Diversity of European seagrass indicators: patterns within and across regions

WATER BODIES IN EUROPE

Diversity of European seagrass indicators: patternswithin and across regions

Nuria Marba • Dorte Krause-Jensen • Teresa Alcoverro • Sebastian Birk •

Are Pedersen • Joao M. Neto • Sotiris Orfanidis • Joxe M. Garmendia •

Inigo Muxika • Angel Borja • Kristina Dencheva • Carlos M. Duarte

Received: 7 May 2012 / Accepted: 24 November 2012 / Published online: 21 December 2012

� Springer Science+Business Media Dordrecht 2012

Abstract Seagrasses are key components of coastal

marine ecosystems and many monitoring programmes

worldwide assess seagrass health and apply seagrasses

as indicators of environmental status. This study aims

at identifying the diversity and characteristics of

seagrass indicators in use within and across European

ecoregions in order to provide an overview of seagrass

monitoring effort in Europe. We identified 49 seagrass

indicators used in 42 monitoring programmes and

including a total of 51 metrics. The seagrass metrics

represented 6 broad categories covering different

seagrass organizational levels and spatial scales. The

large diversity is particularly striking considering that

the pan-European Water Framework Directive sets

common demands for the presence and abundance of

seagrasses and related disturbance-sensitive species.

The diversity of indicators reduces the possibility to

provide pan-European overviews of the status ofGuest editors: C. K. Feld, A. Borja, L. Carvalho & D. Hering /

Water bodies in Europe: integrative systems to assess

ecological status and recovery

N. Marba (&) � C. M. Duarte

Department of Global Change Research, IMEDEA

(CSIC-UIB), Institut Mediterrani d’Estudis Avancats,

Miquel Marques 21, 07190 Esporles, Illes Balears, Spain

e-mail: [email protected]

D. Krause-Jensen

National Environmental Research Institute, Department of

Marine Ecology, Aarhus University, Frederiksborgvej

399, 4000 Roskilde, Denmark

T. Alcoverro

Department of Marine Ecology, Centre d’Estudis

Avancats de Blanes (CEAB-CSIC), C/Acces a la Cala St.

Francesc, 14, 17300 Blanes, Girona, Spain

S. Birk

Department of Applied Zoology/Hydrobiology,

University of Duisburg-Essen, Universitatstraße 5,

45117 Essen, Germany

A. Pedersen

NIVA, Gaustadalleen 21, 0349 Oslo, Norway

J. M. Neto

Department of Life Sciences, IMAR—Institute of Marine

Research (CMA), University of Coimbra, Largo Marques

Pombal, 3004-517 Coimbra, Portugal

S. Orfanidis

National Agricultural Research Foundation, Fisheries

Research Institute, 640 07 Nea Peramos, Kavala, Greece

J. M. Garmendia � I. Muxika � A. Borja

AZTI-Tecnalia, Herrera Kaia, Portualdea s/n,

20110 Pasaia, Spain

K. Dencheva

Institute of Oceanology, Bulgarian Academy of Sciences,

P.O. Box 152, 9000 Varna, Bulgaria

C. M. Duarte

UWA Oceans Institute, The University of Western

Australia, 35 Stirling Highway, Crawley, WA 6009,

Australia

123

Hydrobiologia (2013) 704:265–278

DOI 10.1007/s10750-012-1403-7

seagrass ecosystems. The diversity can be partially

justified by differences in species, differences in

habitat conditions and associated communities but

also seems to be determined by tradition. Within each

European region, we strongly encourage the evalua-

tion of seagrass indicator–pressure responses and

quantification of the uncertainty of classification

associated to the indicator in order to identify the

most effective seagrass indicators for assessing eco-

logical quality of coastal and transitional water bodies.

Keywords Monitoring � Zostera marina � Zostera

noltii � Cymodocea nodosa � Posidonia oceanica �European Water Framework Directive � Metrics

Introduction

Global human population has doubled during the

second half of the twentieth century (Cohen, 1995)

now exceeding 7 billion people. Twenty-three percent

of human population inhabits areas located within

100 km from the ocean with the highest population

density occurring within the closest 10 km (Nicholls

& Small, 2002). The rapid growth of the human

population in the coastal zone is transforming both

coastal land and marine environments. Natural eco-

systems are being replaced by urban areas, artificial

structures (e.g., harbors and dikes) and infrastructures

to produce resources (e.g., food, freshwater, energy).

Inputs of nutrients, organic matter and contaminants to

the coastal zone have also increased worldwide

(Nixon & Fulweiler, 2009). As a result, there is a

widespread deterioration of coastal environmental

quality, evidenced by a decrease of water transpar-

ency, coastal eutrophication and coastal erosion and

coastal key ecosystems, such as seagrass meadows, are

declining at an alarming rate (0.9% year-1, Waycott

et al., 2009).

Seagrass meadows are the dominant marine eco-

system of sandy coastal areas, extending from the

tropics to the poles except in Antarctica. Seagrasses

encompass about 60 species of clonal angiosperms

adapted to life in the sea (Hemminga & Duarte, 2000).

Four seagrass species occur in European waters,

including the small, fast growing and short lived

Zostera noltii, which is the most ubiquitous, Z. marina,

dominant in most European seas but rare in the

Mediterranean, Cymodocea nodosa, occurring in the

Mediterranean and the southern NE Atlantic, and the

large, slow growing and long lived Posidonia

oceanica, endemic to the Mediterranean (den Hartog,

1970; Hemminga & Duarte, 2000). Seagrasses are

present from the intertidal or shallow subtidal

(Z. noltii) down to 5-15 meters depth in North

European waters (Z. marina) and to 40 m in clear

Mediterranean waters (C. nodosa and P. oceanica)

along the European coastline (Duarte et al., 2007).

Because of the key ecological services they provide

to the coastal zone, seagrass meadows rank amongst

the most valuable ecosystems in the biosphere

(Costanza et al., 1997). They are highly productive,

influence the structural complexity of habitats,

enhance biodiversity, play important roles in global

carbon and nutrient cycling, stabilize water flow and

promote sedimentation, thereby reducing particle

loads in the water as well as coastal erosion (Jones

et al., 1994; Hemminga & Duarte, 2000; Orth et al.,

2006). Since seagrass meadows are experiencing

global declines (e.g., Short & Wyllie-Echeverria,

1996; Duarte et al., 2008; Waycott et al., 2009) and

because recovery, at least for the slow growing

species, may be irreversible at human-time scales

(Hemminga & Duarte, 2000), monitoring programmes

aiming at assessing seagrass health and success of

coastal restoration efforts are proliferating worldwide

(e.g., Orth et al., 2006; Short et al., 2006). The high

sensitivity of seagrasses to environmental deteriora-

tion (e.g., decline of water transparency, eutrophica-

tion, erosion, warming) and the widespread

geographical distribution of these plants also make

seagrasses useful ‘‘miner’s canaries’’ of coastal dete-

rioration (Orth et al., 2006). Indeed, several policies

aiming at improving marine ecological quality

[Europe: Water Framework Directive (WFD, 2000/60/

EC) and the Marine Strategy Framework Directive

(MSFD, 2008/56/EC); USA: Clean Water Act (CWA),

National Estuary Programme (www.epa.gov/nep)] use

seagrasses as indicators to assess ecosystem quality

(Borja et al., 2008, 2012). For instance, the European

WFD defines ‘‘good ecological status’’ of coastal

waters with respect to seagrasses, other angiosperms

and macroalgae as a situation where ‘‘most disturbance

sensitive macroalgal and angiosperm taxa associated

with undisturbed conditions are present and the level of

266 Hydrobiologia (2013) 704:265–278

123

macroalgal cover and angiosperm abundance shows

slight signs of disturbance’’.

Monitoring programmes use a wide repertoire of

indicators to evaluate the status of seagrass meadows,

representing different structural and functional levels

and different spatial scales; including meadow distri-

bution and extent, abundance, shoot characteristics,

chemical composition of the plants, and process rates

such as growth or population dynamics (e.g., Borum

et al., 2004; Lopez y Royo et al., 2010). Often, indicators

of other brackish angiosperms, macroalgae and fauna

present in seagrass communities are also considered.

Monitoring programmes currently conducted in Europe

in compliance with the WFD, as well as aiming at

assessing conservation status of these endangered

ecosystems, comprise a selected set of seagrass indica-

tors that may vary across species and, hence, regions.

Here, we examine European seagrass monitoring

programmes and review the diversity and character-

istics of indicators in use in seagrass monitoring

programmes within and across European ecoregions.

We do so by compiling the seagrass indicators

available to assess ecological quality of European

coastal waters and conservation status of European

seagrass meadows.

Methods

We searched the literature and monitoring pro-

grammes to identify indicators used in European

seagrass monitoring programmes to assess the eco-

logical status of seagrass meadows and coastal envi-

ronmental quality in the 4 European ecoregions: The

North East Atlantic, the Baltic, the Mediterranean and

the Black seas. We extracted information on seagrass

indicators used in the WFD from the survey conducted

by the EU-project WISER (Birk et al., 2010). We

supplemented the database by searching the scientific

and the grey literature and through further communi-

cation with national experts on seagrass monitoring.

We used the following terminology: ‘‘Programme’’

refers to a seagrass monitoring programme in a

specific area (e.g. ‘‘Monitoring programme of conser-

vation status of P. oceanica in Murcia’’). Each

programme includes one or more ‘‘indicators’’, repre-

senting a single ‘‘metric’’ or a composite of metrics

(‘‘an index’’). The term ‘‘metric’’ is here used in a

broad sense encompassing the term ‘‘parameter’’. For

example ‘‘seagrass depth limit’’ is a metric that uses

the average level of the parameter ‘‘seagrass depth

limit’’ in an assessment of water quality. Similarly

‘‘density’’ or ‘‘aboveground biomass’’ are metrics that

use the average level of the parameters ‘‘density’’ and

‘‘biomass’’ at a given water depth, and the metric

‘‘Cymoskew’’ uses the skewness of the distribution of

the parameter ‘‘shoot length’’ in the assessment of

ecological status. An ‘‘index’’ is composed of several

metrics, collapsing various metrics of the seagrass

meadow onto a single value. For example, the indicator

‘‘POMI’’ (Posidonia oceanica monitoring index, Ro-

mero et al., 2007) is an index composed of up to 14

different seagrass metrics, while ‘‘Seagrass depth

limit’’ is an indicator composed of just one metric.

For each monitoring programme we allocated each

of the metrics composing the seagrass indicators

to one of the following categories: ‘‘Distribution’’,

‘‘Abundance’’, ‘‘Shoot characteristics’’, ‘‘Processes’’,

‘‘Chemical constituents’’, and ‘‘Associated flora and

fauna’’ (Table 1). The category ‘‘Associated flora and

fauna’’ was only considered in the cases when the

research programme also included at least an indicator

of a seagrass component.

Metrics sharing a large degree of commonality

were described in common terms. For instance, some

programmes express the abundance of sensitive spe-

cies as cover and other as biomass and we used the

general term ‘‘sensitive species abundance’’ (Table 1)

to represent both. Metrics describing maximum depth

limits and depth limits of a specific percentage cover

were also grouped as one (i.e. ‘‘depth limit’’, Table 1).

Moreover, all metrics describing species composition,

species number or community structure grouped

under the common term ‘‘Diversity’’. The Portuguese

intertidal seagrass index (Neto et al. unpublished)

represents a special case as it includes ‘‘species

composition’’ as a metric even though Z. noltii is the

only seagrass potentially present, so in this case

‘‘diversity’’ covers information on the presence or the

absence of this species only. This grouping of metrics

implied that our compilation represents a minimum

estimate of the total number of European seagrass

metrics in use. However, the number of metrics

contained in individual indicators is not affected by the

groupings, except in the case of the Swedish index

‘‘Multispecies maximum depth index’’ and the Ger-

man index ‘‘Balcosis’’. The ‘‘Multispecies maximum

depth index’’ combines the depth limit of a selection of

Hydrobiologia (2013) 704:265–278 267

123

species of which Z. marina makes part in few areas, but

rather than listing depth limits the entire selection of

species as individual metrics, we included only ‘‘sea-

grass depth limit’’ and ‘‘depth limit of selected species’’.

We also underestimate the number of metrics in the

German indicator ‘‘Balcosis’’ because we grouped the

metrics ‘‘opportunist proportion in the seagrass zone’’

and ‘‘opportunist proportion in the red algae zone’’ into

the metric ‘‘tolerant species proportion’’.

Some monitoring programmes collect samples of

more metrics than are used in the indicators, but our

compilation does not list such additional metrics.

For example, we listed the 14 metrics that poten-

tially make part of POMI, but did not list the depth

limit and depth limit type of P. oceanica, which is

not used to calculate the POMI index even though it

is assessed every 2–3 years, e.g., along the Catalan

coast. The 14 potential POMI metrics are sometimes

reduced to 7–9 metrics actually used but, as the

selection may vary between areas and over time, we

listed those used at least in one survey by the

research programme.

Results

Quantification of seagrass monitoring programmes

and indicators

We identified 42 monitoring programmes of European

seagrass meadows aiming at evaluating seagrass

Table 1 List of categories of European seagrass indicators

(in bold) and the metrics contained in them

Distribution

Depth limit

Depth limit type

Area

Abundance

Shoot density

Cover

Aboveground biomass

Above/belowgr. biomass

Dead matte cover

Shoot characteristics

Shoot biomass

Shoot leaf area

No. of leaves per shoot

Leaf width

Leaf length skewness

Leaf necrosis

Broken leaves

Plagiotrophic rhizomes

Processes

Leaf production

Rhizome production

Rhizome elongation

Change in density

Shoot recruitment

Shoot mortality

Flowering

Shoot burial, rhizome baring

Herbivore pressure

Chemical constituents

Rhizome N

Rhizome P

Rhizome d15N

Rhizomes d34S

Rhizome sucrose

Rhizome Cu

Rhizome Pb

Rhizome Zn

Associated flora and fauna

Diversity—soft bot. sp.

Diversity—macroalgae

Diversity—all flora

Tolerant sp. proportion

Tolerant sp. abundance

Sensitive sp. proportion

Table 1 continued

Sensitive sp. abundance

Tolerant species area

Vegetation abundance

Fucus abundance

Furcellaria proportion

Invasive sp. presence

Epiphyte N

Epiphyte biomass

Depth limit—Fucus

Depth limit—Characeans

Depth limit—selected sp.

Macrofauna abundance

The first five categories relate directly to the seagrasses while

the last category relate to the entire community

268 Hydrobiologia (2013) 704:265–278

123

Table 2 List of European seagrass indicators with information

on the source where the indicator is described (reference), the

region, country, and the monitoring programme using them.

The seagrass species and categories and number of metrics

assessed by the indicator are also indicated. Indicators used in

European Water Frame Directive programmes are identified (*)

Indicator Reference1 Region Country Monitoring Programme (MP) Seagrass species Category

NE

. Atla

ntic

B

altic

B

lack

Sea

M

edite

rran

ean

P. o

cean

ica

C. n

odos

a Z

. mar

ina

Z. n

olti

i se

agra

sses

D

istr

ibut

ion

Abu

ndan

ce

Shoo

t cha

ract

eris

tics

Proc

esse

s

Che

mic

al c

onst

ituen

ts

Ass

ocia

ted

flor

a &

fau

na

Associated macrofauna 1 x Spain Murcia- conservation status MP x 1

Area 2 x Denmark Øresund fixed link MP 1996-2000

x x 1

,3- 4 x x Denmark National MP2 x 1

- x Norway Habitat mapping x

Macrophytes (*) x Germany

Macrophytes (*) x Romania x 3

Vegetation (*) x The Netherlands

1

Intertidal seagrass (*) x Germany Balcosis (*) x Germany 5Macrophytes (*) x Poland 1Biomass

2000 Cover

2000 - -

MP -

MP -

status MP - - - -

Regional MP -

Regional MP - - -

Regional MP CS (*) CymoSkew (*) CYMOX (*) Dead matte

Regional MP Density

2000 Depth limit (*)

2000 - - - - -

2 x Denmark Øresund fixed link MP 1996-

2 x Denmark Øresund fixed link MP 1996-

3, 4 x x Denmark National MP 5 x Spain Catalonia- conservation status

6 x Spain Valencia- conservation status

7 x Spain Balearic Islands- conservation

8 x Algeria Algeria-MP

8 x France Provence Alpes Côte d'Azur -

8 x France Languedoc Roussillon-

8 x Italy National MP

8 x Italy Liguria, Tuscany, Latium-

x Valencia9 x Greece

x Spain8 x France Languedoc Roussillon-

2 x Denmark Øresund fixed link MP 1996-

2 x Denmark Øresund fixed link MP 1996-

3, 4 x x Denmark National MP

8 x Algeria Algeria-MP

8 x France Provence Alpes Côte d'Azur - Regional MP

1

x x 1 1 3

x x 1

x x 1 1 1x x 1x xx 1

x 1

x 1x 1

x 1

x 1

1 x Spain Murcia- conservation status MP x 1x 1

8 x France Corsica- Regional MP x 1x 1

x 1

x 18 x Italy Liguria- Regional MP x 1

x 1

x 3 3 2 1x 1x 2 6 1

x 1

x 1

x 1

x 11 x Spain Murcia- conservation status MP x 1

x 18 x France Corsica- Regional MP x 1

x 1

Hydrobiologia (2013) 704:265–278 269

123

Table 2 continued

Indicator Reference1 Region Country Monitoring Programme (MP) Seagrass species Category

NE

. Atla

ntic

B

altic

B

lack

Sea

M

edite

rran

ean

P. o

cean

ica

C. n

odos

a Z

. mar

ina

Z. n

olti

i se

agra

sses

D

istr

ibut

ion

Abu

ndan

ce

Shoo

t cha

ract

eris

tics

Proc

esse

s

Che

mic

al c

onst

ituen

ts

Ass

ocia

ted

flor

a &

fau

na

- Regional MP

x 1

- x 1- -

Regional MP x 1

- x 1 1

- -

Regional MP x 1

8 x France Languedoc Roussillon-

8 x Italy National MP8 x Italy Liguria- Regional MP x 18 x Italy Liguria, Tuscany, Latium-

x Norway Habitat mappingDepth limit type 8 x Algeria Algeria-MP

8 x France Corsica- Regional MP x 18 x France Provence Alpes Côte d'Azur -

- Regional MP

- - -

Regional MP EEI (*) x Slovenia 2- (*) x Greece 2EEI & S/W x Bulgaria 2Elbo (*) x Germany

1Phytobenthos Index (*) x Estonia National MP Exclame (*) x France 4

pain Valencia- conservation status MP

Intertidal seagrass (*) x Ireland Leaf area - - -

Regional MP Leaf necrosis -

Regional MP

-

8 x Italy Liguria- Regional MP x 1

Flowering intensity 1 x Spain Murcia- conservation status MP x 1

8 x France Corsica- Regional MP x 1

8 x France Corsica- Regional MP x 1- -

Regional MP

8 x France Languedoc Roussillon- x 1

8 x Italy National MP x 1

8 x Italy Liguria, Tuscany, Latium- x 1

? x x

xx x 1 2

Epiphyte biomass 8 x Algeria Algeria-MP xx x 1 2

x

Global seagrass density 6 x S x 2

x x 1 1 18 x Algeria Algeria-MP x 1

8 x Italy National MP x 18 x Italy Liguria, Tuscany, Latium- x 1

8 x Italy National MP x 18 x Italy Liguria, Tuscany, Latium- x 1

Leaf production 8 x Algeria Algeria-MP x 1

8 x Italy National MP x 18 x Italy Liguria, Tuscany, Latium- x 1

Leaf tips lost (Coefficient A) - - -

Regional MP E-MaQI and R-MaQI (*) 3Multispecies maximum depth index (*)

1xxnedewSx01

- - -

Regional MP

8 x Italy National MP x 18 x Italy Liguria, Tuscany, Latium- x 1

x x x x1

No. of leaves per shoot 8 x Algeria Algeria-MP x 1

8 x Italy National MP x 18 x Italy Liguria, Tuscany, Latium- x 1

Plagiotrophic rhizomes 8 x Algeria Algeria-MP x 1

8 x Algeria Algeria-MP x 1

8 x France Corsica- Regional MP x 1

x Italy

8 x France Corsica- Regional MP x 1

270 Hydrobiologia (2013) 704:265–278

123

Table 2 continued

Indicator Reference1 Region Country Monitoring Programme (MP) Seagrass species Category

NE

. Atla

ntic

B

altic

B

lack

Sea

M

edite

rran

ean

P. o

cean

ica

C. n

odos

a Z

. mar

ina

Z. n

olti

i se

agra

sses

D

istr

ibut

ion

Abu

ndan

ce

Shoo

t cha

ract

eris

tics

Proc

esse

s

Che

mic

al c

onst

ituen

ts

Ass

ocia

ted

flor

a &

fau

na

- - - POMI (*) - (*) - (*)

Prei Presence of invasive species

- status MP

8 x Italy National MP x 1

11 x Spain Catalonia MP x 2 3 8 112 x Spain Balearic Islands MP x 2 3 8 1

x Croatia x 2 3 8 1POSWARE (*) x Italy x 1 1 3

13 x France x 2 1 1 1

Rate of density change 14 x Spain Balearic Islands MP x 17 x Spain Balearic Islands- conservation x 1

Rate of shoot mortality 7

8 x France Corsica- Regional MP x 1

8 x Italy Liguria- Regional MP x 1

1 x Spain Murcia- conservation status MP x 1

x Spain Balearic Islands- conservation x 1status MP

status MP

- - -

Regional MP

- - -

Regional MP Seagrass (*)

Shoot burial talonia- conservation status MP

- - - -

Regional MP - - Density lonia- conservation status

MP -

MP

Rate of shoot recruitment 7 x Spain Balearic Islands- conservation x 1

Rhizome elongation 8 x Algeria Algeria-MP x 1

8 x Italy National MP x 18 x Italy Liguria, Tuscany, Latium- x 1

Rhizome production 8 x Algeria Algeria-MP x 1

8 x Italy National MP x 18 x Italy Liguria, Tuscany, Latium- x 1

x x 1 1 1

Shoot biomass 8 x Italy National MP x 15 x Spain Ca x 1

8 x Algeria Algeria-MP x 1

8 x France Languedoc Roussillon- x 1

8 x Italy National MP x 1

5 x Spain Cata x 1

6 x Spain Valencia- conservation status x 1

-

8 x France Corsica- Regional MP x 1

8 x France Corsica- Regional MP x 1

x UK

1 x Spain Murcia- conservation status MP x 1

8 x France Corsica- Regional MP x 1

8 x Italy Liguria- Regional MP x 1

7 x Spain Balearic Islands- conservation x 1status MP

- - - -

Regional MP -

Regional MP - - -

Regional MP SPA ? 1SQI

8 x Algeria Algeria-MP x 1

8 x France Provence Alpes Côte d'Azur - x 1

8 x France Languedoc Roussillon- x 1

8 x Italy National MP x 1

8

1 x Spain Murcia- conservation status MP x 1

8 x France Corsica- Regional MP x 1

8 x Italy Liguria- Regional MP x 1x Italy Liguria, Tuscany, Latium- x 1

x Greecex Portugal x 1 1 1

Hydrobiologia (2013) 704:265–278 271

123

health (11 programmes), assessing coastal quality (28

programmes) or both (3 programmes, Table 2). The

monitoring programmes span across the four Euro-

pean ecoregions, the North East Atlantic, the Baltic,

the Mediterranean and the Black seas, and involve the

four European seagrass species. However, the moni-

toring effort, in terms of number of programmes,

allocated to Z. nolti, Z. marina, and P. oceanica

meadows is six to eightfold greater than that to

C. nodosa (Table 2). The European seagrass monitor-

ing programmes examine a total of 49 indicators of

seagrass health (Table 2), but only 25 of them are

monitored in P. oceanica, 19 in Z. marina, 12 in

Z. noltii, and 3 in C. nodosa (Table 2).

Metrics included in seagrass indicators

The seagrass indicators identified included a total of

51 metrics representing a wide range of structural and

functional aspects of seagrass ecosystems, which we

grouped in six different categories (Table 1). Five

categories relate directly to seagrasses while one

relates to the flora and fauna associated with the

seagrasses. The seagrass categories consider structural

aspects ranging from large-scale distribution patterns

in entire coastal areas and smaller scale abundance

patterns in individual seagrass meadows to character-

istics of individual shoots, as well as process and rates

of change at shoot or meadow scale and plant chemical

constituents. The category representing the associated

flora and fauna characterizes diversity aspects based

on species or functional groups (e.g., tolerant versus

sensitive species, the presence of epiphytes) as well as

distribution and abundance patterns of species asso-

ciated with the seagrasses (e.g., depth limits of other

angiosperms or macroalgae).

The 49 seagrass indicators of the various Euro-

pean monitoring programmes include from 1 to 14

metrics each. Seagrass indicators based on just one

metric are by far the most common, accounting for

61% of the indicators in use (Fig. 1). These only

describe a limited aspect of the seagrass ecosystem,

but seagrass monitoring programmes often quantify

several indicators together and thereby provide a

more complete description of the ecosystem. The

multi-metric indicators (indices), on the other hand,

cover up to four metric categories each and thereby

synthesize several aspects of the ecosystem in one

estimate (Table 2).

The top-three seagrass metrics mostly used in

Europe, as evaluated based on the number of moni-

toring programmes using them are shoot density

(included in 24 programmes) and cover (included in

18 programmes) both belonging to the category

‘‘abundance’’, and depth limit (included in 16 pro-

grammes) belonging to the category ‘‘distribution’’

(Fig. 2). In addition, the metric ‘‘Change in density’’,

which is included in 2 programmes also relies on

measurements of shoot density.

The most monitored seagrass category is ‘‘Abun-

dance’’ (included in 47 programmes) closely fol-

lowed by ‘‘Distribution’’ and ‘‘Shoot characteristics’’

(included in 33 and 34 programmes, respectively),

while ‘‘Processes’’ and ‘‘Chemical constituents’’ are

slightly less frequently monitored (included in 29 and

Table 2 continued

a (1) Ruiz-Fernandez et al., 2009; (2) Krause-Jensen et al., 2001a; (3) http://www.naturstyrelsen.dk/Naturbeskyttelse/

National_naturbeskyttelse/Overvaagning_af_vand_og_natur/NOVANA/; (4) Krause-Jensen et al., 2001b; (5) Sanchez-Rosas &

Olivella-Prats, 2009; (6) Codina-Soler et al., 2009; (7) Alvarez et al., 2009; (8) Lopez y Royo et al., 2010; (9) Orfanidis et al., 2009;

(10) Swedish Environmental Protection Agency, 2008; (11) Romero et al., 2007; (12) Baron et al. 2007; (13) Gobert et al., 2009; (14)

Marba et al., 2005b Since 2004 the monitoring programme has been reduced to only include area surveys in one area (the Wadden Sea) and not to

include associated measurements of biomass and shoot density any longer

0

10

20

30

1 2 3 4 5 6 7 8 9 10 11 12 13 14

No.

of i

ndic

ator

s

No. of metrics in indicator

Fig. 1 Number of seagrass indicators containing a given

number of metrics

272 Hydrobiologia (2013) 704:265–278

123

30 programmes, respectively) (Fig. 2). The associated

flora and fauna is also a very commonly monitored

category (included in 45 programmes) (Fig. 2). While

the categories ‘‘Distribution’’ and ‘‘Abundance’’ are

among the most monitored categories and also include

the top-three metrics, the remaining categories

0

10

20

30N

o. o

f p

rog

ram

s

Distribution33 programs

0

10

20

30

No

. of

pro

gra

ms

Processes29 programs

0

10

20

30

No

. of

pro

gra

ms

Abundance47 programs

0

10

20

30

No

. of

pro

gra

ms

Chemical constituents30 programs

0

10

20

30

No

. of

pro

gra

ms

Shoot characteristics34 programs

0

10

20

30

No

. of

pro

gra

ms

Associated flora and fauna45 programs

Fig. 2 Number of seagrass monitoring programmes which

monitors metrics within each of the categories ‘‘Distribution’’,

‘‘Abundance’’, ‘‘Shoot characteristics’’, ‘‘Processes’’, ‘‘Chemical

constituents’’, and ‘‘Associated flora and fauna’’. Each metric is

counted for each time a different programme includes it

Hydrobiologia (2013) 704:265–278 273

123

encompass multiple metrics, each of which is only

infrequently (\10 times) included in monitoring

programmes.

Seagrass metrics across regions

The diversity of seagrass metrics in use is high within

as well as between regions (Fig. 3). ‘‘Associated flora

and fauna’’ is the only category spanning across all

regions. The metric categories ‘‘Distribution’’ and

‘‘Abundance’’ are represented in all regions except the

Black Sea and are thereby the most ubiquitous of the

categories relating directly to seagrasses. By contrast

the seagrass categories ‘‘Shoot characteristics’’, ‘‘Pro-

cesses’’, and ‘‘chemical constituents’’ are only used in

the Mediterranean Sea, where they make part of

several P. oceanica and C. nodosa indicators.

In fact, monitoring programmes in the Mediterra-

nean include by far the largest diversity in seagrass

indicators and is the only region where the full range of

metric categories is assessed. Seagrass monitoring

programmes of the North East Atlantic region and the

Baltic Sea encompass three metric categories, while

those of the Black Sea encompass just one category

(Fig. 3).

Discussion

Our compilation demonstrates that European coun-

tries allocate substantial effort to monitor the

seagrass meadows fringing their coasts. The imple-

mentation of the European WFD since year 2000

has been a key driver increasing seagrass monitoring

effort in Europe, since most (66%) programmes

have been initiated in order to comply with WFD

(Table 2). The substantial effort invested in moni-

toring coastal ecological status through seagrass

health reflects both the high intrinsic conservation

value of seagrasses and their role as ‘‘miner’s

canaries’’ of coastal ecological quality.

European seagrass monitoring programmes apply a

wide diversity of indicators. The 42 monitoring

programmes compiled here include a total of 49

seagrass indicators based on a total of 51 seagrass

metrics used either alone or in various combinations of

up to 14 metrics per indicator. The actual diversity of

metrics is even larger since we grouped metrics with

commonalities and many metrics represent specific

water depths that may differ among areas and mon-

itoring programmes. The metrics in use span across six

broad categories covering various seagrass organiza-

tional levels and spatial scales ranging from square

centimeters to hectares. The set of seagrass indicators

quantified by the individual programmes varies within

and across regions. Similarly, the inclusion of seagrass

indicators from different categories in European

programmes is not restricted to programmes monitor-

ing seagrass health but also observed in many of them

aiming to comply with the European Water Frame-

work Directive (WFD), despite the WFD only requests

to define the ecological status of the water body

according with the presence and abundance of seag-

rasses and related disturbance-sensitive species.

The variability in the selection of seagrass metrics

between regions is to some extent due to the uneven

distribution along European coasts of seagrass flora

and, hence, to the differences in dynamics and

longevity of the species. Thus, the fact that the

endemic slow-growing and long-lived P. oceanica is

the dominant seagrass species in the Mediterranean,

whereas the faster growing and shorter-lived Z. noltii

and Z. marina are the dominant species growing in the

rest of European coasts, may be a major reason for the

particularly marked difference in seagrass metrics

applied in the Mediterranean when compared with

0

10

20

30

40

50

60

No.

of

met

rics

mon

itore

d

NEA

BALTIC

BLACK

MED

Fig. 3 Number of metrics monitored by seagrass monitoring

programmes in different regions: the NE Atlantic Sea (NEA),

the Baltic Sea (BALTIC), the Black Sea (BLACK), and the

Mediterranean Sea (MED). Metrics are grouped by category and

counted for each time a different programme includes it. Three

metrics are counted twice, since they are included in monitoring

programmes in the Baltic Sea as well as in the NE Atlantic Sea

274 Hydrobiologia (2013) 704:265–278

123

those in other European programmes. The slow

dynamics of P. oceanica implies that classic indicators

such as shoot density, biomass, or coverage may not be

sensitive enough, because of inherent patchiness, to

reliably infer whether the meadows show only slight

signs of disturbance as required by the WFD and

seagrass conservation programmes. Once a decline in

these parameters is sufficiently large to be detected in

P. oceanica meadows, there is a considerable risk that

the seagrass meadow has already undergone serious

damage that may not be reversible within reasonable

time scales (e.g., Marba et al., 2005). In assessments of

the status of P. oceanica meadows, the classic

abundance indicators are therefore often supple-

mented with additional metrics belonging to other

categories such as ‘‘Processes’’, ‘‘Chemical constitu-

ents’’, and ‘‘Shoot characteristics’’ which may respond

faster to disturbance and thereby can be early warning

indicators for seagrass deterioration. Indeed, metrics

from these three additional categories are regularly

measured only in Mediterranean monitoring pro-

grammes (Fig. 3; Table 2). Similarly, Giovannetti

et al. (2010) have proposed to use the epiphyte

community on P. oceanica leaves as early warning

indicators of deterioration of water quality in Medi-

terranean monitoring programmes.

The use of different metrics within and across

regions can also be attributable to different hydro-

graphic and habitat conditions such as water transpar-

ency, substratum type, salinity and tidal range, which

lead to the development different communities of

benthic flora. The Baltic, the NE Atlantic and the

Black seas, for example, often support mixed com-

munities of seagrasses and macroalgae in shallow

areas where hard substrate is scattered on the sandy sea

floor, and the large tidal range of the NE Atlantic

further supports intertidal in addition to subtidal

vegetation. The diversity of angiosperms is also

stimulated in the low saline areas of the Baltic Sea

where brackish water plants of the genera Ruppia,

Zannichellia and Potamogeton as well as Characeans

often mix with populations of Zostera. Such mixed

communities of angiosperms and macroalgae is in

contrast with the dominance of monospecific seagrass

meadows including a minor representation of macro-

algae in the marine flora of the Mediterranean.

Differences in habitat characteristics and vegetation

communities may, therefore, partially explain why the

Mediterranean has relatively fewer indicators (12%)

of the category ‘‘Associated flora and fauna’’ com-

pared to the Baltic Sea (48%), the NE Atlantic Sea

(33%), and the Black Sea (100%).

The use of different seagrass indicators within as

well as between regions also reflects scientific tradi-

tions and local knowledge, so that the choice of

indicator in a given country is connected with the

accumulated knowledge and available time series of

seagrass data. This component of the diversity of

seagrass indicators applied in European monitoring

programmes is, of course, to some extent connected

with the reasons discussed above. However, within

regions having similar seagrass species, habitat con-

ditions and benthic flora communities the tradition

component may be particularly important in explain-

ing differences in the choice of seagrass indicators.

Within European marine eco-regions this component

may act as a barrier to adopt common monitoring

methods and metrics. The scientific tradition compo-

nent should be strongest in countries and regions with

multiple institutions involved in seagrass research. In

contrast, areas with fewer and newer seagrass research

institutions and/or a more central organization of the

monitoring effort should carry less historical weight

and should be more flexible in the choice of metrics.

The numerous and long-living seagrass research

institutions in the Mediterranean countries in combi-

nation with a local organization of the monitoring

effort may help explain the high diversity of seagrass

indicators when compared with the Baltic Sea, the NE

Atlantic, and the Black Sea (Table 2), where the

diversity in seagrass research institutions is smaller

and monitoring efforts probably tend to be more

centrally organized. In addition, many countries

around the Baltic Sea and in the NE Atlantic region

only recently initiated a monitoring effort on seag-

rasses, and indicators are being developed through

communication with neighboring countries (e.g.,

Denmark) having a longer tradition in seagrass

research.

The large diversity in seagrass indicators applied

within and between regions complicates and reduces

the possibility to provide large-scale overviews of the

status of European seagrass meadows since a common

metric is lacking. The WFD, however, demands that

evaluation of ecological status based on biological

quality elements such as seagrasses and other benthic

flora must be comparable within given types of water

bodies and much effort has accordingly been allocated

Hydrobiologia (2013) 704:265–278 275

123

to the intercalibration of the various seagrass indica-

tors within regions (Lopez y Royo et al., 2011). This

study has been and still is being conducted through

geographical intercalibration groups (GIGs, i.e.,

within regions) of the WFD though with variable

success due to limited overlap of applied indicators

between areas.

If the diversity in seagrass indicators used across

European monitoring programs is justifiable and

scientifically sound, the differences within eco-

regions may not be always the case, and there is

potential to reduce the diversity of metrics into

common standards. This standardization of monitor-

ing metrics should follow the principle of parsimony,

and follow from the critical evaluation and test of the

strengths and limitations of the range of available

indicators. This evaluation can be conducted by (1)

testing the strength of the individual indicators with

respect to their sensitivity to reflect the responses to

pressures, (2) analyzing the robustness of the indicator

to uncertainty due to sampling, within-site variability,

interannual variability, etc., connected with the mea-

surement and with the associated evaluation of

ecological status, and (3) considering whether the

sampling is destructive or not. Such an evaluation

would form a sound basis for selecting the best set of

indicators for a given region to achieve the goals of the

monitoring programme. Intercalibration exercises

being conducted within European eco-regions, the

need to examine indicator–pressure–response rela-

tionships in order to comply with European WFD as

well the growing efforts aiming at quantifying the

uncertainty associated to the indicators (Bennet et al.,

2011; Balsby et al., 2012; Mascaro et al., 2012a, b) are

certainly contributing towards the standardization of

monitoring metrics.

Documentation of the pressure–response relation-

ships for the various seagrass indicators is limited and

largely based on spatial relationships (e.g., Krause-

Jensen et al. 2008) rather than temporal relationships

describing the response of indicators to a change in the

pressure over time (but see Borja et al., 2010).

Responses to pressures over time may differ consid-

erably from responses along spatial gradients in

pressures. The pathways of responses to an increase

in pressure such as eutrophication may also differ from

those of a release of pressure, such as oligotrophica-

tion, because alternative stable states, hysteresis

effects, and/or changing baselines may play important

roles (Scheffer & Carpenter, 2003; Duarte et al., 2009;

Carstensen et al., 2011). The uncertainty connected

with a given indicator also provides important infor-

mation on the probability that the indicator be

sensitive to a change in pressure, but this type of

information is also very limited at present.

In conclusion, the compilation of indicators of

seagrass health provided here demonstrates a large

variability in seagrass indicators within and across

European ecoregions. This variability reflects the

broad interest for documenting the status of these

valuable ecosystems and highlights the potential for

using seagrasses as indicators of ecological status in

the European coastal zone. However, the large diver-

sity of indicators applied and their limited overlap

across regions limits the possibility to provide pan-

European overviews of the status of seagrass ecosys-

tems. The diversity of indicators can be partially

justified by differences in species and associated time

scales of responses as well as by differences in habitat

conditions and associated community types but also

seems to be determined by scientific traditions. We

encourage an evaluation of the performance of

seagrass indicators on the basis of their responses to

pressures in space and, particularly, time and their

associated uncertainty in order to identify the most

suitable indicators that should conform the standards

of monitoring for specific coastal European eco-

regions.

Acknowledgments This study was funded by the European

project WISER (Water bodies in Europe: Integrative Systems to

assess Ecological status and Recovery; funded under the 7th EU

Framework Programmeme, Theme 6 (Environment including

Climate Change), Contract No.: 226273), and the COST Action

(Seagrass productivity: from genes to ecosystem management;

COST Action ES0906). We thank an anonymous reviewer and

L.R. Carvalho for useful comments on the ms.

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