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Multi-year comparisons of fish recruitment, growth and production in two

drought-affected Iberian estuaries

Article  in  Marine and Freshwater Research · January 2010

DOI: 10.1071/MF10002

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CSIRO PUBLISHING

www.publish.csiro.au/journals/mfr Marine and Freshwater Research, 2010, 61, 1399–1415

Multi-year comparisons of fish recruitment, growth

and production in two drought-affected Iberian estuaries

Marina DolbethA,C, Filipe MartinhoA, Vânia FreitasB, Sérgia Costa-DiasB,

Joana CamposB and Miguel Ângelo PardalA
A
CEF ] Centre for Functional Ecology, Department of Life Sciences, University of Coimbra,
Apartado 3046, 3001-401 Coimbra, Portugal.
B
CIMAR/CIIMAR ] Centro Interdisciplinar de Investigação Marinha e Ambiental ]
Universidade do Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal.
C
Corresponding author. Email: mdolbeth@ci.uc.pt

Abstract. Climate extremes, such as drought and floods, are increasing and should be considered in ecosystem
management plans. The effects of an extreme drought were studied in two estuaries of the Iberian coast, Minho and
Mondego, by exploring fish recruitment, growth and production over four years. The two estuaries are located within an
area with transitional climate, and differ considerably in size, availability of freshwater wetlands and freshwater inflow.
Fishes from the Minho estuary, at higher latitude, generally had lower growth rates and later timing of recruitment. During
the drought, freshwater inflow was severely reduced in both estuaries. The overall fish assemblage production in the
Minho estuary decreased considerably, whereas in the Mondego estuary it showed an increase. However, the drought
effects seemed highly species-specific and dependent on local geomorphology; the increase in the Mondego estuary
was a result of an increase in a single species, whereas other species decreased or maintained similar production levels.
Decreases in production in both estuaries were attributed to direct and indirect effects of changes in the freshwater inflow
during the study period. This parameter should therefore be considered when undertaking management plans for
transitional waters.

Additional keywords: climate, drought, estuarine fish, geomorphology, hydrology, Iberian Peninsula.

Introduction 2007; Martinho et al. 2009). For instance, several studies

Estuaries support high levels of primary and secondary pro-
duction, as they are nutrient and detritus traps for the abundant
autochthonous and allochthonous material of adjacent areas
(Dolbeth et al. 2007a; Svensson et al. 2007). A plentiful supply
of food resources is available for the estuarine inhabitants,
which, coupled with high availability of habitats and protection,
turns the estuarine ecosystem into a focal point around which
many coastal communities develop and grow (Martı́nez et al.
2007). Consequently, fisheries, agriculture and other industries
prosper in and around the estuarine ecosystem, deriving a large
economic resource from its communities and the ecosystem
itself (Martı́nez et al. 2007; Svensson et al. 2007). Estuaries
provide nursery, refuge, feeding areas and migration routes for
various fish species, besides supporting their own resident fish
assemblage (Elliott et al. 2007). These fishes are directly linked
to higher trophic levels or constitute a significant amount of
biomass exported for coastal recreational and commercial
fisheries (Houde and Rutherford 1993; Cowley and Whitfield
2002).
Estuarine fish populations are highly dynamic owing to
fluctuating levels of recruitment and migration (Costa et al.
2002; Cowley and Whitfield 2002), which may be severely
affected by hydrological parameters and climate (Costa et al.
have showed that altered hydrology patterns, as a result of
floods and drought events, have effects on the fish dynamics
of estuarine ecosystems (Whitfield 2005; Costa et al. 2007)
and on their production levels (Dolbeth et al. 2008a). The
impacts depend on the species affected (Costa et al. 2007)
and on local conditions, such as geomorphology constraints,
among other factors. Changes in hydrodynamics may affect
fish recruitment, growth and production in two ways:
(1) directly, through changes in physico–chemical para-
meters (e.g. salinity, turbidity, oxygen) (Pampoulie et al.
2001); or (2) indirectly, through changes in food availability
(Salen-Picard et al. 2002; Whitfield 2005), or in the river
plumes that regulate the entrance of marine juvenile fish
into the estuary (Amara et al. 2000; Martinho et al. 2009;
Vinagre et al. 2009a). Temperature is also an important
trigger for several estuarine processes. Changes in tempera-
ture, whether latitudinal or owing to climate, may affect
fish reproduction, growth and migration patterns (Attrill and
Power 2002; Vinagre et al. 2009b). It is therefore expected
that both hydrological changes and temperature will affect
production levels, as production is influenced by the biotic
and environmental conditions influencing individual growth
and population mortality (Brey 2001).

Ó CSIRO 2010 10.1071/MF10002 1323-1650/10/121399

1400 Marine and Freshwater Research M. Dolbeth et al.

10⬚0⬘0⬙W 0⬚0⬘0⬙E 10⬚0⬘0⬙E

60⬚0⬘0⬙N

60⬚0⬘0⬙N
(a)
Minho estuary
St. 7
50⬚0⬘0⬙N

50⬚0⬘0⬙N
Minho
River
St. 6
40⬚0⬘0⬙N

40⬚0⬘0⬙N
St. 5
St. 4

St. 3

10⬚0⬘0⬙W 0⬚0⬘0⬙E 10⬚0⬘0⬙E

Coura 2 km
N St. 2 River
St. 1
(a)

(b) St. 1

St. 4
St. 5
(b)

Spain Mondego
River

Portugal St. 2

Atlantic St. 3
Ocean
Pranto
River
Mondego estuary 2 km

Precipitation stations Runoff stations Sampling stations

Caminha Foz do Mouro
Casal do Rato Açude Ponte Coimbra Intertidal areas

Fig. 1. Location of the studied estuaries on the Portuguese coast, showing sampling stations and intertidal areas; (a) Minho estuary, (b) Mondego estuary.

The perspectives above have triggered the main objectives of
this study: to perform multi-year comparisons of fish recruit-
ment, growth and production in two contrasting estuaries of the
Iberian Peninsula, which were both subjected to an extreme
drought. These climate extremes are expected to increase in
magnitude and frequency (Intergovernmental Panel on Climate
Change 2007), so knowledge of their consequences for fish
carrying capacity becomes essential to understand and mitigate
possible impacts on the ecosystem and economy. Additionally,
both estuaries differ markedly in hydrology and geomorphol-
ogy, and are located within a transitional area with respect to
climate. Both have a temperate climate, but Minho estuary is
characterised by a mild summer, whereas Mondego has a warm
summer (Kottek et al. 2006). Our research questions were:
(1) Are there differences in the recruitment and growth of fish,
despite the slight latitudinal difference?
(2) How does a drought affect the fish recruitment and produc-
tion, taking into account the carrying capacity of each
estuary for fish resources?
(3) Which species are most affected by changes in freshwater
inflow, and is the fish response different depending on local
hydrology and geomorphology?
Materials and methods
Study area
The study was conducted in the Minho and Mondego estuaries,
on the Atlantic coast of the Iberian Peninsula (Fig. 1). Both
estuaries lie in a warm temperate region, with dry summers, but
Minho estuary has a mild summer, whereas Mondego has a
warm summer (Kottek et al. 2006). The main geomorphologic
and hydrological characteristics and anthropogenic pressures
for both estuaries are in Table 1.
The Minho estuary is on the north-west coast (Fig. 1a) and
has a maximum width of 2 km and maximum length of 40 km.
This mesotidal estuary is partially mixed, although during high
flood periods it tends develop into a salt-wedge estuary (Sousa
et al. 2008a, 2008b). The influence of spring tides extends to the
most upstream areas, with several tidal freshwater wetlands
Drought effects on fishes from Iberian estuaries Marine and Freshwater Research 1401

Table 1. Main geomorphological and hydrological characteristics and anthropogenic pressures of Minho and Mondego estuaries
z
Mean temperatures (minimum and maximum temperatures in brackets) during the study period (October 2003–July 2007)

Variable Minho estuary Mondego estuary

0
Latitude 41852 N 408080 N
Area 23 km2 8.6 km2
Mean depth 2.3 m 2–4 m
Intertidal area 9% Whole estuary: 64% (south arm: 75%;
north arm: 10%)
River Minho River, Coura River Mondego River, Pranto River
Mean freshwater flow 300 m3 s1 79 m3 s1
Residence time (days) 1–2 days 1–3 days
Mean tidal range 3m 1–3 m
Water Framework Directive typology Type A1 (mesotidal stratified estuary) Type A2 (mesotidal well-mixed estuary
with irregular river discharge)
Anthropogenic pressures Agriculture, domestic and industrial waste water Bank regulation (owing to port activities,
drainage, bank regulation, fishing, recreational agriculture and aquaculture), fishing
and commercial watercraft activities, dredging and eutrophication
Economic activities Agriculture, fishing and tourism Agriculture, aquaculture, fishing and tourism
(initial development)
Estuarine temperature (8C)z 14.6 (7.2–22.7) (measured in the morning) 16.1 (6.0–25.4) (measured at dusk)
Sea surface temperature (8C)z 16.4 (13.0–21.1) 17.0 (13.0–22.6)

located in the upper 30 km. The main freshwater discharge
to the estuary is from the Minho River, with a catchment of
17 080 km2. The downstream portion of the Coura River also
drains into the Minho estuary in the lowermost 3 km, where it
forms a salt marsh (220 ha). Most of the estuary is subtidal, with
only 9% of the area comprising intertidal sand and mudflats. The
estuary has low pollution levels (Sousa et al. 2008b), but other
threats have been identified, such as habitat loss or disruption,
invasion of non-indigenous species and intensive dredging for
navigation purposes (Table 1, Sousa et al. 2008a, 2008b).
The Mondego estuary is on the central Portuguese coast
(Fig. 1b). It is a small mesotidal estuary (8.6 km2, Table 1) of
well-mixed waters, with its upstream limit 21 km from the
mouth (Teixeira et al. 2008). In the lowermost 7 km, the estuary
separates into two arms (north and south, Fig. 1b) of contrasting
hydrologic characteristics. The north arm is deeper (4–10 m
during high tide), has a mercantile harbour and is the main
navigation channel. Constant dredging and shipping occur
in this area, causing physical disturbance of the bottom. The
main freshwater inflow to the north arm is from the Mondego
River, which drains a catchment of 6670 km2. The south arm is
shallower (2–4 m during high tide) and is characterised by large
areas of exposed intertidal flats during low tide (75% of total
area) (Table 1). Water circulation in the south arm mostly
depends on the tides, on the small freshwater input from the
Pranto River (Fig. 1b), and on a small connection with the north
arm (1-m width). The downstream areas of the south arm contain
Spartina maritima and Scirpus maritimus marshes (66.2 ha)
and a meadow composed of Zostera noltii (4.6 ha), but in the
inner parts the seagrass community has completely disappeared,
mainly as a result of severe eutrophication in the past (Dolbeth
et al. 2007a).
Sampling procedures
Fish were collected monthly from October 2003 to July 2007 in
both estuaries. In Minho estuary, sampling was carried out using
a 1-m beam trawl, with a tickler chain and a 5-mm stretched-
mesh cod end. Sampling occurred in the morning of neap tides.
In general, sampling occurred at seven sampling stations, cov-
ering the different estuarine habitats and salinity ranges (Sousa
et al. 2008a) (Fig. 1a): St. 1, 2.7
0.8 m deep (mean and s.d.);
St. 2, close to a saltmarsh area, 1.3
0.3 m deep; St. 3, in a main
channel, 1.9
0.4 m deep; St. 4, near a sandbank, 2.7
0.9 m
deep; St. 5, close to a saltmarsh area, 2.7
0.9 m deep; St. 6,
with regular freshwater flow, 2.9
0.6 m deep; and St. 7, with
permanent freshwater flow from the Minho river, 2.9
1.0 m
deep. From October 2003 to November 2004 sampling did not
include station 5, and from February 2007 sampling occurred
only at stations 1, 3, 5 and 6 (Fig. 1a). Each survey consisted
of one haul, at each sampling station, with a duration of 3 min
(occasionally only 1.5 min), at a constant speed of 0.51 ms1.
In the Mondego estuary, sampling was carried out using a
2-m beam trawl, with one tickler chain and a 5-mm stretched-
mesh cod end, during the night, at spring tides and in 5 sampling
stations (Fig. 1b): St. 1, 8.7
1.2 m deep; St. 2, upstream of a
Z. noltii bed, 2.3
0.4 m deep; St. 3, 2.4
1.0 m deep; St. 4,
with regular freshwater flow, 5.5
0.5 m deep; and St. 5,
with permanent freshwater flow from the Mondego River,
4.5
0.3 m deep (Fig. 1b). Each survey consisted of three hauls,
at each sampling station, for a total of 3 min duration per station
(occasionally 5 min), at a speed of 1.54 m s1.
In both estuaries, sampling was done around high-water
slack to allow a more homogeneous distribution of the demersal
species, as during low water, organisms are confined to smaller
areas and densities could be overestimated. Also, sampling at
high tide enabled access to certain areas, which could not be
conveniently sampled during low tide.
All fish caught were identified, measured (total length – TL,
with 1-mm precision) and weighed (wet weight – WW, with
0.001-g precision). Owing to the amount of data required for the
production estimates, only the most abundant fish species were
analysed in the present study. The fishes were grouped into
1402 Marine and Freshwater Research
ecological guilds, according to the ‘Estuarine Use Functional
Groups’ by Elliott et al. (2007), which defines the overall
ecological use of an estuary by a species. These corresponded
to the marine–estuarine-dependent species, whose juveniles use
the estuary as nursery grounds: Platichthys flesus and Solea
solea in both estuaries, and Dicentrarchus labrax only in the
Mondego estuary, and the resident species, which live in the
estuary throughout their life cycle: Pomatoschistus microps in
both estuaries and Pomatoschistus minutus only in the Mondego
estuary, as the abundance of this species in the Minho estuary
was quite low.
At each sampling station and for each sampling area, tem-
perature and salinity were measured from water near the bottom
collected with a Van Dorn sampler. Precipitation and freshwater
inflow values were acquired from the Portuguese Water
Institute – INAG (www.snirh.inag.pt) and the Portuguese
Weather Institute – IM (www.meteo.pt). For the Minho estuary,
measured precipitation was acquired from Caminha station
(02E/04UG, INAG); mean precipitation for the 1971–2000
period from Porto station (IM), the closest coastal city to the
Minho estuary with available data; and freshwater inflow from
Foz do Mouro station (01G/02H, INAG) (Fig. 1). For the
Mondego, measured precipitation was acquired from Casal do
Rato station (13D/04UG, INAG); mean precipitation for 1971–
2000 from Coimbra station (IM), 40 km upstream of the estuary;
and freshwater inflow from Açude Ponte Coimbra station (12G/
01A, INAG) (Fig. 1), near the city of Coimbra.
Secondary production and absolute growth rates
In both study areas, the sampled distance was obtained with
GPS. For standardisation of the results, density (N) was obtained
by dividing abundance (total catch) by sampled area. A similar
procedure was done for biomass.
The beam-trawl has been widely used in estuarine systems to
sample the demersal and benthic fish community. Although it
is easy to use and provides qualitative and quantitative data, its
catch efficiency is considered low and variable depending on
the environmental conditions (Hemingway and Elliott 2002).
Because this gear efficiency has generally been assumed to be
30% (Hemingway and Elliott 2002), results are presented with
and without catch efficiency correction, applied to both beam-
trawls used in the present study.
The population structure of each species was defined by
tracking recognisable cohorts (C) from the successive sampling
dates. Spatial samples were pooled together and analysed using
the size frequency distribution of successive sampling dates.
This method enables inference of growth from apparent shift
of modes in a time series of size frequency data. However, the
estimated cohorts were not validated by a direct method to
determine age, such as otolith ageing, and therefore are subject
to error.
For all fish species, cohorts were determined using FAO-
ICLARM Stock Assessment Tools (FiSAT software, http://
www.fao.org/fi/statist/fisoft/fisat/index.htm [Verified 23
August 2010]). Initially, the location of the modes was explored
with Bhattacharya’s method to obtain initial estimates based on
the separation index for the age groups identified (Gayanilo
et al. 2005). The expected mean length for the each age group
M. Dolbeth et al.
was then refined and corrected with the NORMSEP procedure,
which separates normally distributed components of the size-
frequency samples (Gayanilo et al. 2005). The output of this
analysis is mean length, standard deviation, population sizes and
separation indices for the identified age groups.
After recognition of the cohorts, the annual production was
estimated by the cohort increment summation method (Winberg
1971) given by:
1 
TX 
Nt þ Nt þ 1
Pcn ¼  ð  tÞ
wt þ 1  w ð1Þ
2
t¼0
where Pcn is the growth production (g WW m2 year1) of
cohort n; N is the density (ind m2), determined as mentioned
 is the mean individual weight (g WW); and t and t þ 1,
above; w
consecutive sampling dates. Population production estimates
correspond to the sum of each cohort production (Pcn). Negative
production values were not included in the overall estimates and
were regarded as zero production. Monthly and annual pro-
duction values were analysed for this study. Annual production
was computed per hydrological year, from October to
September.
Absolute growth rates (AGR, cm day1) were determined for
each cohort per age (0þ, 1þ), according to:
Lt2  Lt1
AGR ¼ ð2Þ
t2  t1
where Lt2 and Lt1 are the total length at time t2 and t1 respectively.
Multivariate statistical analyses
To evaluate the relationships between production of the differ-
ent species and the environmental variables, data were ordinated
using CANOCO v 4.0 software (Ter Braak and Smilaeur 1998).
Monthly data of the fish production and environmental para-
meters was pooled into seasons for ordination. Initially, a
detrended correspondence analysis (DCA) was performed with
the fish species mean annual production to evaluate if the
species had a linear or unimodal response to the environment
(Ter Braak and Smilaeur 1998). Whenever a linear response
was detected, a redundancy analysis (RDA) was applied; if
the response was unimodal, a canonical correspondence ana-
lysis (CCA) was applied to examine the relationships between
biotic and abiotic parameters (biplot rule, inter-sample dis-
tances). The environmental variables included precipitation,
freshwater inflow, mean estuarine salinity and mean estuarine
temperature. All environmental variables were used in a first
analysis and their statistical significance was tested with the
model forward-selection procedure (Ter Braak and Smilaeur
1998). A second analysis was performed only with the sig-
nificant environmental variables.
Results
Environmental characterisation
The mean estuarine salinity in both estuaries (Fig. 3a, b) was
clearly associated with the river inflow to the estuary, which
in turn was associated with precipitation (Fig. 2). Higher
precipitation led to increases in river inflow (Fig. 2a, b), with
Drought effects on fishes from Iberian estuaries Marine and Freshwater Research 1403

Minho
(a) 30 ⫻ 108 350

25 ⫻ 108 300

250

Precipitation (mm)
River runoff (m3)

20 ⫻ 108
200
15 ⫻ 108
150
10 ⫻ 108
100

5 ⫻ 108 50

0 0
M-03
M-03
J-03
S-03
N-03
J-04
M-04
M-04
J-04
S-04
N-04
J-05
M-05
M-05
J-05
S-05
N-05
J-06
M-06
M-06
J-06
S-06
N-06
J-07
M-07
M-07
J-07
S-07
N-07
(b) 30 ⫻ 108 Mondego 350

25 ⫻ 108 300

250

Precipitation (mm)
River runoff (m3)

20 ⫻ 108
200
15 ⫻ 108
150
10 ⫻ 108
100

5 ⫻ 108 50

0 0
M-03
M-03
J-03
S-03
N-03
J-04
M-04
M-04
J-04
S-04
N-04
J-05
M-05
M-05
J-05
S-05
N-05
J-06
M-06
M-06
J-06
S-06
N-06
J-07
M-07
M-07
J-07
S-07
N-07
2003 2004 2005 2006 2007

Runoff Avg. precipitation 1971–2000 Precipitation

Fig. 2. Temporal variations in precipitation during the study period and freshwater runoff (cubic metres, m3) to Minho and Mondego estuaries, and average
precipitation values during the period of 1971–2000 for north Portugal (Minho) and for central Portugal (Mondego). Arrows, above 1971–2000 mean
precipitation (floods); dashed lines, below 1971–2000 mean precipitation (droughts).

subsequent decreases in the mean estuarine salinity and in the especially considering these are night-time water temperatures,
salinity of the most upstream areas (Fig. 3a, b). In contrast, as opposed to the daily measured temperatures in the Minho
prolonged periods of low precipitation, low freshwater inflow estuary. This tendency was also observed in sea-surface tem-
(Fig. 2) and high mean salinity (Fig. 3a, b) occurred in both peratures in the coastal areas adjacent to both systems (Fig. 3c, d,
estuaries. In 2004, a drought occurred, extending to a severe Table 2). The hydrological year with the highest mean estuarine
drought in 2005 (Table 2), with associated reduction in the and sea surface temperature was 2005–06 for both estuaries
freshwater inflow and higher salt incursion for both estuaries (Table 2).
(Fig. 2), especially in 2005 and in the most-upstream areas
(Fig. 3a, b). According to the Portuguese Weather Institute (IM),
the 2005 drought was the harshest since 1931. The amount of Recruitment and growth rate
freshwater discharge and mean water flow was considerably Despite the difference in the beam-trawl width used in each
higher in the Minho estuary (Fig. 2, Table 1). The amount of estuary (1-m and 2-m beam trawl), the size range of fishes
precipitation during the drought period, compared with Porto caught was similar (Figs 4, 5). During the study period, and for
and Coimbra 1971–2000 means, was lower and more extensive the studied species, 50 679 individuals were caught in the Minho
in the Mondego estuary (
70% lower) than in the Minho (
50% estuary (98% were Pomatoschistus microps) and 6915 indivi-
lower) (Table 2, Fig. 2). duals in the Mondego estuary.
Higher temperatures were observed in the Mondego estuary In the Minho estuary, the recruitment of the flatfishes
compared with the Minho estuary (Fig. 3c, d, Table 2), Platichthys flesus and Solea solea seemed to occur in May
1404 Marine and Freshwater Research M. Dolbeth et al.

Minho Mondego
(a) 40 (b) 40
35 35
30 30
25 25
Salinity

20 20
15 15
10 10
5 5
0 0
O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07

O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07
Downstream area (St. 1) Estuarine mean Upstream area (St. 6) Downstream area (St. 1) Estuarine mean Upstream area (St. 5)

(c) 27 (d) 27
24 24
21 21
Temperature (⬚C)

18 18
15 15
12 12
9 9
6 6
3 3
O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07

O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07
Estuarine mean Sea surface water Estuarine mean Sea surface water

2003 2004 2005 2006 2007 2003 2004 2005 2006 2007

Fig. 3. Mean estuarine salinity, salinity values at downstream and upstream areas (a, b), and mean estuarine temperature
s.d. (c, d) for the Minho and the
Mondego estuaries.

Table 2. Annual precipitation, mean estuarine temperature and mean sea surface water temperature (minimum and maximum in brackets) during
the study period for the Minho and Mondego estuaries, and average precipitation during the period of 1971]2000 for northern Portugal (Minho) and
for central Portugal (Mondego)

Measure Hydrological year (Oct–Sep)

2003–04 2004–05 2005–06 2006–07 1971–2000

Minho estuary
Precipitation (mm) 1052 578 1202 1271 1254
Sea surface temperatures (8C) 16.8 (13.0–21.1) 16.3 (13.5–20.0) 16.6 (13.4–20.0) 16.3 (13.0–20.0) –
Estuarine temperature (8C) 15.0 (10.4–20.0) 14.5 (9.0–18.9) 14.9 (10.2–19.4) 14.3 (9.6–18.5) –
Mondego estuary
Precipitation (mm) 712 285 662 1023 905
Sea surface temperatures (8C) 17.5 (13.5–22.6) 16.6 (13.0–21.0) 17.2 (13.0–22.2) 17.3 (14.0–20.8) –
Estuarine temperature (8C) 15.7 (9.7–23.1) 16.2 (6.0–25.4) 16.5 (9.3–24.8) 16.2 (9.3–23.3) –

(Fig. 4a, b). A few small S. solea were found during the previous seemed to occur in January in 2004 and 2005 (C3 and C4), but
winter (C3 and C4, Fig. 4b), but the majority of individuals was delayed until April in 2006 and 2007 (C5 and C6, Fig. 4d).
appeared in May. P. flesus remained for at least two years in For both flatfishes, individuals stayed up to two years in the
the estuary, with larger individuals only occasionally being estuary, completely disappearing before the age of three years
captured (Fig. 4a). In contrast, only small individuals of S. solea (Fig. 4d). Higher growth rates were observed for S. solea
were found, and all were less than one year old (Fig. 4b). The compared with P. flesus (Table 3). Dicentrarchus labrax
highest growth rates of P. flesus were in 2005, the drought year, recruited in June (Fig. 4e), with individuals staying in the
whereas for S. solea, the lowest was in 2003 and similar growth estuary for at least 18–19 months (Fig. 4e).
rates were obtained afterwards (Table 3). For P. microps, a For the resident species, three recruitment periods per year
single recruitment was identified per year in June, although this were detected for P. microps in January, April and June–July
period might extend until September as smaller individuals also (Fig. 5b); and two for Pomatoschistus minutus in April and
occurred at that time (Fig. 5a). Growth rates were similar within November (Fig. 5c). In the April cohorts of 2003 and 2005 of
the years (Table 3). P. minutus (C3 and C6 respectively), individuals were absent from
In the Mondego estuary, recruitment of P. flesus took place in October to February, returning afterwards to the estuary. Recruits
April (Fig. 4c). In 2005 and 2007, individuals only appeared in from April 2004 stayed in the estuary slightly longer, but the older
June–August (C4 and C6); however, the lack of the smaller size individuals did not appear again (C4, Fig. 5c). In 2005, individuals
classes in these cohorts suggests that recruitment also started in were scarce, but a new cohort appeared in August (C7) and in
April (similar to C3 and C5, Fig. 4c). For S. solea, recruitment 2006, the usual November recruitment did not occur (Fig. 5c).
 Length (cm) Length (cm)
0
5
10
15
20
25
30
35
(b) 40
0
5
10
15
20
25
30
(a) 35

O-03 O-03
D-03 D-03
2003
C1

F-04 F-04
A-04 A-04
J-04 J-04
2004

A-04 A-04
C2
C1

O-04 O-04
D-04 D-04
F-05 F-05
C4
C2

A-05 A-05
J-05 J-05
2005

A-05
estuaries, with indication of the cohorts (C).

A-05
O-05
Minho

O-05
C3

D-05 D-05
F-06 F-06
A-06
C5

A-06
J-06 J-06
2006
C3

A-06 A-06
O-06 O-06
C4

D-06 D-06
F-07 F-07
A-07 A-07
2007

J-07 J-07
S. solea
P. flesus

A-07
C4

C5

A-07
C5
C6

Length (cm) Length (cm) Length (cm)

0
5
10
15
20
25
30
(e) 35
0
5
10
15
20
25
30
35
(d) 40
0
5
10
15
20
25
30
(c) 35

O-03 O-03 O-03

D-03 D-03

2003
D-03
C3

F-04 F-04 F-04

C3

C2 A-04
A-04
C1

A-04
C1

C4
J-04 C1 J-04 J-04

2004
A-04 A-04 A-04
O-04 O-04 O-04
D-04 D-04 D-04
C4
F-05 F-05 F-05
A-05 A-05 A-05

C5
C4

J-05 J-05 J-05

C2

2005
A-05 A-05 A-05
O-05 O-05 O-05
Mondego

D-05 D-05 D-05

F-06 F-06 F-06

C3
C5
C5
C2

A-06 A-06

C6
A-06
J-06 J-06

C3
J-06

2006
A-06 A-06 A-06
O-06 O-06 O-06
C3

C4
D-06 D-06 D-06

C4

C5
C6
F-07 F-07 F-07
A-07 A-07 A-07

2007
D. labrax
P. flesus

S. solea
C6
J-07
C4

J-07 J-07

C5

C6
C5
A-07

C7
A-07

Fig. 4. Mean cohort length of the marine–estuarine-dependent species (Dicentrarchus labrax, Platichthys flesus and Solea solea) (
s.d.) from Minho and Mondego
A-07
1405 Marine and Freshwater Research Drought effects on fishes from Iberian estuaries
1406 Marine and Freshwater Research M. Dolbeth et al.
Table 3. Absolute growth rates (AGR, cm day21) for each fish cohort, from each age group (01 and 11) per year, with 95% confidence limits, the cohort (C) and year when the cohort started

C5: 0.037
0.002, 0.070
0.02*

Individuals of P. minutus grew faster than those of P. microps,
*S. solea AGR for time period smaller than 5 months (mean time duration of Minho cohorts). Confidence limits were not computed when the sample size (n) of one of the means was lower than 3

with the highest rates observed in 2005 and 2006 (Table 3). For
both resident species, most of the cohorts were mainly young
individuals, with one-year-old individuals representing only a

C10: 0.009
0.0007

C11: 0.007
0.0003
C12: 0.009
0.0007
2006

small fraction of the overall population (Fig. 5a, c).

C6: 0.032
0.012
C5: 0.036
0.022

C6: 0.026
0.003

C5: 0.052
0.007

C9: 0.013
0.002

–
In general, higher absolute growth rates were observed in
the Mondego estuary for all species and ages (Table 3). The
C4: 0.034

C8: 0.011
exception occurred for 2005 cohorts, when the absolute
growth of the flatfish, P. flesus and S. solea, was higher in
the Minho estuary (Table 3).
Production dynamics
C4: 0.046
0.016, 0.051
0.03*
Mondego estuary

In the Minho estuary, P. flesus was the main species con-

tributing to community production. Accordingly, the pro-
duction peaks in each year occurred in summer, mainly as a
C7: 0.006
0.0003
C8: 0.006
0.0004
C9: 0.008
0.0004
2005

result of P. flesus production (Fig. 6a). During 2005–06, this

C5: 0.023
0.006
C4: 0.023
0.008

C3: 0.039
0.012

C5: 0.029
0.010

C4: 0.028
0.005

C7: 0.014
0.001

–

pattern changed and the resident P. microps had the highest

biomass and production (Fig. 6, Table 4). P. microps exhib-
C6: 0.011

ited highest density in all years and had higher production than
S. solea (Table 4, Fig. 6a). During the whole study period, the
lowest production occurred in the hydrological year of 2004–
05 (Table 4, Fig. 6a), which corresponded to the year with
C3: 0.049
0.016, 0.050*

minimal annual precipitation (less than half of the 1971–2000

mean, Table 2) and lowest freshwater inflow (Fig. 2a). In this
year, density, biomass and production of S. solea increased
C4: 0.027
0.007
C3: 0.027
0.008

C2: 0.038
0.010

C4: 0.006
0.002

C5: 0.006
0.001
C6: 0.006
0.001

C4: 0.011
0.001

C5: 0.012
0.001
2004

compared with the previous year, whereas P. flesus and P.

–

microps biomass and production decreased considerably, and

C4: 0.031
C3: 0.043

the P/B increased substantially (Table 4, Fig. 6a). In 2006–07,

production values were similar to 2005–06, bearing in mind
that values refer only to 10 months (and therefore may have
been even higher) (Table 4).
C5: 0.069
0.011*

C5: 0.005
0.0005

In the Mondego estuary, the marine–estuarine-dependent

C5: 0.025
0.002
C4: 0.028
0.016

C4: 0.006
0.001

species attained higher levels of production than the resident

2006

species (Table 4), which had the lowest biomass and production
–

–
–

(Table 4, Fig. 6b). None of the seasons showed a clear and

systematic increase in production (Fig. 6b). The highest annual
community production occurred in 2004–05, the year with
minimal annual precipitation (less than a third of the 1971–
C4: 0.061
0.003*

C4: 0.004
0.0005

2000 mean, Table 2), mainly as a result of increased production

C4: 0.033
0.002

C3: 0.005
0.001

Minho estuary

of S. solea (Table 4, Fig. 6b). The other species maintained

2005

similar levels of production compared with the other years,

–

–
–

–
C3: 0.034

except in 2006–07, and except for P. minutus, whose production

decreased considerably (Table 4, Fig. 6b). In 2006–07, there
seemed to be a decreasing trend in the fish production (Table 4),
which matches the early disappearance of P. flesus (C4, Fig. 4b)
C3: 0.036
0.007*

C3: 0.004
0.0005

C3: 0.025
0.013

C2: 0.005
0.001

and D. labrax (C5, Fig. 4e) cohorts and the lack of young
individuals in the cohorts of 2007 (C6 for P. flesus and C7 for

2004

D. labrax, Fig. 4b, e). For all species and in both estuaries, P/B
–

–
–

–
C2: 0.023

ratios were generally higher in 2004–05 (Table 4).

Comparing both estuaries, community annual density,
biomass and production were much higher in the Minho
estuary (2 to 3 times higher) than in the Mondego estuary
 were obtained in
Pomatoschistus microps

Pomatoschistus minutus

(Fig. 6c, Table 4). For P. microps, higher P/B

Dicentrarchus labrax

the Mondego estuary (Table 4), consistent with the shorter

Platichthys flesus

cohort life spans (Fig. 5b). S. solea had higher density values
in the Minho estuary than in the Mondego estuary, yet
Growth year

Solea solea

biomass values were considerably lower, which translated

into lower production and higher P/B  (Table 4), as the
0þ
1þ

0þ
1þ

0þ
1þ

0þ

1þ

0þ

population was mainly composed of juveniles (Fig. 4c).

Drought effects on fishes from Iberian estuaries Marine and Freshwater Research 1407

(a) 7 Minho P. microps

6
C4
C2 C3
5
C1 C5
Length (cm)

2 C3
C5 C6
C4
1

0
O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07
2003 2004 2005 2006 2007

(b) 7 Mondego P. microps

C7
6 C9
C1 C8
5 C4 C5 C11
C10
Length (cm)

C2
4 C6 C12
C3
3 C13

2 C13
C4 C5
C7 C14
1 C6 C8
C9 C10 C11 C12
0
O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07
(c) 9 P. minutus
C1 C3
8 C5 C7
C8
7 C2 C6
6
Length (cm)

5 C4 C9
4
3 C10
C1
2 C5
C4 C8 C9
1 C6 C7

0
O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07

2003 2004 2005 2006 2007

Fig. 5. Mean cohort length of the resident species (Pomatoschistus minutus and Pomatoschistus microps) (
s.d.) from Minho
and Mondego estuaries, with indication of the cohorts (C).

Relation between fish production (Po0.05, after forward-selection) in the distribution of the fish
and environmental parameters species production (Fig. 7a). Total variance explained by the
The DCA detected a linear response for the data of each estuary fish production and temperature was 17%. S. solea and P. flesus
alone (gradient lengtho3), and a unimodal response for the production was associated with higher temperatures, occurring
combined data of both estuaries (gradient length43). Accord- mainly in spring-summer, but also in some autumn periods
ingly, a RDA was applied to each estuary’s data and a CCA was (Figs 3c, 7a). These results match the observed distribution of
used for the combined data of both estuaries. production peaks during the year for both species (Fig. 6a).
The RDA for the Minho estuary revealed that the mean P. microps production seemed to be associated with lower
estuarine temperature was the single significant predictor temperatures (Fig. 7a), occurring mainly in autumn and winter
1408 Marine and Freshwater Research M. Dolbeth et al.

(a) 0.8 Minho estuary

0.7

0.6
g WW m⫺2 month⫺1

0.5

0.4

0.3

0.2

0.1

0
Aut Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum

(b) 0.2 Mondego estuary

0.18
0.16
g WW m⫺2 month⫺1

0.14
P. microps
0.12 P. minutus
0.1 P. flesus
0.08 D. labrax
0.06 S. solea
0.04
0.02
0
Aut Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum

(c) 0.8

0.6
g WW m⫺2 month⫺1

0.4

0.2 Minho estuary

Mondego estuary

0
O-03
D-03
F-04
A-04
J-04
A-04
O-04
D-04
F-05
A-05
J-05
A-05
O-05
D-05
F-06
A-06
J-06
A-06
O-06
D-06
F-07
A-07
J-07
A-07

Aut Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum Aut Win Spr Sum

2003 2004 2005 2006 2007

Fig. 6. Monthly variation in production along the study period, with cumulative community production and contribution of each
species for the Minho (a) and the Mondego (b) estuaries.

(Figs 3c, 6a, 7a). A similar RDA analysis was performed with However, the total variance explained by the fish and all
the Mondego estuary data, but no significant environmental environmental parameters relation was again low – only 18%.
relationships were detected and the variance explained by the The samples of the Mondego estuary clearly separated from the
model was only 7%. Therefore, this analysis was not presented ones of Minho estuary, with higher freshwater inflow associated
graphically. with the Minho samples (Fig. 7b). D. labrax and P. minutus
The CCA for the combined data from Mondego and Minho production was associated with the Mondego samples (Fig. 7b).
estuaries revealed that temperature and freshwater inflow were S. solea occurred in both estuaries, had higher production from
significant in the distribution of the fish species production. the hydrological year of 2004–05 onwards and was associated
Table 4. Annual mean density (ind m22), mean biomass (g WW m22), with indication of confidence intervals at 95% (6LC), production (g WW m22 year21) and P/B  ratios for each species and
the fish community in study
In brackets, production values after correction for the gear catch efficiency of the beam trawl (0.3); 2006–07*, data refers to 10 months only (annual production might be higher)

Parameter Hydrological year (Oct–Sep)

Minho estuary Mondego estuary
2003–04 2004–05 2005–06 2006–07* 2003–04 2004–05 2005–06 2006–07*

Density (ind m2)

Drought effects on fishes from Iberian estuaries

D. labrax – – – – 0.010
0.0012 0.003
0.0004 0.004
0.0006 0.002*
0.0006

P. flesus 0.03
0.005 0.03
0.008 0.02
0.003 0.03*
0.007 0.002
0.0003 0.001
0.0002 0.001
0.0001 o0.001*
0.0002
S. solea 0.006
0.0009 0.018
0.0051 0.002
0.0004 0.015*
0.0045 0.001
0.0001 0.002
0.0002 0.002
0.0004 0.002*
0.0004
P. microps 1.32
0.14 1.01
0.10 2.60
0.19 2.52*
0.55 0.005
0.0012 0.006
0.0010 0.008
0.0021 0.005*
0.0007
P. minutus o0.001 o0.001 0.012 0.001* 0.003
0.0007 0.001
0.0002 0.002
0.0007 0.002*
0.0001
Community 1.36
0.14 1.05
0.09 2.63
0.19 2.57*
0.55 0.022
0.0015 0.013
0.0015 0.016
0.0027 0.011*
0.0012
Biomass (g WW m2)
D. labrax 0.16
0.020 0.07
0.009 0.05
0.006 0.03*
0.009
P. flesus 0.35
0.056 0.10
0.016 0.17
0.032 0.32*
0.101 0.06
0.008 0.02
0.004 0.03
0.006 0.01*
0.006
S. solea 0.003
0.001 0.02
0.006 0.01
0.002 0.04*
0.016 0.08
0.012 0.12
0.022 0.05
0.014 0.06*
0.012
P. microps 0.43
0.045 0.26
0.023 0.67
0.043 0.61*
0.122 0.001
0.0001 0.001
0.0002 0.002
0.0003 0.002*
0.0003
P. minutus o0.001 o0.001 0.01 0.001* 0.003
0.0008 0.001
0.0004 0.002
0.0004 0.001*
0.0004
Community 0.91 0.36 0.91 1.11* 0.30
0.039 0.22
0.030 0.14
0.021 0.11*
0.015
Production (g WW m2 year1)
D. labrax – – – – 0.25 (0.83) 0.23 (0.77) 0.17 (0.57) 0.03* (0.10)
P. flesus 1.45 (4.83) 0.66 (2.20) 0.82 (2.73) 0.83* (2.77) 0.10 (0.34) 0.08 (0.27) 0.10 (0.35) 0.01* (0.03)
S. solea 0.02 (0.07) 0.25 (0.83) 0.17 (0.57) 0.21* (0.70) 0.10 (0.34) 0.34 (1.14) 0.11 (0.35) 0.15* (0.51)
P. microps 0.55 (1.83) 0.39 (1.29) 0.91 (3.03) 0.71* (2.37) 0.002 (0.007) 0.003 (0.010) 0.004 (0.013) 0.004* (0.013)
P. minutus – – – – 0.01 (0.033) 0.004 (0.013) 0.004 (0.013) 0.003* (0.010)
Community 2.02 (6.73) 1.30 (4.32) 1.90 (6.33) 1.75* (5.84) 0.46 (1.54) 0.68 (2.26) 0.38 (1.26) 0.20* (0.66)
P/B
 (year1)
D. labrax – – – – 2.3 4.5 3.0 2.0*
P. flesus 2.7 6.9 3.2 1.3* 2.2 2.9 2.5 1.3*
S. solea 10.9 9.6 5.4 11.6* 2.3 3.9 1.6 3.5*
P. microps 1.5 1.8 1.4 1.5* 3.0 3.2 2.5 4.1*
P. minutus – – – – 4.2 3.2 2.2 3.3*
Marine and Freshwater Research
1409
1410 Marine and Freshwater Research M. Dolbeth et al.

(a)

2.5

P. flesus

Mean temperature
S. solea P. microps

Samples
Spring
Summer
⫺1.5

Autumn
Winter
⫺2.0 2.0

(b)
3.0

P. minutus

P. microps

D. labrax

S. solea
Runoff Samples
2003–04
Mean temperature 2004–05
P. flesus
2005–06
⫺1.5

2006–07
⫺2.5 3.0

Fig. 7. Ordination plots relating fish production and environmental variables along the study
period: (a) RDA ordination triplot for Minho estuary samples, with classification of the
samples per season (winter, December–February; spring, March–May; summer, June–August;
autumn, September–November); (b) CCA ordination triplot for all samples from Minho and
Mondego estuaries, with classification of the samples per hydrological year. Squares, Minho
estuary samples within the ordination space; circles, Mondego estuary samples within the
ordination space; grey vector lines, fish production; black vector lines, relationship of
significant environmental variables to the ordination axis, whose length is proportional to
their relative significance; black cross, species production positions within the ordination
space.

with higher temperatures (Fig. 7b). P. flesus and P. microps Discussion

production was mainly associated with the Minho estuary and Recruitment and growth rates: the role of temperature
with higher freshwater inflow values (Fig. 7b). For both species,
In the Minho estuary, located at higher latitude than the Mon-
the highest production values were obtained in 2003–04 and
dego estuary, the recruitment of all species took place later,
2005–07. P. flesus production was also associated with higher
and growth rates were slightly lower. Although the latitudinal
temperature (Fig. 7b), occurring mostly in spring and summer
difference is small, the Minho estuary typically had lower
(Fig. 7a), whereas P. microps production was linked to lower
temperatures than the Mondego, which agrees with the classi-
temperatures (Fig. 7b), mostly in winter and spring (Fig. 7a).
fication of Kottek et al. (2006). These differences might have
Table 5. Production estimates from European transitional waters, with indication of the production for the species in the present study, and the community production values and the number of
species included in the community; in brackets production after correction for the catch efficiency of the sampling gear
*Original units in ash free dry weight (AFDW) were converted to wet weight (WW) (WW–AFDW: 0.251, Brey 2001)

Location Latitude Estuarine Study Sampling Production Production (g WW m2 year1) No. species Community Reference
area (km2) period gear estimation P. flesus S. solea D. labrax P. minutus P. microps studied within production
method the community (g WW m2 year1)

Gullmarsvik, 588 0.015 1978–1980 Portable Cohort – – – 0.96* 1.16* 2.23* 1.67* 3 3.19* 3.78* Pihl and
Drought effects on fishes from Iberian estuaries

Sweden drop trap Increment 1.27* 0.04* 0.04* 0.16* 1.67* 0.96* Rosenberg 1982
summation
Laholm Bay, 568 25 km May–Sep: 2-m beam Cohort – 0.17* 0.04* – – – 3 4.41* 1.42* Pihl 1989
Sweden shoreline 1984–1986 trawl Increment 0.21* (5 (juvenile 5.63* (5 months)
length summation months) flatfishes)
Forth estuary, 568 84 1982–1985 Beam trawl Instantaneous 1.193 – – – – 47 4.030 4.239 Elliott and
Scotland growth 1.406 4.626 4.400 Taylor 1989
1.455
1.030
Oosterschelde 518 351 1987–1989 3-m beam Empirical 0.16* 0.24* – 0.08* – 40 11.95* Hostens and
estuary, trawl model: Hamerlynck
Netherlands P/B
 ¼ 2.5 1994
Minho estuary, 418 23 2003–2006 1-m beam Cohort 1.45 0.66 0.02 0.25 – – 0.55 0.39 3 2.02 1.30 Present study
Portugal trawl Increment 0.82 (2.20– 0.17 (0.07– 0.91 (1.29– (benthic and 1.90 (4.32–6.73)
summation 4.83) 0.83) 3.03) demersal
community)
Ria de Aveiro, 408 47 1999 and 2000 ‘Chincha’ Instantaneous – – 0.015 0.596 – 0.012 0.033 10 1.59 1.98 Pombo et al.
Portugal traditional growth (2.10–2.48) 2007
beach-
seine
net
Mondego 408 8.6 2003–2006 2-m beam Cohort 0.10 0.08 0.10 0.34 0.25 0.23 0.01 0.004 0.002 0.003 5 0.46 0.68 Present study
estuary, trawl Increment 0.10 0.11 0.17 0.004 (0.013– 0.004 (benthic and 0.38
Portugal summation (0.27–0.35) (0.34–1.14) (0.57–0.83) 0.033) (0.007– demersal (1.26–2.26)
0.013) community)
Marine and Freshwater Research
1411
1412 Marine and Freshwater Research
been the main cause for the present results, as temperature is an
important trigger for fish migration, growth and reproduction
patterns (Attrill and Power 2002; Henderson and Seaby 2005).
Similar latitudinal gradients, related to temperature, have also
been observed at larger geographical scales, in different Eur-
opean coastal areas, in spawning, recruitment, growth rate and
life spans of the species analysed in the present study. In general,
earlier recruitment, higher growth rates and shorter life spans
occur at lower latitudes, e.g. Pomatoschistus minutus and P.
microps (Bouchereau and Guelorget 1998; Dolbeth et al.
2007b), Dicentrarchus labrax (Vinagre et al. 2009b) and Solea
solea (Henderson and Seaby 2005; Vinagre et al. 2008).
Another relevant aspect was the higher recruitment for
P. microps in the Mondego estuary compared with the Minho.
A continuous breeding season from January to June, with some
spawning peaks during this period, has been hypothesised
for P. microps, as found by Fouda and Miller (1981) and
Bouchereau and Guelorget (1998). The high temperatures and
high productivity of the Mondego estuary are probable reasons
for the long breeding season (Dolbeth et al. 2007b). This longer
reproductive season could be regarded as an opportunist strategy
(Fonseca and Cabral 2007) and favour the Mondego populations
under climatic and anthropogenic stress, analogous to the
observed differences found by Dolbeth et al. (2007b), when
comparing P. microps and P. minutus strategies to cope with
environmental instability. However, during the study period, the
production of P. microps from the Minho estuary was always
considerably higher than in the Mondego, suggesting that other
factors may influence production.
Multi-year comparisons of fish species abundance and pro-
duction for each estuary suggest that the recruitment strength
was different throughout the study period, especially during
the drought. This may be related to the limiting effects of
high temperatures and salinity variations, caused by hydrologi-
cal changes during the drought, for eggs and larval development
(Fonds and Van Buurt 1974), or larval migration to the estuary
(Amara et al. 2000; Whitfield 2005), restraining the subsequent
population development, as outlined by Dolbeth et al. (2008a).
Similarly, Costa et al. (2002) showed that in very dry years, the
recruitment of marine juveniles using the estuaries as nurseries
could be reduced.
Estuarine fish community production
The fish assemblage was composed475% by abundance of
benthic and demersal fish. This gives an indication of the car-
rying capacity of each estuary for those fish. Results have also
an economic relevance, since all of the marine juvenile species
in this study are commercially exploited (Teixeira and Cabral
2009; Vinagre et al. 2009b) and their estuarine production will
have impacts on the adult coastal populations (Dolbeth et al.
2008a; Vasconcelos et al. 2008).
The main source of inaccuracy for fish production estimation
lies in the error in determining population sizes and their
changes (Cowley and Whitfield 2002); for this reason, estuarine
fish production studies are not common (Costa et al. 2002).
Because the sampling procedure was different, comparisons of
estuarine production between estuaries must be tentative. In the
Minho estuary, sampling took place during the day which, when
comparing day and night beam trawl catches, may result in
M. Dolbeth et al.
lower fish density (Rotherham et al. 2008). In contrast, Ribeiro
et al. (2006) did not observe diurnal changes in fish densities of
the Ria Formosa, southern Portugal, a system more influenced
by the tidal regime. There are no studies comparing day and
night sampling in the Minho estuary, nor are there studies
comparing the catch efficiency for 1-m and 2-m beam trawl.
Nonetheless, sampling was performed in the Minho estuary by
França et al. (2009), using a 2-m beam trawl during the night in
May and July 2006, covering the sampling stations of the present
study. Their estimates of population density were higher for the
flatfishes P. flesus and S. solea, and slightly lower for P. microps
in those months (S. França, pers. comm.). This comparison only
refers to two sampling dates, but it seems reasonable to assume
that the present results on fish density, biomass and consequent
production were underestimated for the Minho estuary.
For the reasons mentioned above, fish production results of
both estuaries and from other European transitional waters are
not comparable, owing to differences in sampling procedures
and estimation methods (Table 5). Even so, benthic and demer-
sal fish assemblage production in the Minho estuary was higher
than in the Mondego estuary, and generally higher than in other
European areas, especially after gear efficiency correction
(Table 5).
The main geomorphological differences between the two
studied estuaries are: (1) estuarine area – the Minho estuary area
is 2.5 times larger; (2) freshwater inflow, associated with the
precipitation regime – on average, almost four times higher in
the Minho estuary; (3) estuarine width smaller in the Mondego
estuary (525 m for the Minho and 250 m for the Mondego
estuary), probably influencing the abundance of marine–
estuarine-dependent species (Martinho et al. 2007; Dolbeth
et al. 2008a; Costa-Dias et al. 2010); and (4) higher availability
of freshwater wetlands in the Minho estuary, with plentiful food
resources (Sousa et al. 2008a, 2008b). Comparing studies of fish
production along the European coast with the present ones,
no pattern seems to exist between production and latitude (and
temperature regimes) or with estuarine area (Table 5). However,
some studies have shown that freshwater inflow into the estuary
has a strong impact on its physical, chemical and biological
characteristics (Salen-Picard et al. 2002), which in turn has
direct or indirect effects on fish abundance (Costa et al. 2007;
Martinho et al. 2007; Gillson et al. 2009) and production
(Dolbeth et al. 2008a). Although excessive freshwater inflow,
during extreme flooding episodes, may be detrimental (e.g.
Pampoulie et al. 2001), moderate discharges may have positive
impacts for coastal fisheries (Houde and Rutherford 1993;
Whitfield 2005), as these may provide extra food resources
for the fish assemblage (Salen-Picard et al. 2002; Vinagre et al.
2007).
The hypothesis that freshwater inflow might have conse-
quences on the fish production levels acquires special relevance
when performing multi-year comparisons of production in each
estuary and their response to the drought effects. In the Minho
estuary, a considerable decrease in the community production
was observed during the hydrological year of 2004–05, when
the drought was more noticeable and the freshwater inflow the
lowest. The relationship between fish production and the studied
environmental parameters was not strong, suggesting that
other factors may explain the obtained results (e.g. predation,
Drought effects on fishes from Iberian estuaries
competition for food and space), including indirect factors
associated with freshwater inflow (e.g. food availability, estuar-
ine immigration of fish larvae; see Salen-Picard et al. 2002;
Schlacher et al. 2008; Vinagre et al. 2009a). The pattern
observed in the present study is consistent with other worldwide
studies on the impacts of drought in fish estuarine communities,
which report overall decreases of fish abundance with reduced
freshwater inflow (South Africa: Whitfield 2005; Europe: Costa
et al. 2007; Martinho et al. 2007; US: Houde and Rutherford
1993; Australia: Gillson et al. 2009).
Species-specific responses to drought events
During the drought in 2004–05, fish community production
decreased in the Minho estuary by more than 60% and increased
in the Mondego estuary, showing that the response to the
drought effects and lower freshwater inflow may be highly
species-specific and dependent on local conditions. In the
Minho estuary, the decrease in community production was a
result of a substantial decrease of P. flesus. Compared with other
European systems, P. flesus density (Cabral et al. 2007) and
production (after gear efficiency correction) were relatively
high (Table 5) (bearing in mind that production in the Minho
estuary is probably underestimated). Given that this species’
coastal stocks probably predominantly originate in northern
Portuguese estuaries (Vasconcelos et al. 2008), such as Minho
estuary, this decrease in the estuarine production might imply
negative impacts on fisheries. P. flesus juveniles generally
prefer low-salinity water (Cabral et al. 2001, 2007), and the
Minho estuary has several freshwater wetlands, which provide
both refuge habitats and plentiful food resources (Sousa et al.
2008a, 2008b; Freitas et al. 2009), and serve as potential nursery
grounds for the species. Production of this species was asso-
ciated with high freshwater inflow, which was considerably
reduced during the drought. In Mondego estuary, this tendency
also occurred, with a reduced production of P. flesus during
drought. Similarly, Martinho et al. (2009) showed that the
abundance of P. flesus juveniles was strongly associated with
the precipitation and freshwater discharge regimes. The pro-
duction decrease was not as high as in the Minho estuary,
because production levels in the Mondego are naturally lower.
This has been attributed to the fact that the central Portuguese
coast is the current southern limit for the distribution of P. flesus
(Cabral et al. 2001), related to high thermal sensitivity because
P. flesus eggs have high levels of mortality in winter water
temperatures above 128C (Cabral et al. 2001, 2007). Thus, in
addition to the lower freshwater inflow, the higher water tem-
peratures in 2005 may have also induced the production
decreases in the Mondego estuary. In line with this result, a
declining trend has been observed for P. flesus in southern
estuaries, which has been related to continuous increases in
seawater temperatures (Cabral et al. 2001; Vinagre et al. 2009a).
In contrast to P. flesus, S. solea production increased in both
estuaries during the drought. In the Mondego estuary, commu-
nity production only increased in 2004–05 owing to the 3-fold
increase of S. solea production. As the food resources for sole,
mainly polychaetes (Dolbeth et al. 2008b), are assumed to be
abundant in both estuaries (Dolbeth et al. 2007a; Sousa et al.
2008a, 2008b), the increased production might be related to the
warmer winter temperatures which could affect spawning
Marine and Freshwater Research 1413
and lead to a higher recruitment in 2005. S. solea growth and
egg production are positively correlated with temperature
(Henderson and Seaby 2005; Vinagre et al. 2008). Local hydro-
dynamic conditions also constrain the larval migration to the
estuary (Vinagre et al. 2008), with lower river flows favouring
the estuarine incursion (Amara et al. 2000). Based on the
temperature tolerances of both species, changes in the composi-
tion of fish assemblages with future temperature rises might
be expected, such as increased S. solea production and decreased
P. flesus production, especially in the Mondego estuary.
The Mondego estuary is characterised by irregular river
discharges, implying that the existing fish assemblage would
be better adapted to variations in the freshwater inflow. Previous
studies showed that the composition and structure of the fish
assemblage changed with varying inflow regimes (Martinho
et al. 2007; Baptista et al. 2010). Despite the higher overall
community production in 2004–05, monthly production of
P. flesus, D. labrax and P. minutus remained low during 2005
and the beginning of 2006, corresponding to the drought period,
which was more prolonged than in the Minho estuary. A
previous study on Mondego estuary fish production including
spring and summer of 2003 confirmed this tendency (Dolbeth
et al. 2008a). Additionally, production likely to be exported to
the coastal stocks of S. solea, P. flesus and D. labrax decreased
considerably during the drought, potentially because of lower
tolerance to temperature and salinity variations, predation or
lowered primary production levels, owing to lower freshwater
inflow (Dolbeth et al. 2007b, 2008a).
Production of P. microps decreased considerably in the
Minho estuary during the drought, whereas in the Mondego
there was a slight increase. This result is not straightforward
to interpret, as P. microps is relatively tolerant to salinity and
temperature variations (Fonds and Van Buurt 1974) and has a
wide spatial distribution in the estuarine system (Dolbeth et al.
2007b; Costa-Dias et al. 2010). Competition between P. minutus
and P. microps in the Mondego estuary may also be among the
reasons for the results obtained, as suggested for other estuaries
(Costa et al. 2002). P. minutus and P. microps compete for food
and space, and the distribution of P. microps is limited by P.
minutus (Costa et al. 2002; Dolbeth et al. 2007b). The decrease
of P. minutus during the drought could mean more food and
habitat available for P. microps, and therefore higher produc-
tion. This hypothesis does not extend to the Minho estuary,
where P. minutus abundance is naturally low. There was a
positive relationship between freshwater inflow and P. microps
production dynamics. However, this correlation was low,
suggesting that other factors might be involved (e.g. nest
availability, sediment characteristics, higher predation). The
difference in the number of recruitment events, as mentioned
previously, also suggests that the populations from the Minho
estuary may be less able to maximise their survivorship during
changing environmental conditions.
Conclusions
The frequency and intensity of climate extremes is expected
to increase in future, so knowledge on their effects on the biota
becomes essential in order to mitigate possible impacts on the
ecosystems and economy. The extreme drought that occurred on
the Iberian Peninsula substantially reduced freshwater inflows
1414 Marine and Freshwater Research
in the studied estuaries. Both estuaries differ considerably in
their hydrological and geomorphologic characteristics and have
different water-management plans. Therefore, it was reasonable
to expect differences in the fish assemblages’ response to
drought. In line with this hypothesis, the fish assemblage in
the Minho estuary declined markedly in production, whereas
the one from the Mondego had an initial increased production
(mostly owing to S. solea), decreasing thereafter. However, the
analysis of the individual fish species dynamics in both estuaries
showed clearly that several species had decreased production
during the drought period. This occurred, for instance, with
P. flesus in the Minho estuary and D. labrax in the Mondego
estuary, which could compromise the coastal adult stocks of
these marine–estuarine-dependent species, especially if extreme
climate events continue to occur as projected by several climate
change scenarios. Additionally, despite the slight latitudinal
differences, the two estuaries differed in their temperature
regimes, which translated into lower growth rates and later
recruitment timing and fewer recruitment events in the Minho
estuary. This might also affect individual species response to the
drought, with longer recruitment periods probably representing
an advantage towards changes in the environment.
Overall, the relationship between the environmental condi-
tions studied and fish production was not high. However, the
variations in fish production were associated with the changes in
freshwater inflow (in this study dependent on the precipitation
regime), either with direct effects (e.g. salinity, turbidity,
temperature) and/or indirect effects (e.g. food supply, larval
immigration to the estuary). This highlights the importance of
appropriate water management plans for transitional waters,
especially if weather-related extremes continue to occur or even
increase in intensity.
Acknowledgements
The authors are indebted to all colleagues who helped in fieldwork. This
work was supported by the FCT (Portuguese Foundation for Science and
Technology) through a grant attributed to M. Dolbeth (SFRH/BPD/41117/
2007). The paper benefited from the comments and suggestions of three
anonymous referees and the editor Dr Andrew Boulton.
References
Amara, R., Lagardere, F., and Desaunay, Y. (2000). Metamorphosis and
estuarine colonisation in the common sole, Solea solea (L.): implications
for recruitment regulation. Oceanologica Acta 23, 469–484. doi:10.1016/
S0399-1784(00)00134-1
Attrill, M. J., and Power, M. (2002). Climatic influence on a marine fish
assemblage. Nature 417, 275–278. doi:10.1038/417275A
Baptista, J., Martinho, F., Dolbeth, M., Viegas, I., Cabral, H., and Pardal, M.
(2010). Effects of freshwater flow on the fish assemblage of
the Mondego estuary (Portugal): comparison between drought and
non-drought years. Marine and Freshwater Research 61, 490–501.
doi:10.1071/MF09174
Bouchereau, J. L., and Guelorget, O. (1998). Comparison of three Gobidae
(Teleostei) life history strategies over their geographical range. Oceano-
logica Acta 21, 503–517. doi:10.1016/S0399-1784(98)80034-0
Brey, T. (2001). ‘Population Dynamics in Benthic Invertebrates. A Virtual
Handbook (Version 01.2).’ Alfred Wegener Institute for Polar and
Marine Research, Germany. Available at http://www.awi-bremerhaven.
de/Benthic/Ecosystem/FoodWeb/Handbook/main.html [Verified 15
March 2010].
M. Dolbeth et al.
Cabral, H. N., Costa, M. J., and Salgado, J. P. (2001). Does the Tagus fish
community reflect environmental changes? Climate Research 18, 119–126.
doi:10.3354/CR018119
Cabral, N. H., Vasconcelos, R. P., Vinagre, C., França, S., Fonseca, V.,
Maia, A., Reis-Santos, P., Lopes, M., Ruano, M., Campos, J., Freitas, V.,
Santos, P. T., and Costa, M. J. (2007). Relative importance of estuarine
flatfish nurseries along the Portuguese coast. Journal of Sea Research
57, 209–217. doi:10.1016/J.SEARES.2006.08.007
Costa, M. J., Cabral, H. N., Drake, P., Economou, A. N., Fernandez-
Delgado, C., Gordo, L., Marchand, J., and Thiel, R. (2002). Recruitment
and production of commercial species in estuaries. In ‘Fishes in
Estuaries’. (Eds M. Elliott and K. Hemingway.) pp. 54–123. (Blackwell
Science: Oxford.)
Costa, M. J., Vasconcelos, R., Costa, J. L., and Cabral, H. N. (2007). River
flow influence on the fish community of the Tagus estuary (Portugal).
Hydrobiologia 587, 113–123. doi:10.1007/S10750-007-0690-X
Costa-Dias, S., Freitas, V., Sousa, R., and Antunes, C. (2010). Factors
influencing epibenthic assemblages in the Minho Estuary (NW Iberian
Peninsula). Marine Pollution Bulletin 61, 240–246. doi:10.1016/
J.MARPOLBUL.2010.02.020
Cowley, P. D., and Whitfield, A. K. (2002). Biomass and production
estimates of a fish community in a small South African estuary. Journal
of Fish Biology 61, 74–89. doi:10.1111/J.1095-8649.2002.TB01763.X
Dolbeth, M., Cardoso, P. G., Ferreira, S. M., Verdelhos, T., Raffaelli, D., and
Pardal, M. A. (2007a). Anthropogenic and natural disturbance effects
on a macrobenthic estuarine community over a 10-year period. Marine
Pollution Bulletin 54, 576–585. doi:10.1016/J.MARPOLBUL.2006.
12.005
Dolbeth, M., Martinho, F., Leitão, R., Cabral, H. N., and Pardal, M. A.
(2007b). Strategies of Pomatoschistus minutus and Pomatoschistus
microps to cope with environmental instability. Estuarine, Coastal and
Shelf Science 74, 263–273. doi:10.1016/J.ECSS.2007.04.016
Dolbeth, M., Martinho, F., Viegas, I., Cabral, H., and Pardal, M. A. (2008a).
Estuarine production of resident and nursery fish species: conditioning
by drought events? Estuarine, Coastal and Shelf Science 78, 51–60.
doi:10.1016/J.ECSS.2007.11.021
Dolbeth, M., Martinho, F., Leitão, R., Cabral, H., and Pardal, M. A. (2008b).
Feeding patterns of the dominant benthic and demersal fish community
in a temperate estuary. Journal of Fish Biology 72, 2500–2517.
doi:10.1111/J.1095-8649.2008.01856.X
Elliott, M., and Taylor, C. J. L. (1989). The structure and functioning of
an estuarine/marine fish community in the Forth Estuary, Scotland. In
‘Proceedings of the 21st European Marine Biology Symposium’. (Eds R.
Z. Klekowsky, E. Styczynska-Jurewicz and J. Falkowsky.) p. 639.
(Polish Academy of Sciences and Institute of Oceanology Gdansk:
Gdansk.)
Elliott, M., Whitfield, A. K., Potter, I. C., Blaber, S. J. M., Cyrus, D. P.,
Nordlie, F. G., and Harrison, T. D. (2007). The guild approach to
categorizing estuarine fish assemblages: a global review. Fish and
Fisheries 8, 241–268. doi:10.1111/J.1467-2679.2007.00253.X
Fonds, M., and Van Buurt, G. (1974). The influence of temperate and salinity
on development and survival of goby eggs (Pisces, Gobiidae). Hydro-
logical Bulletin 8, 110–116. doi:10.1007/BF02254911
Fonseca, V. F., and Cabral, H. N. (2007). Are fish early growth and condition
patterns related to life-history strategies? Reviews in Fish Biology and
Fisheries 17, 545–564. doi:10.1007/S11160-007-9054-X
Fouda, M. M., and Miller, P. J. (1981). Age and growth of the common
goby, Pomatoschistus microps on the south coast of England. Estuarine,
Coastal and Shelf Science 12, 121–129. doi:10.1016/S0302-3524(81)
80091-6
França, S., Costa, M. C., and Cabral, H. C. (2009). Assessing habitat specific
fish assemblages in estuaries along the Portuguese coast. Estuarine,
Coastal and Shelf Science 83, 1–12. doi:10.1016/J.ECSS.2009.
03.013
 Drought effects on fishes from Iberian estuaries
Freitas, V., Costa-Dias, S., Campos, J., Bio, A., Santos, P., and Antunes, C.
(2009). Patterns in abundance and distribution of juvenile flounder,
Platichthys flesus, in Minho estuary (NW Iberian Penı́nsula). Aquatic
Ecology 43, 1143–1153. doi:10.1007/S10452-009-9237-8
Gayanilo, F. C., Jr., Sparre, P., and Pauly, D. (2005). ‘FAO-ICLARM Stock
Assessment Tools II (FiSAT II). User’s Guide. FAO Computerized
Information Series (Fisheries).’ No. 8, Revised version. (Food and
Agriculture Organisation: Rome.)
Gillson, J., Scandol, J., and Suthers, I. (2009). Estuarine gillnet fishery catch
rates decline during drought in eastern Australia. Fisheries Research 99,
26–37. doi:10.1016/J.FISHRES.2009.04.007
Hemingway, K. L., and Elliott, M. (2002). Field methods. In ‘Fishes in
Estuaries’. (Eds M. Elliott and K. Hemingway.) pp. 410–509. (Blackwell
Science: Oxford.)
Henderson, P. A., and Seaby, R. M. (2005). The role of climate in
determining the temporal variation in abundance, recruitment and
growth of sole Solea solea in the Bristol Channel. Journal of the
Marine Biological Association of the United Kingdom 85, 197–204.
doi:10.1017/S0025315405011069H
Hostens, K., and Hamerlynck, O. (1994). The motile epifauna of the soft
bottoms in the subtidal Oosterschelde estuary: structure, function and
impact of storm-surge barrier. Hydrobiologia 282/283, 479–496.
Houde, E. D., and Rutherford, E. S. (1993). Recent trends in estuarine
fisheries: prediction of fish production and yield. Estuaries 16, 161–176.
doi:10.2307/1352488
Intergovernmental Panel on Climate Change (2007). Climate Change 2007:
The Physical Science Basis. Contribution of Working Group I to the
Fourth Assessment. Report of the Intergovernmental Panel on Climate
Change. (Cambridge University Press: Cambridge, UK.)
Kottek, M., Grieser, J., Beck, C., Rudolf, B., and Rubel, F. (2006). World
map of the Koppen-Geiger climate classification updated. Meteorolo-
gische Zeitschrift 15, 259–263. doi:10.1127/0941-2948/2006/0130
Martı́nez, M. L., Intralawan, A., Vázquez, G., Pérez-Maqueo, O., Sutton, P.,
and Landgrave, R. (2007). The coasts of our world: ecological, economic
and social importance. Ecological Economics 63, 254–272. doi:10.1016/
J.ECOLECON.2006.10.022
Martinho, F., Leitão, R., Viegas, I., Dolbeth, M., Neto, J., Cabral, H. N.,
and Pardal, M. A. (2007). The influence of an extreme drought event in
the fish community of a southern Europe temperate estuary. Estuarine,
Coastal and Shelf Science 75, 537–546. doi:10.1016/J.ECSS.2007.
05.040
Martinho, F., Dolbeth, M., Viegas, I., Teixeira, C. M., Cabral, H. N., and
Pardal, M. A. (2009). Environmental effects on the recruitment varia-
bility of nursery species. Estuarine, Coastal and Shelf Science 83,
460–468. doi:10.1016/J.ECSS.2009.04.024
Pampoulie, C., Chauvelon, P., Rosecchi, E., Bouchereau, J., and Crivelli, A.
(2001). Environmental factors influencing the gobiid assemblage of a
Mediterranean lagoon: Empirical evidence from a long-term study.
Hydrobiologia 445, 175–181. doi:10.1023/A:1017565715463
Pihl, L. (1989). Abundance, biomass and production of juvenile flatfish in
southeastern Kattegat. Netherlands Journal of Sea Research 24, 69–81.
doi:10.1016/0077-7579(89)90171-3
Pihl, L., and Rosenberg, R. (1982). Production, abundance and biomass
of motile epibenthic marine fauna in shallow waters, western Sweden.
Journal of Experimental Marine Biology and Ecology 57, 273–301.
doi:10.1016/0022-0981(82)90197-6
Pombo, L., Rebelo, J. E., and Elliott, M. (2007). The structure, diversity and
somatic production of the fish community in an estuarine coastal lagoon,
Ria de Aveiro (Portugal). Hydrobiologia 587, 253–268. doi:10.1007/
S10750-007-0687-5
Ribeiro, J., Bentes, L., Coelho, R., Gonçalves, J. M. S., Lino, P. G., Monteiro,
P., and Erzini, K. (2006). Seasonal, tidal and diurnal changes in fish
assemblages in the Ria Formosa lagoon (Portugal). Estuarine, Coastal
and Shelf Science 67, 461–474. doi:10.1016/J.ECSS.2005.11.036
http://www.publish.csiro.au/journals/mfr
View publication stats
Marine and Freshwater Research 1415
Rotherham, D., Gray, C., Johnson, D., and Lokys, P. (2008). Effects of
diel period and tow duration on estuarine fauna sampled with a beam
trawl over bare sediment: Consequences for designing more reliable and
efficient surveys. Estuarine, Coastal and Shelf Science 78, 179–189.
doi:10.1016/J.ECSS.2007.11.019
Salen-Picard, C., Darnaude, A., Arlhac, D., and Harmelin-Vivien, M.
(2002). Fluctuations of macrobenthic populations: a link between
climate-driven river run-off and sole fishery yields in the Gulf of Lions.
Oecologia 133, 380–388. doi:10.1007/S00442-002-1032-3
Schlacher, T. A., Skillington, A. J., Connolly, R. M., Robinson, W., and
Gaston, T. F. (2008). Coupling between marine plankton and freshwater
flow in the plumes off a small estuary. International Review of Hydro-
biology 93, 641–658. doi:10.1002/IROH.200711050
Sousa, R., Dias, S., Freitas, V., and Antunes, C. (2008a). Subtidal macro-
zoobenthic assemblages along the River Minho estuarine gradient (north-
west Iberian Peninsula). Aquatic Conservation: Marine and Freshwater
Ecosystems 18, 1063–1077. doi:10.1002/AQC.871
Sousa, R., Dias, S., Guilhermino, L., and Antunes, C. (2008b). Minho River
tidal freshwater wetlands: threats to faunal biodiversity. Aquatic Biology
3, 237–250. doi:10.3354/AB00077
Svensson, C. J., Hyndes, G. A., and Lavery, P. S. (2007). Food web analysis
in two permanently open temperate estuaries: consequences of saltmarsh
loss? Marine Environmental Research 64, 286–304. doi:10.1016/
J.MARENVRES.2007.02.002
Teixeira, C. M., and Cabral, H. N. (2009). Time series analysis of flatfish
landings in the Portuguese coast. Fisheries Research 96, 252–258.
doi:10.1016/J.FISHRES.2008.12.004
Teixeira, H., Salas, F., Borja, A., Neto, J. M., and Marques, J. C. (2008).
A benthic perspective in assessing the ecological status of estuaries:
the case of the Mondego estuary (Portugal). Ecological Indicators 8,
404–416. doi:10.1016/J.ECOLIND.2007.02.008
Ter Braak, C. J. F., and Smilaeur, P. (1998). ‘CANOCO Reference Manual
and User’s Guide to CANOCO for Windows: Software for Canonical
Community Ordination (Version 4).’ (Microcomputer Power: Ithaca.)
Vasconcelos, R. P., Reis-Santos, P., Tanner, S., Maia, A., and Latkoczy, C.
(2008). Evidence of estuarine nursery origin of five coastal fish species
along the Portuguese coast through otolith elemental fingerprints.
Estuarine, Coastal and Shelf Science 79, 317–327. doi:10.1016/J.ECSS.
2008.04.006
Vinagre, C., Costa, M. J., and Cabral, H. N. (2007). Impact of climate
and hydrodynamics on sole larval immigration towards the Tagus
estuary, Portugal. Estuarine, Coastal and Shelf Science 75, 516–524.
doi:10.1016/J.ECSS.2007.05.035
Vinagre, C., Amara, R., Maia, A., and Cabral, H. N. (2008). Latitudinal
comparison of spawning season and growth of 0-group sole, Solea solea
(L.). Estuarine, Coastal and Shelf Science 78, 521–528. doi:10.1016/
J.ECSS.2008.01.012
Vinagre, C., Santos, F. D., Cabral, H. N., and Costa, M. J. (2009a). Impact of
climate and hydrology on juvenile fish recruitment towards estuarine
nursery grounds in the context of climate change. Estuarine, Coastal and
Shelf Science 85, 479–486. doi:10.1016/J.ECSS.2009.09.013
Vinagre, C., Ferreira, T., Matos, L., Costa, M. J., and Cabral, H. N. (2009b).
Latitudinal gradients in growth and spawning of sea bass, Dicentrarchus
labrax, and their relationship with temperature and photoperiod. Estuar-
ine, Coastal and Shelf Science 81, 375–380. doi:10.1016/J.ECSS.2008.
11.015
Whitfield, A. (2005). Fishes and freshwater in southern African estuaries –
A review. Aquatic Living Resources 18, 275–289. doi:10.1051/ALR:
2005032
Winberg, G. G. (1971). ‘Methods for the Estimation of Production of
Aquatic Animals.’ (Academic Press: London.)
Manuscript received 4 January 2010, accepted 6 August 2010