße 5, 45117 Essen, Germany
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5 NIVA,
Gaustadalléen 21, NO-0349 OSLO, Norway
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6 IMAR
– Institute of Marine Research (CMA), Dep. Life Sciences, University of
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Coimbra, Largo Marquês Pombal, 3004-517 Coimbra, Portugal 7 National
Agricultural Research Fundation, Fisheries Research Institute, 640 07
Nea Peramos, Kavala, Greece 8 AZTI-Tecnalia;
Herrera Kaia, Portualdea s/n; 20110 Pasaia (Spain)
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Institute of Oceanology, Bulgarian Academy of Sciences, PO Box 152, 9000 Varna, Bulgaria
10 UWA
Oceans Institute, The University of Western Australia. 35 Stirling Highway,
6009 - Crawley (WA). Australia
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* Corresponding author: e-mail
[email protected]; telephone: +34
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971611720; FAX: +34 971611761
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Abstract
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Seagrasses are key components of coastal marine ecosystems and many
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monitoring programmes worldwide assess seagrass health and apply seagrasses
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as indicators of environmental status. This study aims at identifying the diversity
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and characteristics of seagrass indicators in use within and across European
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ecoregions in order to provide an overview of seagrass monitoring effort in
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Europe. We identified 49 seagrass indicators used in 42 monitoring programmes
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and including a total of 51 metrics. The seagrass metrics represented 6 broad
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categories covering different seagrass organizational levels and spatial scales. The
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large diversity is particularly striking considering that the pan-European Water
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Framework Directive sets common demands for the presence and abundance of
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seagrasses and related disturbance-sensitive species. The diversity of indicators
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reduces the possibility to provide pan-European overviews of the status of
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seagrass ecosystems. The diversity can be partially justified by differences in
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species, differences in habitat conditions and associated communities but also
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seems to be determined by tradition. Within each European region, we strongly
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encourage the evaluation of seagrass indicator-pressure responses and
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quantification of the uncertainty of classification associated to the indicator in
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order to identify the most effective seagrass indicators for assessing ecological
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quality of coastal and transitional water bodies.
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Keywords: monitoring, Zostera marina, Zostera noltii, Cymodocea nodosa, Posidonia
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oceanica, European Water Framework Directive, metrics
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Introduction
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Global human population has doubled during the second half of the 20th
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Century (Cohen 1995) now exceeding 7 billion people. Twenty three percent of
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human population inhabits areas located within 100 km from the ocean with the
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highest population density occurring within the closest 10 km (Nicholls & Small
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2002). The rapid growth of the human population in the coastal zone is
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transforming both coastal land and marine environments. Natural ecosystems are
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being replaced by urban areas, artificial structures (e.g. harbors, dikes) and
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infrastructures to produce resources (e.g. food, freshwater, energy). Inputs of
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nutrients, organic matter and contaminants to the coastal zone have also increased
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worldwide (Nixon & Fulweiler 2009). As a result, there is a widespread
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deterioration of coastal environmental quality, evidenced by a decrease of water
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transparency, coastal eutrophication and coastal erosion and coastal key
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ecosystems, such as seagrass meadows, are declining at an alarming rate (0.9 % yr-
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1,
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Waycott et al 2009). Seagrass meadows are the dominant marine ecosystem of sandy coastal
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areas, extending from the tropics to the poles except in Antarctica. Seagrasses
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encompass about 60 species of clonal angiosperms adapted to life in the sea
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(Hemminga & Duarte 2000). Four seagrass species occur in European waters,
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including the small, fast growing and short lived Zostera noltii, which is the most
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ubiquitous, Z. marina, dominant in most European seas but rare in the
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Mediterranean, Cymodocea nodosa, occurring in the Mediterranean and the
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southern NE Atlantic, and the large, slow growing and long lived Posidonia
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oceanica, endemic to the Mediterranean (den Hartog 1970; Hemminga & Duarte
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2000). Seagrasses are present from the intertidal or shallow subtidal (Z. noltii)
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down to 5-15 meters depth in North European waters (Z. marina) and to 40 meters
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in clear Mediterranean waters (C. nodosa and P. oceanica) along the European
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coastline (Duarte et al. 2007).
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Because of the key ecological services they provide to the coastal zone,
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seagrass meadows rank amongst the most valuable ecosystems in the biosphere
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(Costanza et al. 1997). They are highly productive, influence the structural
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complexity of habitats, enhance biodiversity, play important roles in global carbon
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and nutrient cycling, stabilize water flow and promote sedimentation, thereby
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reducing particle loads in the water as well as coastal erosion (Hemminga &
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Duarte 2000; Jones et al. 1994; Orth et al. 2006). Since seagrass meadows are
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experiencing global declines (e.g. Duarte 2009; Short and Wyllie-Echeverria 1996;
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Waycott et al. 2009) and because recovery, at least for the slow growing species,
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may be irreversible at human-time scales (Hemminga & Duarte 2000), monitoring
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programmes aiming at assessing seagrass health and success of coastal restoration
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efforts are proliferating worldwide (e.g., Orth et al.; 2006; Short et al.; 2006). The
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high sensitivity of seagrasses to environmental deterioration (e.g., decline of water
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transparency, eutrophication, erosion, warming) and the widespread geographical
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distribution of these plants also make seagrasses useful “miner’s canaries” of
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coastal deterioration (Orth et al. 2006). Indeed, several policies aiming at
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improving marine ecological quality (Europe: Water Framework Directive (WFD,
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2000/60/EC) and the Marine Strategy Framework Directive (MSFD, 2008/56/EC);
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USA: Clean Water Act (CWA), National Estuary Programme (www.epa.gov/nep))
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use seagrasses as indicators to assess ecosystem quality (Borja et al. 2008, 2012).
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For instance, the European WFD defines “good ecological status” of coastal waters 5
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with respect to seagrasses, other angiosperms and macroalgae as a situation
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where “most disturbance sensitive macroalgal and angiosperm taxa associated with
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undisturbed conditions are present and the level of macroalgal cover and
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angiosperm abundance shows slight signs of disturbance”.
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Monitoring programmes use a wide repertoire of indicators to evaluate the
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status of seagrass meadows, representing different structural and functional levels
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and different spatial scales; including meadow distribution and extent, abundance,
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shoot characteristics, chemical composition of the plants, and process rates such as
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growth or population dynamics (e.g. Borum et al. 2004; Lopez y Royo et al. 2010).
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Often, indicators of other brackish angiosperms, macroalgae and fauna present in
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seagrass communities are also considered. Monitoring programmes currently
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conducted in Europe in compliance with the WFD, as well as aiming at assessing
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conservation status of these endangered ecosystems, comprise a selected set of
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seagrass indicators that may vary across species and, hence, regions.
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Here we examine European seagrass monitoring programmes and review
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the diversity and characteristics of indicators in use in seagrass monitoring
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programmes within and across European ecoregions. We do so by compiling the
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seagrass indicators available to assess ecological quality of European coastal
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waters and conservation status of European seagrass meadows.
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Methods We searched the literature and monitoring programmes to identify indicators used in European seagrass monitoring programmes to assess the
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ecological status of seagrass meadows and coastal environmental quality in the 4
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European ecoregions: The North East Atlantic, the Baltic, the Mediterranean and
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the Black seas. We extracted information on seagrass indicators used in the WFD
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from the survey conducted by the EU-project WISER (Birk et al. 2010). We
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supplemented the database by searching the scientific and the grey literature and
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through further communication with national experts on seagrass monitoring.
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We used the following terminology: ‘Programme’ refers to a seagrass
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monitoring programme in a specific area (e.g. ‘Monitoring programme of
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conservation status of P. oceanica in Murcia‘). Each programme includes one or
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more ‘indicators’, representing a single ‘metric’ or a composite of metrics (‘an
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index’). The term ‘metric’ is here used in a broad sense encompassing the term
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‘parameter’. For example ‘seagrass depth limit’ is a metric that uses the average
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level of the parameter ‘seagrass depth limit’ in an assessment of water quality.
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Similarly ‘density’ or ‘aboveground biomass’ are metrics that use the average level
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of the parameters ‘density’ and ‘biomass’ at a given water depth, and the metric
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‘Cymoskew’ uses the skewness of the distribution of the parameter ‘shoot length’
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in the assessment of ecological status. An ‘index’ is composed of several metrics,
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collapsing various metrics of the seagrass meadow onto a single value. For
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example, the indicator ‘POMI’ (Posidonia oceanica monitoring Index, Romero et al.
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2007) is an index composed of up to 14 different seagrass metrics, while ‘Seagrass
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depth limit’ is an indicator composed of just one metric.
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For each monitoring programme we allocated each of the metrics
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composing the seagrass indicators to one of the following categories: ‘Distribution’,
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‘Abundance’, ‘Shoot characteristics’, ‘Processes’, ‘Chemical constituents’ and
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‘Associated flora and fauna’ (Table 1). The category ‘Associated flora and fauna’ 7
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was only considered in the cases when the research programme also included at
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least an indicator of a seagrass component.
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Metrics sharing a large degree of commonality were described in common
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terms. For instance, some programmes express the abundance of sensitive species
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as cover and other as biomass and we used the general term ‘sensitive species
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abundance’ (Table 1) to represent both. Metrics describing maximum depth limits
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and depth limits of a specific percentage cover were also grouped as one (i.e.
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“depth limit”, Table 1). Moreover, all metrics describing species composition,
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species number or community structure grouped under the common term
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‘Diversity’. The Portuguese intertidal seagrass index (Neto et al . unpublished)
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represents a special case as it includes ‘species composition’ as a metric even
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though Z. noltii is the only seagrass potentially present, so in this case ‘diversity’
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covers information on presence or absence of this species only. This grouping of
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metrics implied that our compilation represents a minimum estimate of the total
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number of European seagrass metrics in use. However, the number of metrics
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contained in individual indicators is not affected by the groupings, except in the
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case of the Swedish index ‘Multispecies maximum depth index’ and the German
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index ‘Balcosis’. The ‘Multispecies maximum depth index’ combines the depth limit
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of a selection of species of which Z. marina makes part in few areas, but rather than
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listing depth limits the entire selection of species as individual metrics, we
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included only ‘seagrass depth limit’ and ‘depth limit of selected species’. We also
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underestimate the number of metrics in the German indicator ‘Balcosis’ because
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we grouped the metrics ‘opportunist proportion in the seagrass zone’ and
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‘opportunist proportion in the red algae zone’ into the metric ‘tolerant species
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proportion’.
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Some monitoring programmes collect samples of more metrics than are
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used in the indicators, but our compilation does not list such additional metrics.
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For example, we listed the 14 metrics that potentially make part of POMI, but did
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not list the depth limit and depth limit type of P. oceanica, which is not used to
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calculate the POMI index even though it is assessed every 2-3 years e.g. along the
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Catalan coast. The 14 potential POMI metrics are sometimes reduced to 7-9
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metrics actually used but, as the selection may vary between areas and over time,
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we listed those used at least in one survey by the research programme.
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Results
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Quantification of seagrass monitoring programmes and indicators
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We identified 42 monitoring programmes of European seagrass meadows
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aiming at evaluating seagrass health (11 programmes), assessing coastal quality
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(28 programmes) or both (3 programmes, Table 2). The monitoring programmes
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span across the four European ecoregions, the North East Atlantic, the Baltic, the
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Mediterranean and the Black seas, and involve the four European seagrass species.
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However, the monitoring effort, in terms of number of programmes, allocated to Z.
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nolti, Z. marina and P. oceanica meadows is 6 to 8 fold greater than that to C.
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nodosa (Table 2). The European seagrass monitoring programmes examine a total
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of 49 indicators of seagrass health (Table 2), but only 25 of them are monitored in
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P. oceanica, 19 in Z. marina, 12 in Z. noltii and 3 in C. nodosa (Table 2).
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Metrics included in seagrass indicators
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The seagrass indicators identified included a total of 51 metrics
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representing a wide range of structural and functional aspects of seagrass
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ecosystems, which we grouped in 6 different categories (Table 1). Five categories
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relate directly to seagrasses while one relates to the flora and fauna associated
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with the seagrasses. The seagrass categories consider structural aspects ranging
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from large-scale distribution patterns in entire coastal areas and smaller scale
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abundance patterns in individual seagrass meadows to characteristics of
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individual shoots, as well as process and rates of change at shoot or meadow scale
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and plant chemical constituents. The category representing the associated flora
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and fauna characterizes diversity aspects based on species or functional groups
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(e.g. tolerant versus sensitive species, presence of epiphytes) as well as
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distribution and abundance patterns of species associated with the seagrasses (e.g.
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depth limits of other angiosperms or macroalgae).
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The 49 seagrass indicators of the various European monitoring
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programmes include from 1 to 14 metrics each. Seagrass indicators based on just
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one metric are by far the most common, accounting for 61% of the indicators in
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use (Fig. 1). These only describe a limited aspect of the seagrass ecosystem, but
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seagrass monitoring programmes often quantify several indicators together and
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thereby provide a more complete description of the ecosystem. The multi-metric
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indicators (indices), on the other hand, cover up to 4 metric categories each and
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thereby synthesize several aspects of the ecosystem in one estimate (Table 2).
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The top-three seagrass metrics mostly used in Europe, as evaluated based
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on the number of monitoring programmes using them are shoot density (included
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in 24 programmes) and cover (included in 18 programmes) both belonging to the
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category ‘abundance’, and depth limit (included in 16 programmes) belonging to
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the category ‘distribution’ (Fig. 2). In addition, the metric ‘Change in density’,
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which is included in 2 programmes also relies on measurements of shoot density.
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The most monitored seagrass category is ‘Abundance’ (included in 47
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programmes) closely followed by ‘Distribution’ and ‘Shoot characteristics’
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(included in 33 and 34 programmes, respectively), while ‘Processes’ and ‘Chemical
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constituents’ are slightly less frequently monitored (included in 29 and 30
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programmes respectively) (Fig. 2). The associated flora and fauna is also a very
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commonly monitored category (included in 45 programmes) (Fig. 2). While the
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categories ‘Distribution’ and ‘Abundance’ are among the most monitored
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categories and also include the top-three metrics, the remaining categories
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encompass multiple metrics, each of which is only infrequently (
