Ecological quality assessment of transitional waters based on fish assemblages in Portuguese...

Please cite this article in press as: Cabral, H.N., et al., Ecological quality assessment of transitional waters based on fish assemblages in

Portuguese estuaries: The Estuarine Fish Assessment Index (EFAI). Ecol. Indicat. (2011), doi:10.1016/j.ecolind.2011.08.005

ARTICLE IN PRESSG ModelECOIND-952; No. of Pages 10

Ecological Indicators xxx (2011) xxx–xxx

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Ecological Indicators

jo ur nal homep age: www.elsev ier .com/ locate /eco l ind

Ecological quality assessment of transitional waters based on fish assemblages in

Portuguese estuaries: The Estuarine Fish Assessment Index (EFAI)

H.N. Cabrala,∗, V.F. Fonsecaa, R. Gamitoa, C.I. Gonc alvesa, J.L. Costaa, K. Erzinib, J. Gonc alvesb,J. Martinsb, L. Leiteb, J.P. Andradeb, S. Ramosc, A. Bordaloc,d, E. Amorimc, J.M. Netoe, J.C. Marquese,J.E. Rebelo f, C. Silva f, N. Castroa, P.R. Almeidag, I. Domingosa, L.S. Gordoa, M.J. Costaa

a Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugalb Universidade do Algarve, Centro de Ciências Marinhas, CCMAR, P-8005139 Faro, Portugalc Centro Interdisciplinar Investigac ão Marinha & Ambiental C, P-4050123 Oporto, Portugald Univ Porto, Institute Biomedical Science, Lab. Hydrobiology, P-4099003 Oporto, Portugale Institute of Marine Research, Faculty of Sciences and Technology, University of Coimbra, 3004-517 Coimbra, Portugalf Universidade de Aveiro, Departamento de Biologia, P-3800 Aveiro, Portugalg Universidade de Évora, Departamento de Biologia, P-7004516 Evora, Portugal

a r t i c l e i n f o

Keywords:

Water ecological quality

Fish assemblages

Multi-metric indices

Estuaries

Transitional waters

Water Framework Directive

Fish-based indices

a b s t r a c t

The assessment of water quality has changed markedly worldwide over the last years, especially in Europe

due to the implementation of the Water Framework Directive. Fish was considered a key-element in this

context and several fish-based multi-metric indices have been proposed. In this study, we propose a multi-

metric index, the Estuarine Fish Assessment Index (EFAI), developed for Portuguese estuaries, designed

for the overall assessment of transitional waters, which could also be applied at the water body level

within an estuary. The EFAI integrates seven metrics: species richness, percentage of marine migrants,

number of species and abundance of estuarine resident species, number of species and abundance of

piscivorous species, status of diadromous species, status of introduced species and status of disturbance

sensitive species. Fish sampling surveys were conducted in 2006, 2009 and 2010, using beam trawl,

in 13 estuarine systems along the Portuguese coast. Most of the metrics presented a high variability

among the transitional systems surveyed. According to the EFAI values, Portuguese estuaries presented

a “Good” water quality status (except the Douro in a particular year). The assessments in different years

were generally concordant, with a few exceptions. The relationship between the EFAI and the Anthro-

pogenic Pressure Index (API) was not significant, but a negative and significant correlation was registered

between the EFAI and the expert judgement pressure index, at both estuary and water body level. The

ordination analysis performed to evaluate similarities among North-East Atlantic Geographical Intercal-

ibration Group (NEAGIG) fish-based indices put in evidence four main groups: the French index, since it

is substantially different from all the other indices (uses only four metrics based on densities); indices

from Ireland, United Kingdom and Spain (Astúrias and Cantábria); the Dutch and German indices; and

the indices of Belgium, Portugal and Spain (Basque country). The need for detailed studies, including

comparative approaches, on several aspects of these assessment tools, especially in what regards their

response to anthropogenic pressures was stressed.

© 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Water quality assessment includes not only physical and chem-

ical parameters, but also biological elements. A wide variety of

bioindicators have been used, mainly to ensure that water qual-

ity assessment includes components that affect human health, as

∗ Corresponding author. Tel.: +351 217500826; fax: +351 217500207.

E-mail address: [email protected] (H.N. Cabral).

well as goods and services provided by aquatic systems to mankind

(e.g. Deegan et al., 1997; Borja et al., 2008).

In response to the increasing degradation of aquatic systems

observed worldwide (Costanza et al., 1998; Beaumont et al., 2007;

Halpern et al., 2007), several programmes have been developed

and implemented at the international, national and regional lev-

els, providing a framework for the protection and/or restoration of

aquatic systems and ensuring that human activities are carried out

in a sustainable manner. Several examples are the Oceans Policy in

Australia, the Oceans Act and the Clean Water Act in Canada and in

the USA, the Water Framework Directive (WFD) and the European

1470-160X/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecolind.2011.08.005




2 H.N. Cabral et al. / Ecological Indicators xxx (2011) xxx–xxx

Fig. 1. Estuarine systems sampled along the Portuguese coast.

Marine Strategy Directive in Europe, the National Water Act in

South Africa, among others (see Borja et al., 2008, for a review).

In Europe, the WFD (Directive 2000/60/EC) sets the main goal

of achieving a good ecological status in all European water bod-

ies by 2015, including freshwater, transitional waters (estuaries)

and coastal waters. According to this Directive, member states

should assess water quality based on several physical and chemical

variables, but also using some biological key-elements, i.e. phy-

toplankton, macrophytes and phytobenthos, benthic invertebrates

and fish (Borja, 2005).

Although the use of fish as indicators of water quality is not

particularly recent, the development of fish-based multi-metric

indices has only occurred in the last 2 or 3 decades (Karr, 1981;

Breine et al., 2010). The value of fish fauna as a biological qual-

ity element relies on key aspects of their biology and ecology,

namely their wide dispersion in the aquatic environments, diver-

sity of functional guilds, their major ecological role in food webs,

their relatively long life-span which accounts for long-term effects,

and their value for mankind, particularly as a food resource (e.g.

Whitfield and Elliott, 2002; Van Der Oost et al., 2003; Harrison

and Whitfield, 2004). Nevertheless, some disadvantages of using

fish as indicators should also be considered, in particular their

high mobility, their high tolerance to contaminants and physi-

cal degradation of habitats, the selective nature of the sampling

gears required and the need for large sampling efforts. Also, fish

are subject to strong resource exploitation regimes and represent

generally higher trophic levels (e.g. Whitfield and Elliott, 2002;

Harrison and Whitfield, 2004). However, most of these disadvan-

tages, which can also be recognised for other taxonomic groups,

namely benthic invertebrates (e.g. Karr et al., 1986; Whitfield and

Elliott, 2002), are out-weighed by the advantages (Harrison and

Whitfield, 2004).

Several estuarine fish based-indices have been developed over

the last two decades (Ramm, 1988; Cooper et al., 1994; Deegan

et al., 1997; Quinn et al., 1999; Paul, 2003; Borja et al., 2004;

Harrison and Whitfield, 2004; Breine et al., 2007, 2010; Coates




H.N. Cabral et al. / Ecological Indicators xxx (2011) xxx–xxx 3

Table 1Main geomorphologic and hydrologic characteristics of the estuarine systems surveyed along the Portuguese coast.

Estuaries Total area

(km2)

River flow

(m3 s−1)

Mean

depth (m)

Residence

time (days)

Entrance

width (m)

Intertidal

area (%)

Latitude Number of

water bodies

Minho 24.5 300 3 2 1246 9 41◦52′39.32′′N 5

Lima 11.3 62 2 1–7 647 <1 41◦41′38.82′′N 3

Cávado 4.3 66 2 <2 87 <1 41◦30′44.72′′N 2

Ave 1.7 32 4 <2 283 <1 41◦20′48.32′′N 1

Douro 7.3 450 4 2 219 11 41◦08′21.08′′N 3

Vouga 120.8 40 2 17 437 64.0 40◦40′11.72′′N 5

Mondego 8.6 79 2 3 264 64 40◦06′56.12′′N 4

Lis 0.4 8 1 <1 41 <10 39◦52′53.84′′N 1

Tejo 367.5 300 5 25 4909 40 38◦52′44.62′′N 4

Sado 212.4 40 6 30 1740 44 38◦24′33.54′′N 6

Mira 4.7 3 4 15 519 42 37◦42′22.45′′N 3

Arade 8.7 50 6 1 220 25 37◦09′23.55′′N 2

Guadiana 37.5 80 3 12 1720 24 37◦16′30.67′′N 4

et al., 2007; Delpech et al., 2010) and some have been applied in

the assessment and monitoring programmes of the WFD. Most

of European Union (EU) member-states deal with several prob-

lems regarding these assessments, especially those related with

the selection of metrics for the indices, the estimation of ecolog-

ical quality ratios (based on reference conditions), the setting of

boundaries between the different ecological quality status, and also

the interpretation of ecological quality ratios and their relationship

with different types and magnitudes of human pressure. Another

major challenge is the intercalibration process, which aims to stan-

dardize the ecological quality status results obtained with different

indices and using different sampling methodologies for common

estuarine systems. Due to the strict agenda for respecting mile-

stones imposed by the implementation of WFD, research on these

methodological aspects has been scarce. Although some contribu-

tions have been published recently (e.g. Uriarte and Borja, 2009;

Delpech et al., 2010) it is expected that more studies address these

aspects and that assessment tools may suffer some changes in the

future.

The WFD establishes guidelines for the use of biological ele-

ments in the assessment of ecological water quality. In the case

of fish fauna, assessment tools should include taxonomic com-

position, abundance, disturbance sensitive species and indicator

species, but the ambiguity of these guidelines led to the develop-

ment of a wide diversity of indices.

In this paper, we propose an index developed for Portuguese

estuaries, designed for the overall assessment of transitional waters

and with the possibility of also being used at the level of water bod-

ies within an estuary, as required by the WFD. A comparison with

other indices proposed by several European member-states was

established, highlighting the difficulties inherent to the intercali-

bration process.

2. Materials and methods

2.1. Fish sampling surveys

Fish was sampled in 13 estuaries along the Portuguese coast

(Fig. 1 and Table 1), following a sampling protocol established for

the implementation of the WFD. This protocol has several require-

ments proposed by the national water agency (INAG), concerning

its simplicity and low cost, but was based on the analysis of pre-

vious data available for the majority of Portuguese estuaries. In

this previous work, the effect of sampling size (number of hauls) in

the metrics was analysed and boundaries of water quality classes,

defined later, had the sampling effort into account. Estuaries were

divided in water bodies (varying from 1 to 6 per estuary). In each

water body, 3–5 hauls (according to water body area; 3 hauls were

performed only in very small water bodies, where trawled area was

almost overlaped among hauls) were performed during the night at

ebb tide, using a 2 m beam-trawl with a tickler chain and a stretched

mesh size of 5 mm at the cod end. Most of Portuguese estuaries

present a high water transparency, especially in lower areas, and

thus the night period allowed to reduce fish avoidance to the net by

visual recognition (differences between day and night hauls were

analysed in previous surveys and results taking into account for

the selection of the best sampling period). Hauls were performed

at a constant speed for a distance of ca. 300 m, monitored by a GPS.

Table 2Most relevant anthropogenic sources of pressure considered in the present study and their effects on different types of metric.

Pressures

Degradation of water

and sediment quality

Loss of

habitat

Selective

mortality

Physical

barriers

Changes in

river flow

Biological

pollution

Sources Population X X X

Port activity X X

Aquaculture X X X

Agriculture X

Industry X X

Dredging X X

Fisheries X X

Dams X X

Effects on type of metrics Species richness X

Ecological guilds X X X X

Feeding guilds X X X

Introduced species X

Diadromous species X X X X

Disturbance sensitive species X X X X





Samples were collected in Spring, in 2006, 2009 and 2010. This

season was selected since it is the period when a higher species rich-

ness and fish abundance was documented in Portuguese estuaries

and that allows to evaluate several functional aspects, including the

nursery function of estuaries. All fish caught were identified and

counted. Fish species were assigned to ecological guilds reflecting

habitat use and feeding habits, according to Franco et al. (2008).

2.2. Index development

The Estuarine Fish Assessment Index (EFAI) was developed fol-

lowing the steps proposed by Borja and Dauer (2008), i.e. (1) scope

of the index application, (2) analysis of candidate metrics, (3) selec-

tion of metrics, (4) metric combination and index formulation, and

(5) index validation. The most important human pressures in estu-

aries and the guidelines pointed out in the WFD (the assessment

of ecological water quality based on fish, to be compliant to the

WFD, should integrate species composition, abundance, sensitive

and indicator species) were considered. Table 2 includes the most

relevant anthropogenic pressures considered, their effects and the

expected response by type of metric.

Several candidate metrics were selected based on empirical

knowledge and literature, and also considering the metrics in

homologous multi-metric indices used in the context of the WFD

(Table 3). A correlation analysis was performed in order to point

out metrics that were strongly correlated. Whenever those metrics

were of the same type (sensu metrics categories listed in Table 2),

only one of them was kept in the multi-metric index in order to

avoid redundancy.

The EFAI included metrics revealing fish community structure

and function (trophic structure and habitat use patterns), as well

as using key-species to evaluate specific impacts of anthropogenic

activities. The ecological guilds used to characterize trophic struc-

ture and habitat use patterns were adapted from Franco et al.

(2008).

The metrics included in the EFAI were the following:

Species richness (SR) – total number of fish species. Species

richness is usually strongly correlated with habitat diversity

and complexity and should be sensitive to habitat loss and/or

degradation. Species richness may vary markedly with latitude,

which is the case along the Portuguese coast, due to its par-

ticular bio-geographic location (between two bio-geographical

provinces: the cold-temperate and warm-temperate). However,

the species that are restricted to one particular area of the

coast (North or South) are substituted by others on the other

edge (e.g. Cabral et al., 2001).

Percentage of marine migrants (% MM) – one of the most impor-

tant functions of estuaries is the role of nursery area for fish. This

Table 3Candidate metrics for the EFAI multi-metric index with indication of the countries

that include similar metrics in homologous indices (IE – Ireland (Coates et al., 2007);

UK – United Kingdom (Coates et al., 2007); ES – Spain (Borja et al., 2004); BE –

Belgium (Breine et al., 2010); FR – France (Delpech et al., 2010); NL – Netherlands

(Jager and Scholle, personal communication; Delpech et al., 2010); DE – Germany

(Jager and Scholle, personal communication; Delpech et al., 2010).

Candidate metrics EU countries that include a similar

metric in their multi-metric indices

Total number of taxa (species

richness)

IE, UK, ES, BE

Number of species that make

up 90% of abundance

IE, UK, ES

Number of estuarine resident

species

IE, UK, ES, BE FR, NL

Percentage of marine juvenile

migrant individuals

IE, UK, ES, FR, NL

Total number of piscivorous

species

IE, UK, ES, FR, BE

Percentage of piscivorous

individuals

IE, UK, ES, FR, BE

Number of diadromous species ES, FR, BE, NL

Percentage of diadromous

individuals

FR, BE, DE, NL

Feeding guilds IE, UK, ES

Percentage of benthic

individuals

ES, FR, BE

Fish health ES

Disturbance sensitive taxa DE, IE, ES, NL

Introduced species ES

metric evaluates the number of individuals of species which use

estuaries as nursery areas, expressing it as a percentage of the total

number of individuals caught. In Portuguese estuaries, the individ-

uals of these species are mainly juveniles (Cabral et al., 2007), so

this metric reflects the nursery function of the transitional waters

considered.

Estuarine species (ES) – this metric is a combination of two sub-

metrics, one that evaluates the percentage of individuals belonging

to this functional guild (Franco et al., 2008) and the other the

number of species. The scoring of this metric results from the com-

bination of the two metrics. A low species number evidences a poor

ecological quality, as well as extremely low or high percentages of

individuals of this guild.

Piscivorous species (P) – this metric is also a combination of

two metrics, similarly to the previous metric. It also includes the

species classified by Franco et al. (2008) as HP and OV, thus, the

percentage of individuals and the number of species that feed on

fish (non-strictly piscivorous) are estimated. This metric evaluates

the complexity of estuarine food webs structure, particularly the

presence and abundance of higher trophic levels.

Table 4Metrics included in the EFAI and their respective scoring system, for the assessment of ecological quality in transitional systems.

Metrics Scores

1 3 5

Species richness (SR) ≤10 11–20 >20

Percentage of marine migrants (%MM) ≤10% 10–50% >50%

Estuarine resident species (ES)

Percentage of individuals ≤10% or >90% 10–30% or 70–90% 30–70%

Number of species ≤2 3–5 >5

Piscivorous species (P)

Percentage of individuals ≤10% or >90% 10–30% or 70–90% 30–70%

Number of species ≤5 6–12 >12

Diadromous species (D) Absent or few species

present/Inability to

complete life cycle

Several species present but rare Several species present

and common

Introduced species (I) Present and abundant Present but rare Absent

Disturbance sensitive species (S) Absent or few species

present in low abundance

Several species present but rare Several species present

and common





Tab

le

5E

FA

I

sco

rin

g

syst

em

for

its

ap

pli

cati

on

at

the

wate

r

bo

dy

(WB

)

lev

el

for

(O)

oli

go

hali

ne, (

M)

meso

hali

ne

an

d

(P)

po

lyh

ali

ne

wate

r

bo

die

s.

Metr

ics

O

M

P

1

3

5

1

3

5

1

3

5

Sp

eci

es

rich

ness

(to

tal

nu

mb

er

of

speci

es)

≤3

4–

8

>8

≤4

5–

10

>1

0

≤5

6–

15

>1

5

Perc

en

tag

e

of

mari

ne

mig

ran

ts

≤10

%

10

–5

0%

>5

0%

≤10

%

10

–5

0%

>5

0%

≤10

%

10

–5

0%

>5

0%

Est

uari

ne

speci

es

Per

cen

tage

of

ind

ivid

uals

≤10

%

or

>9

0%

10

–3

0%

or

70

–9

0%

30

–7

0%

≤10

%

or

>9

0%

10

–3

0%

or

70

–9

0%

30

–7

0%

≤

10

%

or

>9

0%

10

–3

0%

or

70

–9

0%

30

–7

0%

Nu

mb

er

of

spec

ies

≤1

2–

3

>3

≤2

3–

5

>5

Pis

civ

oro

us

speci

es

Per

cen

tage

of

ind

ivid

uals

≤10

%

or

>9

0%

10

–3

0%

or

70

–9

0%

30

–7

0%

≤10

%

or

>9

0%

10

–3

0%

or

70

–9

0%

30

–7

0%

≤10

%

or

>9

0%

10

–3

0%

or

70

–9

0%

30

–7

0%

Nu

mb

er

of

spec

ies

≤1

2

>2

≤1

2–

3

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≤2

3–

5

>5

Dia

dro

mo

us

speci

es

Red

uct

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in

the

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of

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Inab

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in

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te

the

life

cycl

e

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in

the

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red

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Intr

od

uce

d

speci

es

Pre

sen

t

an

d

ab

un

dan

t

Pre

sen

t

bu

t

rare

Ab

sen

t

Pre

sen

t

an

d

ab

un

dan

t

Pre

sen

t

bu

t

rare

Ab

sen

t

Pre

sen

t

an

d

ab

un

dan

t

Pre

sen

t

bu

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Ab

sen

t

Dis

turb

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ve

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ion

Diadromous species (D) – diadromous fish are an important

component of fish assemblages in transitional waters, despite using

this environments for a limited period of time, often only during

their migrations towards upstream (anadromous species) or down-

stream (catadromous species) areas. A reduction in the number

of species or in the abundance of diadromous species should be

related mainly to physical barriers in the river basin area or to river

runoff. Since the occurrence of these species is relatively occasional

or rare in estuarine waters, and given the high dependency of sam-

pling gear on reliable abundance estimates, this metric is assessed

based on expert judgement (enquiries to experts).

Introduced species (I) – this metric evaluates if there are sig-

nificant changes in fish assemblages of transitional waters due to

introduced species. The occurrence and high abundance of alien

species strongly affects the structure of indigenous fish assem-

blages. For the same reason as for metric D, this metric will also

be evaluated based on expert judgement.

Disturbance sensitive species (S) – some species that are char-

acteristic of transitional waters are strongly associated to some

particular habitats or conditions. These species may be good indica-

tors of habitat loss or degradation. Among the resident fish species

that occur in Portuguese estuaries, Syngnathidae are sensitive to

both pressures and have been reducing their abundance in some

estuaries (Cabral et al., 2001). As their distribution is often restricted

to particular areas and the effort of the sampling programme devel-

oped for WFD purposes is probably not sufficient to cover the low

abundance of these species, this metric will also be evaluated based

on expert judgement.

This set of metrics reflect the spirit of the WFD compliance

criteria and have also documented responses to anthropogenic

pressures in estuaries (e.g. Karr, 1981; Whitfield & Elliott, 2002).

2.3. Reference conditions and scoring system

Due to the lack of historical data that could be used to establish

reference conditions, the scoring of the metrics had to be based on

expert knowledge. Theoretical characteristics of fish assemblages

of transitional waters with a high quality status were defined and all

the other quality status were established as deviations from those

conditions. A score of 1, 3 or 5 was assigned to each metric (as sug-

gested by Karr et al., 1986) according to reference values detailed in

Table 4. The scoring system for metrics ER and P was the following:

when both sub-metrics score 1, the final metric score is 1; metric

score 3 is given when one of the sub-metrics scores 1 and the other

scores 3 or 5 or when both sub-metrics score 3; when both metrics

score 5 or when one sub-metric scores 3 and the other scores 5, the

metric score is 5. The EFAI was expressed as the sum of all metrics

scores. Ecological quality ratios (EQR) were determined in order to

assign an ecological quality status to each transitional system, by

dividing the EFAI value obtained for a particular transitional system

by the maximum possible EFAI score (35).

2.4. Application of EFAI to water bodies

According to the WFD, the ecological quality of water bodies

forming a transitional system must also be assessed. To meet this

purpose the EFAI was adapted to be used at the water body level

(EFAIWB). Since water bodies may be profoundly different in both

size and abiotic characteristics, the application of the EFAI implies

the assignment of water bodies to haline zones (based on mean

salinity values as follows: oligohaline, salinity lower than 5; meso-

haline, salinity values between 5 and 18, and polyhaline, salinity

higher than 18). The metrics used in the EFAIWB were similar to

those used in the EFAI, but with different scoring systems. When-

ever a particular metric was not suitable for a particular haline





Table 6Pressures index (Pi) determined as an average value of scores attributed to different estuaries along the Portuguese coast (1 – low; 2 – moderate; 3 – high; see Section 2.5).

Habitat

loss

Industry Ports and

navigation

Dredging Fisheries Agriculture Freshwater

input

Population Pressure

index (Pi)

Minho 1 1 1 2 2 1 2 1.43

Lima 2 2 2 2 2 2.00

Cávado 2 1 2 2 1.75

Ave 2 1 2 2 2 1.80

Douro 3 1 3 2 3 2 3 2 2.38

Vouga 2 3 3 1 2 2 1 2 2.00

Mondego 2 2 2 2 3 1 1 2 1.88

Tejo 2 2 3 3 2 2 1 3 2.25

Sado 1 2 3 2 3 2 1 1 1.88

Mira 1 1 1 1 2 1 1 1.14

Arade 1 2 1 1 1 1 1.17

Guadiana 2 1 2 1 2 2 3 1 1.75

zone, it was removed from EFAIWB calculations. Metrics used in the

EFAIWB and its respective scoring system are presented in Table 5.

2.5. EFAI relationships with anthropogenic pressures

In order to evaluate the EFAI response to anthropogenic pres-

sures, a multi-metric index (API – Anthropogenic Pressure Index)

developed by Vasconcelos et al. (2007) was first calculated for

the estuaries for which specific information on human activities

was available (i.e. Douro, Mondego, Tejo, Sado, Mira, Guadiana;

n = 6). This index considers a wide array of data on different pres-

sure sources, namely population, industry, agriculture, fisheries,

dredging, port activities and dams (see Vasconcelos et al., 2007,

for details).

To further extend the pressure analysis, as to encompass more

systems (n = 12, Lis estuary was excluded from this analysis due

to lack of information) and water bodies (n = 24), another pressure

index (Pi) was determined based on best expert judgement, fol-

lowing Aubry and Elliott (2006) and Borja et al. (2011). Different

pressures, namely habitat loss, industry, agriculture, population,

port activities, dredging, freshwater inputs and fisheries, were clas-

sified as low (1), moderate (2) and high (3), and the Pi resulted from

the average value of the individual pressures scores (Table 6, see

Borja et al., 2011 for further details). Spearman correlations were

calculated between EFAI and EQR values and API and Pi values. A

significance level of 0.05 was considered in these test procedures.

2.6. Comparison of EFAI with other fish-based indices developed

in the context of WFD

A correspondence analysis was performed in order to evalu-

ate similarities between fish-based indices used in the context

of the WFD, in the North-East Atlantic Geographical Intercalibra-

tion Group (NEAGIG). The matrix used in the analysis included all

metrics used by these indices grouped in common typologies (e.g.

metrics relative to estuarine resident species; metrics relative to

indicator species). The values in the matrix were either 0 (absence

of that metric in the index) or 1 (presence of that metric in the

index). The correspondence analysis is a multivariate ordination

technique which allows an evaluation of the main patterns found

in data, especially by representing in the diagram both samples and

variables. This analysis was performed using CANOCO software (ter

Braak and Smilauer, 2002) (Table 7).

3. Results

Most of the metrics presented a high variability among the tran-

sitional systems surveyed (Table 8). Species richness was higher in

the Sado, Guadiana, Arade, Mondego and Tejo estuaries and was

extremely low in small estuaries located in the North coast (Ave,

Cávado and Lis). For those systems where data was available for

more than one year (EQR values, Table 9), the number of species

was relatively constant through the years, except for Mira and Sado

estuaries. The percentage of marine juvenile individuals was also

extremely variable, with the highest values being estimated for

the Ave, Cávado, Douro, Vouga, Mondego and Lis estuaries (val-

ues higher than 60%). For Mira estuary, a high percentage of these

individuals was only registered in 2006. An opposite pattern was

found for the percentage of estuarine resident individuals, which

had its highest values recorded for the Lima, Tejo, Mira (2010)

and Guadiana estuaries. The number of estuarine resident species

ranged from 2 to 6 species for the majority of the estuaries. Only

one species was recorded in the Douro estuary and 7 species were

found in the Arade and the Guadiana estuaries. The number of pis-

civorous species varied between 1 and 12; the numbers registered

in 2006 surveys were higher, and for the majority of the estuar-

ies the number of species feeding on fish was between 3 and 7.

Regarding the relevance of individuals of this trophic guild con-

sidering their abundance (percentage of individuals), the highest

values were obtained for the Ave, Cávado, Douro, Mondego, Lis and

Arade estuaries. For the Mira estuary, a high value was also regis-

tered in 2006. The results for the three metrics evaluated by expert

judgement revealed few differences among estuaries. Regarding

diadromous fish, all estuaries had the score 3, revealing a reduc-

tion of diadromous fish populations, except for the Ave and Douro

to which scored 1, due to the disappearance of some species that

were present in those two estuaries in the past. Considering the

introduced species metric, all transitional systems considered in

the present study obtained the highest score (5), except for the Gua-

diana estuary, where the introduced species Fundulus heteroclitus

has been reported consistently. Finally, the assessment of sensitive

species status by experts resulted in a score of 3 for all systems,

Table 7Boundaries for EFAI values, EQR and ecological quality status (A) applied to estuarine

systems, mesohaline or polihaline water bodies; (B) applied to oligohaline water

bodies.

EFAI EQR Ecological quality

(A)

7–10 0.20 Bad

11–14 0.31 Poor

15–20 0.42 Moderate

21–29 0.60 Good

30–35 0.85 High

(B)

6–8 0.20 Bad

9–12 0.30 Poor

13–17 0.43 Moderate

18–25 0.60 Good

26–30 0.86 High




H.N. Cabral et al. / Ecological Indicators xxx (2011) xxx–xxx 7Ta

ble

8M

etr

ics,

EFA

I

an

d

EFA

I WB

valu

es

for

the

surv

ey

ed

tran

siti

on

al

syst

em

s

alo

ng

the

Po

rtu

gu

ese

coast

in

20

10

,

ex

cep

t

for

the

Do

uro

,

Mo

nd

eg

o,

Av

e

an

d

Cáv

ad

o,

wh

ich

were

sam

ple

d

in

20

09

,

an

d

the

Min

ho

an

d

Vo

ug

a,

wh

ich

were

sam

ple

d

in

20

06

.

Ab

bre

via

tio

ns

use

d

are

:

SR

–

speci

es

rich

ness

;

%

MM

–

perc

en

tag

e

of

mari

ne

mig

ran

ts;

ES

–

est

uari

ne

resi

den

t

speci

es;

%

ind

ivid

.

–

perc

en

tag

e

of

ind

ivid

uals

;

#

speci

es

–

nu

mb

er

of

speci

es;

P

–

pis

civ

oro

us

speci

es;

D

–d

iad

rom

ou

s

speci

es;

I

–in

tro

du

ced

speci

es;

S

–d

istu

rban

ce

sen

siti

ve

speci

es;

G

–g

oo

d

eco

log

ical

statu

s;

an

d

M

–m

od

era

te

eco

log

ical

statu

s.

Metr

ics

Min

ho

Lim

aC

áv

ad

oA

ve

Do

uro

Vo

ug

aM

on

deg

oLis

Tejo

Sad

oM

ira

Ara

de

Gu

ad

ian

a

SR

9

15

5

5

10

12

15

4

16

28

12

22

25

%

MM

23

.18

.16

8.2

76

.78

7.9

68

.36

4.8

66

.72

7.6

57

.52

7.9

35

.2

15

.5

ES

%

ind

ivid

.4

.58

8.0

02

0.0

3.8

19

.3

24

.3

0

69

.5

33

.0

65

.4

58

.9

82

.0

#

spec

ies

35

02

13

30

24

27

5

P %

ind

ivid

.2

7.0

8.8

67

.46

0.0

78

.82

7.0

50

.96

6.7

7.3

11

.63

.2

42

.5

2.6

#

spec

ies

86

31

41

05

24

93

79

DSco

re

3Sco

re

3Sco

re

3Sco

re

1

Sco

re

1

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

ISco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

5Sco

re

3

S

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

Sco

re

3

EFA

I2

1

(0.6

0)

G2

1

(0.6

0)

G2

1

(0.6

0)

G2

1

(0.6

0)

G1

9

(0.5

4)

M2

5

(0.7

1)

G2

5

(0.7

1)

G2

1

(0.6

0)

G2

1

(0.6

0)

G2

9

(0.8

3)

G2

1

(0.6

0)

G2

9

(0.8

3)

G2

3

(0.6

6)

G

EFA

I WB

1

25

(0.7

1)

G2

1

(0.6

0)

G2

1

(0.6

0)

G2

1

(0.6

0)

G2

3

(0.6

6)

G2

5

(0.7

1)

G

17

(0.4

9)

M

23

(0.6

6)

G

23

(0.6

6)

G

21

(0.6

0)

G

19

(0.5

4)

M

29

(0.8

3)

G

23

(0.6

6)

G

EFA

I WB

2

19

(0.5

4)

M2

3

(0.6

6)

G2

1

(0.6

0)

G2

0

(0.6

7)

G2

1

(0.6

0)

G2

5

(0.7

1)

G2

7

(0.7

7)

G2

1

(0.6

0)

G2

1

(0.6

0)

G2

3

(0.6

6)

G2

1

(0.6

0)

G

EFA

I WB

3

20

(0.6

7)

G2

3

(0.6

6)

G2

0

(0.6

7)

G2

3

(0.6

6)

G1

6

(0.5

3)

M

23

(0.6

6)

G

23

(0.6

6)

G

23

(0.6

6)

G

18

(0.6

0)

G

EFA

I WB

4

––

21

(0.6

0)

G2

0

(0.6

7)

G2

5

(0.7

1)

G2

1

(0.6

0)

G

EFA

I WB

5

23

(0.6

6)

G

23

(0.6

6)

G

27

(0.7

7)

G

EFA

I WB

6

23

(0.6

6)

G

Table 9Ecological quality status (Ecological Quality Ratio values between brackets) deter-

mined for Portuguese estuaries based on surveys conducted in 2006, 2009 and

2010.

Estuaries 2006 2009 2010

Minho Good (0.60)

Lima Good (0.60)

Cávado Good (0.60)

Ave Good (0.60)

Douro Good (0.66) Moderate (0.54)

Vouga Good (0.71)

Mondego Good (0.71) Good (0.71)

Lis Good (0.60)

Tejo Good (0.60) Good (0.60)

Sado Good (0.83) Good (0.83)

Mira Good (0.77) Good (0.60)

Arade Good (0.83) Good (0.83)

Guadiana Good (0.66) Good (0.71) Good (0.66)

reflecting a general decrease in the abundance of Syngnathidae

species.

The relationship between the EFAI (EQR values) and the Anthro-

pogenic Pressure Index (API) was not significant (r = −0.39, P > 0.05,

n = 6). The API values were available only for 6 estuaries, limiting

the extent of the analysis. However, significant correlations were

observed between the EFAI (EQR values) and the expert judgement

pressure index (Pi) at both estuary (r = −0.60, P < 0.05, n = 12) and

water body level (r = −0.41, P < 0.05, n = 24). Overall, the anthro-

pogenic pressure gradient was not complete, with only a few values

on the high pressure endpoint (Fig. 2).

The ordination diagram obtained in the correspondence analysis

is shown in Fig. 3. This analysis was performed to evaluate the sim-

ilarities among NEAGIG fish-based indices and accounted for 53%

of the variance in the first two axes. The French index appeared

isolated on the top of the diagram, since it is substantially different

from all the other indices (uses only four metrics based on den-

sities); indices from Ireland, United Kingdom and Spain (Astúrias

and Cantábria) were located on the left side of the diagram, associ-

ated with metrics accounting for the number of species of several

habitat use patterns and trophic guilds; the Dutch and German

indices were set closer (Jager and Scholle, personal communica-

tion; Delpech et al., 2010) in association with metrics relative to

the number of species of certain guilds and also metrics using rel-

ative abundances. Finally, the last cluster grouped the indices of

Belgium (Breine et al., 2010), Portugal and Spain (Basque coun-

try) (Borja et al., 2004) on the right lower area of the ordination

diagram. This group was associated with several metrics based on

relative abundance (percentage of the number of individuals) of

certain functional guilds, as well as metrics relative to sensitive

species, introduced species and fish health (just in the case of the

Basque country index).

4. Discussion

The assessment of water quality has changed markedly world-

wide over the last years. Several legislative documents have

introduced different approaches of assessment, especially by the

inclusion of biological quality elements. Fish have been consid-

ered a key element in most of these documents, as it is the case

of the WFD. As addressed by several authors, using fish as eco-

logical indicators has several advantages in comparison to using

other biological groups, but also some disadvantages (see Whitfield

and Elliott, 2002 and Harrison and Whitfield, 2004 for details).

In the case of transitional waters in the European Union context,

member states have to develop methods to integrate the informa-

tion provided by this biological element. Most countries developed

multi-metric indices that included information on different aspects





Fig. 2. EFAI EQR values of estuarine systems (a, n = 12) and water bodies (b, n = 24) plotted against an anthropogenic pressure index (Pi).

of fish assemblage’s structure and functioning. A major challenge

for these indices was to respond to anthropogenic pressures, while

being robust to the natural variability characteristic of estuarine

systems. This is clearly an extremely difficult task, especially con-

sidering the estuarine-quality paradox, i.e. as estuaries are highly

variable ecosystems exposed to high anthropogenic pressure, it

is difficult to distinguish natural variability from human-induced

stress (Elliott and Quintino, 2007). Therefore, the ultimate goal

for all these assessment methods is to develop tools which are

robust in regarding natural variability, but that at the same time

are capable of identifying and giving alert signs of antropogenic

disturbance.

The EFAI was developed trying to avoid redundant metrics.

Nonetheless, those metrics which were selected for a particular

functional aspect of the fish assemblage to be accounted were

included in the index. The EFAI accounts for the key aspects pointed

out in the guidelines of the WFD, i.e. species composition, abun-

dance, sensitive species and indicator species. The lack of historical

data for the majority of Portuguese estuaries compromised sev-

eral key aspects in the development of an assessment tool, namely

the scoring system and the index validation. Scores and boundaries

of ecological quality ratios and ecological quality status had to be

established by expert judgement and not using reference historical

(pristine) conditions. To define a reference condition in the absence

of pristine sites, authors have developed models (Delpech et al.,

2010), used historical data (Jager and Scholle, personal communi-

cation; Delpech et al., 2010), least-disturbed sites (Harrison and

Whitfield, 2006) or expert judgement (Borja et al., 2004; Harrison

and Whitfield, 2004). The low number of estuaries along the Por-

tuguese coast, and also their high hydrologic and geomorphologic

diversity, do not allow for the development of a validation method-

ology using an appropriate number of replicates. Furthermore,

the lack of detailed information on the levels of pressure in each

transitional system also deeply constrained the study of the EFAI

response to anthropogenic impacts.

Similar constraints resulted in the various indices developed

during WFD implementation, which considered different number

of estuaries (one to thirteen), different methodologies (e.g. beam

trawl, gill nets, stow nets) as well as distinct ways of measur-

ing anthropogenic pressure (development of quantitative pressure

indices; expert judgement) (Coates et al., 2007; Uriarte and Borja,

2009; Breine et al., 2010; Jager and Scholle, personal communica-

tion; Delpech et al., 2010).

Generally, the majority of the metrics exhibited a high variability

both among estuaries and among years (for the transitional systems

where data were available for several years), with the exception of

the metrics evaluated by expert judgement. This variability could

easily be attributed to natural factors, such as the total estuarine

area, depth, river flow, intertidal area, diversity of habitats, among

others.

-0.6 0.6

-0.6

1.0

N spp.

N ES spp.

N diadromous spp.

N MMN MS

N pisc ivorous spp.N benthophagous spp.

N benthic spp.

N 90%N FG

N TG

N individuals

N key spp.% D

% MM

% ES

% pelagic spp.

% benthic spp.

% piscivorous spp.

% Omnivorous spp.

% RG

Introduced spp.

Sensitive spp.

Fish health

BE

GE

FR

IE

NL

PT

SP Basque

SP Astur

UK

Fig. 3. Ordination diagram based on a correspondence analysis of fish-indices met-

rics, grouped in common typologies, developed in the context of the WFD (FR = index

used in France (Delpech et al., 2010); NL = index used in the Netherlands (Jager and

Scholle, personal communication; Delpech et al., 2010.); GE = index used in Germany

(Jager and Scholle, personal communication; Delpech et al., 2010.); IE = index used

in Ireland (Coates et al., 2007); UK = index used in the United Kingdom (Coates

et al., 2007); SP Astur = index used in Asturias/Cantabria (Spain) (Coates et al., 2007);

BE = index used in Belgium (Breine et al., 2010); PT = EFAI; SP Basque = index used

in the Basque country (Spain) (Borja et al., 2004); N benthic spp. = number of ben-

thic species; N diadromous spp. = number of diadromous species; N MS = number of

marine straggler species; % pelagic spp. = percentage of pelagic species; % benthic

spp. = percentage of benthic species; N MM = number of marine migrant species; N

individuals = total number of individuals; N 90% = number of species which make

up 90% of the abundance; N FG = number of functional guilds; N TG = number

of trophic guilds; N benthophagous spp. = number of benthophagous species; N

ES spp. = number of estuarine species; N piscivorous spp. = number of piscivo-

rous species; N spp. = total number of species; Sensitive spp. = sensitive species;

% MM = percentage of marine migrants; % D = percentage of diadromous species;

N key spp. = number of key-species; % RG = percentage of reproductive guilds; %

ES = percentage of estuarine species; % piscivorous spp. = percentage of piscivorous

species; Introduced spp. = introduced species; % Omnivorous spp. = percentage of

omnivorous species.





Although in general the results agreed with those reported

for a large number of estuaries worldwide, in which regards the

dominance of estuarine resident species and marine-estuarine

opportunists (e.g. Maes et al., 1998; Marshall and Elliott, 1998;

Araújo et al., 1999; Thiel and Potter, 2001; Franco et al., 2006;

Martinho et al., 2007), the numerical contribution of these func-

tional guilds were quite variable as outlined by Franc a et al. (2011).

According to Pihl et al. (2002), a high variability in abundance

of species from different ecological guilds should be expected

between estuarine systems, due to their particular hydrologic and

geomorphologic features. Cabral et al. (2007) also evidenced this

high variability in species that use Portuguese estuaries as nursery

grounds.

Many factors and processes have been proposed as responsi-

ble for controlling the structure and composition of estuarine fish

assemblages and these may occur at different scales and in vari-

ous ways. At a large scale, hydrodynamics, geomorphology, climate

and catchment properties of the estuary have been proposed as

the main factors affecting estuarine fish assemblages (Whitfield

and Harrison, 2003; Hillebrand, 2004; Costa et al., 2007; Nicolas

et al., 2010). At smaller scales, fish distribution and abundance have

been demonstrated to result from the responses of individuals to

multiple environmental variables, which can be either dynamic

(e.g., salinity, water temperature, food availability) or fairly sta-

ble (e.g. sediment type, presence of seagrass) (e.g. Marshall and

Elliott, 1998; Araújo et al., 1999; Stoner et al., 2001; Akin et al.,

2005; Barletta et al., 2005; Sosa-Lopez et al., 2007; Vasconcelos

et al., 2010; Franc a et al., 2011). Although a large part of the vari-

ability of the structure of fish assemblages remains to be explained,

Franc a et al. (2011) outlined that patterns of fish assemblage struc-

ture in Portuguese estuarine systems seemed to be influenced

primarily by species-specific responses to dominant environ-

mental gradients. This is clearly a huge difficulty for fish-based

indices to cope with, which may severely constrain their use and

applications.

According to the EFAI, all Portuguese estuaries are in a good eco-

logical status, except for the Douro estuary. Also, when applied at

the water body level (EFAIWB) the results obtained were generally

consistent through the years and with the overall classification of

the transitional system ecological quality status. The large major-

ity of water bodies were considered in good ecological status,

with the exception of three water bodies in the Mondego and the

Mira estuaries. In comparison to the classifications of other Euro-

pean transitional waters in the context of the WFD, it becomes

evident the absence of Portuguese systems on the high-end of

the anthropogenic-pressure gradient, particularly when consid-

ering highly impacted systems such as the Weser (DE) and the

Gironde (FR) estuaries (Jager and Scholle, personal communica-

tion; Delpech et al., 2010). As mentioned above, a major challenge

for these indices is the response to anthropogenic pressures. This

was evident in the lack of correlation between the EFAI and the API

(Anthropogenic Pressure Index, developed by Vasconcelos et al.,

2007), potentially due to the non-specific nature of the pressures

considered, given their quantitative assessment, but most likely

due to the very small number of possible comparisons, limited

by the available pressure information. Hence, the necessity of a

broader comparison scale considering the ecological quality status

obtained with the EFAI and the level of anthropogenic pressure,

led to the best-professional-assessment approach, following Borja

et al. (2011) and Aubry and Elliott (2006). The significant cor-

relations observed with this approach gave an indication of the

relationship between the EFAI and anthropogenic pressures. How-

ever, further work in an international comparison context and tests

of the effects of specific types of pressures in relation to these

multi-metric indices, will greatly benefit the effectiveness of these

tools for monitoring purposes. In the particular case of Portuguese

transitional waters, this intercalibration process will enable the

EFAI calibration including highly impacted systems.

Despite some common metrics which can be identified in sev-

eral fish-based multi-metric indices proposed for the NEAGIG, most

of the assessment tools are substantially different. The multivari-

ate analysis performed in this study revealed different groups of

indices that were mainly clustered according to metrics relative

to species or guild abundance, number of species considering sev-

eral aspects of assemblage structure and occurrence or abundance

of key-species (indicator and/or sensitive species). The efficacy of

these assessment tools is extremely dependent on the sampling

techniques and effort of monitoring plans of each member state.

In fact, recent work has shown that the structure and composi-

tion of fish samples can be affected by the choice of gear type

(Greenwood, 2008) due to different catch efficiencies and area

sampled (Hemingway and Elliott, 2002). There was a high vari-

ability among the hydrologic and geomorphologic features of the

estuarine systems studied in the present work and although beam

trawl has previously been pointed out as one of the most effective

sampling method for estuaries (Hemingway and Elliott, 2002), its

efficiency may vary according to estuaries’ features.

Nevertheless, it is expected that the intercalibration process

which has been taking place between the NEAGIG members will

result in a harmonization between the several fish-based multimet-

ric tools and consequently, in the boundaries of ecological quality

status.

Acknowledgements

We thank all involved in fish sampling and processing. This

study was co-funded by the European Union through the Cohesion

Fund, as well as by the ‘Programa Operacional Temático Valorizac ão

do Território’ (POVT), through the project ‘Avaliac ão do estado

ecológico das massas de água costeiras e de transic ão e do potencial

ecológico das massas de água fortemente modificadas’ (EEMA), the

European Commmission (DG-XII) and the ‘Fundac ão para a Ciência

e a Tecnologia’ (RECONNECT project – PTDC/MAR/64627/2006).

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