Springer 2006

Hydrobiologia (2006) 559:135148

DOI 10.1007/s10750-005-1371-2

Primary Research Paper

Spatial subtidal macrobenthic distribution in relation to abiotic conditions

in the Lima estuary, NW of Portugal
Ronaldo Sousa1,2,*, Sergia Dias1 & Jose Carlos Antunes1
1

CIIMAR Centro Interdisciplinar de Investigacao Marinha e Ambiental, Rua dos Bragas, 123, 4050-123, Porto,
Portugal
2
ICBAS Instituto de Ciencias Biomedicas de Abel Salazar, Universidade do Porto, Lg. Prof. Abel Salazar 2, 4099-003,
Porto, Portugal
(*Author for correspondence: E-mail: ronaldo.sousa@cimar.org)
Received 5 May 2005; in revised form 27 July 2005; accepted 31 July 2005

Key words: Lima estuary, macrobenthic assemblages, abundance, biomass, diversity, environmental factors

Abstract
During the summer of 2002, sampling was carried out in the Lima estuary in order to compare the pattern
of the macrobenthic communitys distribution in relation to physical and chemical variables. A total of 54
macrobenthic taxa were identied. Abundance, biomass and specic diversity varied among the twenty
stations. Abundance ranged from 212 to 9856 ind./m2, with an average of 1581 ind./m2. Abra alba presented the highest density corresponding to 39.1% of the total specimens gathered, followed by Hediste
diversicolor with 31.5%. Biomass ranged from 0.12 to 264.62 g AFDW/m2, with an average of 17.58 g
AFDW/m2. Cerastoderma edule and A. alba were the species with a clear predominance in the total
biomass, contributing 75.3 and 13.8%, respectively. The multivariate techniques used revealed a macrobenthic community with ve distinct groups, particularly related to the sedimentological characteristics and
salinity. These results demonstrated signicant dierences in macrobenthic assemblages composition along
an estuarine gradient. For the rst time the presence of the nonindigenous invasive species Corbicula
uminea was described in this estuary.

Introduction
Estuaries are normally recognized as transitional
areas of distinct biological importance, where
salinity varies between fresh water and seawater
(McLusky, 1989; Little, 2000). These estuarine
areas are used temporarily as a nursery ground for
many commercially and ecologically important
species of marine and migrating shes, shellsh,
crustaceans and shorebirds (Day et al., 1989;
Raaelli, 1999).
At the same time these productive and complex
estuarine ecosystems are frequently located near
large cities and are receptacle of all types of contaminants (Allchin et al., 1999; Baudrimont et al.,

2005; Cave et al., 2005; Cheggour et al., 2005). The

Lima estuary is not an exception, and it is also
subject to various impacts (mainly in the lower part
of the estuary) from harbour activity, constant
dredging in the rst 3 km, discharge of nutrients and
other substances deriving from domestic, industrial
and agricultural areas. These types of activities are
responsible for modications in the bathymetry
with a consequential hydrodynamic change and
also for the increasing eutrophication processes in
this estuarine system (Alves, 1996; Sousa, 2003).
The understanding of the macrobenthic estuarine species distribution relative to their habitat is
fundamental to the development of estuarine
ecology (Ysebaert et al., 2003). In addition, the

136
benthic macroinvertebrates are one of the most
useful bioindicators of possible environmental
changes (Warwick et al., 2002; Ysebaert et al.,
2002). Since there is a complete lack of quantitative data on the relationship between spatial distribution of macrobenthic assemblages and
environmental variables in the Lima estuary reference work was carried out, during the summer of
2002, on the subtidal area. The objectives of this
work were to compare the pattern of the macrobenthic communitys distribution in relation to
physical and chemical variables, to estimate the
abundance and biomass of subtidal macrozoobenthos and to identify possible key species in the
functioning of the ecosystem.

Materials and methods

Study area
The River Lima originates in Serra de Sao Mamede, in the province of OrenseSpain, at about
950 m altitude. It is 108 km long, of which 67 km
are located in Portuguese territory and drains
ENEWSW into the Atlantic Ocean. Its hydrological basin is located between 41 35 N and
42 15 N of latitude and 07 35 W and 08 55 W
of longitude, with an area of 2480 km2, 1303 km2
in Spain (53%) and 1177 km2 in Portugal (47%).
The estuary is located in the NW of Portugal
(Fig. 1) and the inuence of spring tides extends
approximately 20 km upstream. The Lima estuary
has a maximum width of just over 1 km, being

signicantly larger with the ooding of the banks

during high tide. This mesotidal estuary is partially
mixed, however, during the period of high oods it
tends to evolve towards a salt wedge estuary
(Alves, 1996). This estuarine ecosystem includes
biotypes with mobile and rocky substrata,
favourable to the occurrence of various types of
organisms. Rocky substrata are, essentially, represented by sea walls in the lower part of the
estuary. Biotypes with mobile substrata occur in
intertidal and subtidal areas and comprise areas
close to the riverbanks, inlets which form small
bays and as marsh existing on the various islands
found in the lower part of the estuary and on the
north bank (Sousa, 2003). The few biological
studies carried out in this estuary (performed in
the 1980s and the beginning of the 1990s) described the ecology of some species and characterized the main physical and chemical, biological
and human processes which modify the structure
and dynamic of the biological communities (Fontoura, 1984; Fontoura & Moura, 1984; Guimaraes
& Galhano 1987, 1988, 1989; Valente & Alexandrino, 1988; Da Silva, 1990; Coelho, 1997).
Sampling and laboratory analysis
Samples were collected in the summer of 2002 in
the subtidal areas of the Lima estuary at high tide
(Fig. 1). Six replicates per sampling station (one
for sediment analysis and ve for biological analysis) were gathered with a Van Veen grab with an
area of 500 cm2 and a maximum capacity of
5000 cm3.

Figure 1. Map of the Lima estuary showing location of the twenty sampling stations.

137
During eldwork, the following water column
information was collected: temperature, salinity,
dissolved oxygen and pH. This information was
obtained in situ, close to the bottom, using a
multiparametrical sea gauge YSI 820. Particle size
and organic content analyses of the sediment at
every station were carried out. Sediment granulometry was assessed following drying at 60 C for
72 h. Dried sediment was sieved through a column
of sieves corresponding to integer values of the
Wentworth scale and the frequency of each class
was expressed as the percentage of total weight.
The quantity of organic matter contained in the
sediment was determined, after combusting for
24 h at 550 C, in a mue furnace. Values are
expressed in percentage, relatively to the weight
loss on ignition of each sample analysed.
Grab samples were sieved on a 1 mm mesh and
xed with 4% formalin in seawater. Macrofauna
was sorted and, whenever possible, identied to
species level. Biomass was calculated using the Ash
Free Dry Weight Method AFDW (Kramer et al.,
1994).

Data analysis
To compare the similarity between stations (data
pooled over ve biological replicates for each site)
in terms of species composition (abundance and
biomass), univariate measures and multivariate
analyses were applied using the PRIMER package
(Clarke & Warwick, 2001). Univariate measures
included abundance, biomass, number of species,
and diversity (H) and evenness (J) indices. Classication (CLUSTER) and ordination by nonmetric multidimensional scaling (MDS) based on
the BrayCurtis similarity matrix were used to
analyse spatial distribution of benthic assemblages.
In order to establish correlations between biological parameters and abiotic characteristics, indeces of biotic and abiotic similarity were
compared using PCA (Principal Components
Analysis) and BIOENV (using the Spearman
coecient) (Clarke & Ainsworth, 1993).
Biological information was previously transformed (square root transformation; abundance
per unit of area), however, for the abiotic factors
only granulometry and the percentage of organic
matter were transformed )log(1+y).

Results
The physical and chemical parameters are presented in Table 1. The water temperature was
higher in upstream stations and ranged between
17.8 C (station 18) and 13.2 C (stations 5 and 6).
Salinity values varied signicantly with the distance to the river mouth, with the highest value
recorded in station 1 (34.8 psu) and the lowest in
station 20 (0.4 psu). The dissolved oxygen values
varied between 3.7 mg/l (station 14) and 7.8 mg/l
(station 10) and the pH values between 7.0 (station
6) and 8.2 (stations 13 and 14). There was a large
variation in the cumulative curves of distribution
of the sediment throughout the dierent sampling
stations. The stations located in the river mouth
(stations 1, 2, 3 and 4) contained abundant ne
matter and the other stations, located upstream,
contained coarser sediment with a preponderance
of sands and gravels. Organic matter in the sediment ranged from 0.5% (station 19) to 10.8%
(station 3). There were large spatial variations,
related to the type of substrate existent in the
dierent sampling stations and a signicant correlation (r=0.98, p<0.001) between ner sediment
(silt and clay) and organic matter was found.
A total of 7750 individuals corresponding to 54
macrobenthic species were found (Appendix 1).
These species belong to 7 Phyla: Annelida 17,
Mollusca 20, Arthropoda 10, Nemertini 3,
Echinodermata 2, Cnidaria 1 and Spinculida 1.
Abundance per station ranged from 212 ind./
m2 in station 17 to 9856 ind./m2 in station 2 with
an average of 1581 ind./m2 (Table 2 and Appendix
1). Macrofauna abundance was distributed among
Mollusca (56.1%), Annelida (38.8%), Crustaceans
(4.9%) and other faunal groups (0.2%). Abra alba
was the species that presented the greatest number
of individuals per unit of area, which corresponded to 39.1% of the total number of individuals gathered. Hediste diversicolor was the
second most abundant species with 31.5%.
The number of species (Table 2) also had considerable spatial variation. The maximum value of
20 species was registered in station 2 and the
minimum, with only one species, in stations 14, 15
and 17. The ShannonWiener index (Table 2)
values were low with the maximum value at station
1 (H=1.96) and the minimum at stations 14, 15
and 17 (H=0.00). Pielous evenness varied widely

138
Table 1. Physical and chemical parameters of water and sediments
Station T(C) S(psu) DO(mg/l) pH OM(%) G(%) VCS(%) CS(%) MS(%) FS(%) VFS(%) S+C(%) D (m) DST(km)
1

13.5

34.8

6.4

7.6

2.9

0.1

0.1

12.6

27.1

52.1

13.9

33.9

6.4

7.4

8.9

0.6

1.2

5.1

12.3

43.3

33.5

10

0.3

3
4

13.9
14

34.1
33.9

6.2
6.1

7.6 10.8
7.7 7.5

2.4
0.2

1.4
1.2

5.6
5.2

13.4
13.9

17.5
32.6

26.8
27.5

32.9
19.4

10
9

1
1.5

13.2

33.4

5.2

7.4

0.9

27.2

22.9

13.3

9.8

0.5

0.3

2.8

13.2

33.5

6.8

4.3

4.2

14.4

24.1

18.8

23.2

10.6

4.7

13.3

32.4

6.9

7.4

1.9

17.9

19.4

21.3

22.5

15.5

1.6

1.8

13.5

32.2

7.2

7.3

2.2

12.5

33.6

31.8

13.1

2.9

3.6

2.5

14.3

32.3

7.4

7.4

38.4

32.6

18.9

8.6

0.9

0.3

0.3

10

14.3

32.8

7.8

7.5

1.9

21.4

32.6

34.7

8.2

1.2

0.9

11
12

17
14.2

22.9
32.4

5.8
5.4

7.5
7.5

0.8
1

58.9
58.2

17.9
22.4

14.3
16

7.7
2.8

1
0.2

0.1
0.2

0.1
0.2

2
5

7
8

13

15.3

28.9

4.9

8.2

0.7

51.3

28.4

17

2.9

0.2

0.1

0.1

9.5

14

14.7

27.5

3.7

8.2

0.8

19.3

45.1

30.2

4.9

0.3

0.1

0.1

10.5

15

15.2

24.7

3.9

8.1

0.6

66.7

18.4

11.4

3.2

0.1

0.1

0.1

10

12.5

16

17.3

7.4

4.6

2.5

9.1

19.4

36.2

22.2

7.1

3.9

2.1

13.5

17

17.4

4.8

1.9

15.5

18.2

22.9

31.7

7.5

2.8

1.4

14

18

17.8

2.4

5.1

0.6

29.2

35.8

29.3

4.4

0.8

0.4

0.1

14.5

19
20

17.4
17.2

1.1
0.4

5.2
4.7

8.1
8.1

0.5
0.7

54.6
50.5

28.4
19.4

13
16.7

3.8
11.3

0.1
1.9

0.1
0.1

0
0.1

2
3

15
16

26

Temperature (T C), salinity (S psu), dissolved oxygen (DO mg/l), pH, organic matter (OM %), gravel (G %), very coarse sand
(VCS %), coarse sand (CS %), medium sand (MS %), ne sand (FS %), very ne sand (VFS %) and silt+clay (S+C %).
The depth (D m) and distance to the ocean (DST km) of the twenty sampling stations are also given.

among stations (Table 2) with the maximum value

recorded in station 18 (J=0.81) and the minimum
in stations 14, 15 and 17 (J=0.00).
Biomass (Table 2 and Appendix 2) also varied
considerably, having an average value per unit
area of 17.58 g AFDW/m2. Biomass ranged from
0.12 g AFDW/m2 in station 17 to 264.62 g
AFDW/m2 in station 7. It should be pointed out
that the high biomass registered in station 7 was
related to high densities of Cerastoderma edule.
Mollusca (93.4%) presented the highest values,
with a clear domination in the total biomass by C.
edule (75.3%) and A. alba (13.8%). Ignoring the
contribution of C. edule present in the station 7, we
veried that the macrobenthic biomass was dominated by Mollusca (72.2%) and Annelida
(18.4%), with the predominance of A. alba
(53.8%), H. diversicolor (10.8%) and Corbicula
uminea (5.9%).
Figure 2 displays the results of the CLUSTER
analysis and the two-dimensional MDS plot of
samples based on the abundance is shown in

Figure 3. Essentially, the biological community in

the Lima estuary includes ve groups and these
faunal groups are well separate in the MDS
ordering and are distinct (the stress level is very
low). The stations represented by group A (stations 1, 2, 3 and 4) occurred in areas with ne
deposits, where dredging is carried out. These
deeper stations have more inuence of the adjacent marine areas and so this group is colonized
by some marine species, such as Atelecyclus rotundatus, Diogenes pugilator, Nucula nucleus and
Amphipholis squamata. These stations were dominated by the bivalve A. alba in abundance and
biomass. Group B (station 5) occurred in coarser
deposits than stations of group A, and was also
dominated by species derived from adjacent
marine areas such as Nephtys cirrosa and Glycera
convuluta known to occur in well oxygenated
clean, sandy bottoms with strong tidal currents.
The stations represented by group C (stations 6, 7
and 8) were located in shallow areas with coarse
sediment and the dominant species in these sta-

139
Table 2. Abundance (A ind./m2), biomass (B g AFDW/m2),
number of species (S), evenness (J) and Shannon/Wiener index
(H) at the stations sampled
Station

420

1.55

13

0.76

1.96

9856

24.53

20

0.21

0.62

1112

8.14

18

0.39

1.13

3265

28.31

0.14

0.27

360

2.13

0.52

1.14

628

0.70

15

0.68

1.85

7
8

3124
1196

264.62
3.58

8
14

0.39
0.35

0.81
0.93

2632

4.76

0.20

0.39

10

2268

2.46

0.19

0.34

11

888

0.73

0.21

0.34

12

1628

1.23

0.17

0.12

13

568

0.37

0.19

0.13

14

516

0.27

0.00

0.00

15
16

900
304

0.24
1.58

1
4

0.00
0.53

0.00
0.74

17

212

0.12

0.00

0.00

18

632

0.44

0.81

0.56

19

444

5.55

0.22

0.16

20

664

0.30

0.09

0.07

tions were Capitella capitata, Scrobicularia plana

and C. edule. The stations represented by group
D (stations 9, 10, 11, 12, 13, 14, 15, 16, 17 and 18)
were located in areas with coarse sediments and
the dominant and almost exclusive species in
these stations was H. diversicolor. The stations

Figure 3. MDS plot of faunal similarity among the twenty

sampling stations present in the Lima estuary.

represented by group E (stations 19 and 20) were

located in the upper part of the estuary in transition with zones of uvial characteristics, have
coarse sediments and are dominated by Corophium multisetosum.
The PCA matrices of physical and chemical
factors versus stations (Fig. 4) reveal a clear pattern present in the estuary. From the projection
against the rst axis of variability, stations appear
distributed along a physical and chemical gradient,
with the stations with ner sediments along one
edge and the stations with coarser sediments located on the other. Along the second axis of variability, the separation of the stations was related
to the abiotic factors measured in the water
column. The results of the BIOENV analysis
(Table 3) indicated that the best correlation always

Figure 2. A dendogram of the twenty sampling stations present in the Lima estuary.

140

Figure 4. Analysis of physical and chemical factors of water

column and sediment from PCA of factorsstation matrices.
The percentage of variability explained by the principal axis is
given.

occurred with variables related with sediment

characteristics and salinity.

Discussion
The summer temperature values registered in the
Lima estuary increased from the river mouth to
the upstream areas. The stations near the river
mouth are subjected to a great inuence of adjacent marine water, which have lower values than
the water from uvial inux. The upper shallow
stations present higher temperature values due to
atmospheric inuence. Salinity decreased from the
river mouth to upstream areas due to the dilution
of marine water with fresh water derived from
uvial inux. The spatial uctuations of the dissolved oxygen and pH values were never large
(extreme values were never recorded) and the
macrobenthic assemblages present in the estuary
are presumably tolerant to the amplitudes occurTable 3. Summary of results from BIOENV analysis
k

Best variable combination

0.545 Silt+Clay

0.459 Very ne sand

0.703 Salinity

0.681 Salinity

Very ne sand
3

0.731 Salinity

Silt+Clay
0.710 Salinity

Fine sand

Very coarse sand

Silt+Clay

Fine sand

Combination of variables (k) giving the highest correlation

(using the Spearman rank correlation) between biotic and
environmental matrices are shown.

ring in these abiotic parameters. There were no

signicant temporal changes concerning sediment
characteristics in the study area when we compare
our data with the results obtained by Alves (1996).
However, the sediment composition of the stations
1, 2, 3 and 4 can be signicantly inuenced by
human activities in this area, which include urban
and industrial euents, local eutrophication and
periodic dredgings with a possible increase of ne
material.
The multivariate analyses used in this study
identied a faunal gradient correlated with the
dierent types of sediment and salinity, which are
not independent of the inuence of the hydrodynamic conditions. Within estuaries, sediment
composition and salinity are abiotic factors that
can inuence benthic community distribution
(Attrill et al., 1996; Mannino & Montagna, 1997)
because these abiotic parameters can aect the
ecology and physical and chemical characteristics
of estuaries. There are strong salinity and sediment
gradients in the Lima estuary, correlating with
variations in abundance, biomass and species
diversity.
We found higher values of abundance and
biomass in the lower Lima estuary when compared
with the upper estuary. This correlates with the
presence of ner estuarine sediments favourable to
opportunistic colonization of species with high
population densities (stations 2, 3 and 4) and with
the stability of hydrological factors, namely
salinity. The mouth of the estuary is also richer in
organic matter when compared with upper estuarine stations, which results in a great quantity of
potential food resources in the mouth of the
estuary, principally, for deposit-feeding species.
The great abundance and biomass presented by A.
alba in these stations is in agreement with the
description of Skei et al. (1996), who found dense
assemblages of this bivalve in areas with high
organic loads.
The lower part of the estuary contains high
diversity, perhaps due to the greater heterogeneity
of the types of habitats available and the constancy
of the abiotic factors. This greater heterogeneity
provides a higher number of habitats able to shelter
a greater diversity, since sediment granulometry is
a determining factor in the distribution of the
macrobenthic species (Warwick et al., 1991; Meire
et al., 1994; Bachelet et al., 1996). The relative

141
stability of salinity in the lower part of the Lima
estuary may also be responsible for the larger
diversity present, because this area can be easily
colonized by species originating from adjacent
marine areas. There are various examples of marine
species, which generally colonize the lower part of
the estuary: G. convuluta, A. rotundatus, D. pugilator, N. nucleus and A. squamata, amongst others.
These species were present mainly in the river
mouth areas and in the relative deep navigation
channels, where the inuence of the tide is strongest. The decreased diversity in the middle and
upstream areas may be related to the type of habitats available and with environmental stress. The
middle and upper areas of the Lima estuary are
characterized by habitats with clean, coarse sand
and high degree of instability caused by natural
processes (mainly large uctuations of salinity,
high current velocities and high turbidity), resulting in a lower diversity of benthic macroinvertebrates (Marchand & Gascuel, 1988; Attrill et al.,
1996). Furthermore, the middle and upper estuarine areas are poor in phytoplankton (Da Silva,
1990) and organic matter when compared to lower
stations. According to Herman et al. (1999), the
food availability may be a limiting factor for benthic abundances and biomass in estuarine benthic
systems. At the same time, the salinity gradient acts
as a physiological barrier for stenohaline marine
and freshwater species and places environmental
stress on euryhaline organisms (Mannino &
Montagna, 1997) and so great uctuations of
salinity, principally, in the middle estuary can result in a reduction of the number of species.
This kind of macrobenthic distribution, with a
clear dierence in assemblages composition,
abundance and biomass along an estuarine gradient is in conformity with several studies done in
other estuaries and coastal lagoons (Marques
et al., 1993; Mannino & Montagna, 1997; Ysebaert et al. 2002, 2003; Nanami et al., 2005). Other
factors may be responsible for the abundance,
biomass and species diversity observed in the Lima
estuary such as predation, competition, adult-larval interactions and other abiotic factors not
measured in this study. Eects of predation,
competition and adult-larval interactions have
been demonstrated only in dense assemblages of
benthos (Wilson, 1984). They probably are less
important than the abiotic factors in sparse ben-

thic assemblages such as we have in this estuary.

The Lima estuary, with moderate densities, may be
inuenced further by recruitment or the abiotic
factors than by density-dependent variables. Possible exceptions were the stations present in lower
part of the estuary (stations 2, 3 and 4), with large
abundances and biomass of A. alba and station 7
with large abundance and biomass of C. edule.
In contrast with several studies that reported a
complete disappearance of the benthic fauna as a
result of dredging activities (Johnston, 1981; Newell et al., 1998), in this estuarine system a well
developed but unstable assemblage in the dredged
area was found (stations 1, 2, 3 and 4). This situation could be related to the small volume dredged
that permits the presence of monticules of transitory nature, which can be determinant in the
maintenance of the community structure. In fact,
dredging by suction, as done in the Lima estuary,
left intact some monticules that will be important
for the subsequent repopulation. This repopulation
can result from the migration of adults, reproduction and recruitment of the larva from undisturbed
areas or from the existing population found in intact monticules (Hall, 1994; Lu & Wu, 2000).
The presence of C. uminea, in upper estuarine
areas, should be pointed out because this is the rst
time that this species has been recorded in this
estuary. C. uminea is widely recognized as a nonindigenous invader that may have great ecologic
repercussions in the native species and environmental processes (Phelps, 1994; Cataldo & Boltovskoy, 1999; Darrigan, 2002). At this moment, their
abundance, biomass and distribution remain unchanged (Sousa, personal communication).
In conclusion, due to the concentrations of
human activities in the Lima estuary, mainly in the
lower part, this estuarine area has a higher probability of being exposed to nutrient enrichment, oil
pollution, dissemination of heavy metals and
dredging activities. Further experimental work is
required to develop our ecological understanding
of the macrobenthic system present in the Lima
estuary. It is essential to have additional knowledge of the natural spatial and temporal variability
of the benthic communities present in this estuary
since this will help us deduce the changes that may
occur due to man-induced modications and
subsequent readjustment of the communities. The
higher abundances and biomass presented by

142
A. alba, H. diversicolor and C. edule suggest that
these species play a key role in the Lima estuary
and possibly serve as important food resources to
the other trophic levels.
Acknowledgements
Special thanks are addressed to Eduardo, Jonathan Wilson, Jose Calvario and Miguel Pardal.

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Actinidae

Sp2
Sp3

3
4

Sp

Sp

Euclymene lumbricoides (Quatrefages, 1865) 48 128

Exogone verugera (Clapare`de, 1868)
24 x

Glycera convoluta (Keferstein, 1862)

Hediste diversicolor (Muller, 1776)

Heteromastus liformis (Clapare`de, 1864)

Maldane sarsi (Malmgren, 1865)

Melinna palmata (Grube, 1870)

Nephtys cirrosa (Ehlers, 1868)

Nephtys hombergi (Savigny, 1818)

Pectinaria koreni (Malmgren, 1866)

Phyllodoce maculata (Linnaeus, 1767)

11

13

14
15

16

17

18

19

20

21

Abra alba (Wood, 1802)

Cerastoderma edule (Linnaeus, 1758)

Corbicula uminea (Muller, 1774)

23

24

25

Bivalvia

22
Streblospio shrubsolii (Buchanan, 1890)
Mollusca

12

Eteone picta (Quatrefages, 1865)

x
4

28

72

16

x
x

x
x

S4

16

x
x

60

x
x

15

220 x

x
x

S3

x
x

x
8

28

x
x

S6

96
x

16

x
x

S7

84

24

x
x

S9

28

20
x

40

x
x

S10

x
24

x
x

S11 S12

x
x

x
x

x
x

x
x

x
x

x
x

x
x

32

20

16

x
x

x
x

S13 S14 S15 S16 S17 S18 S19 S20

2420 2116 824 1588 552 516 900 224 212 476 x
x
x
x
x
x
x
x
x
x
x
x

944 4

12

x
x

S8

2180 24

192 x

232 x

x
x

x
x

S5

40 8444 760 3105 x

x
x

44 20

Eteone longa (Fabricius, 1780)

10

x
x

Capitella capitata (Fabricius, 1780)

4
x

x
x

S1 S2

Polychaeta
7
Ampharete grubei (Grube, 1860)

Annelida

Oligochaeta

Annelida

Spinculida

Sp1

Nemertini

Cnidaria

Taxa

Appendix 1. List of the taxa identied in the Lima estuary. For each taxa, the average abundance (ind./m2 ) is given (x absent)

Appendix
144

Tellina tenuis (da Costa, 1778)

Venerupis rhomboides (Pennant, 1777)

Venerupis senegalensis (Gmelin, 1791)

35
36

37

Hinia incrassata (Strom, 1768)

Hinia nitidus (Jereys, 1867)

Hinia reticulata (Linnaeus, 1758)

Hydrobia ulvae (Pennant, 1777)

Polinices catenus (da Costa, 1778)

40

41
42

Cyathura carinata (Kroyer, 1847)

Corophium multisetosum (Stock, 1952)

Melitta palmata (Montagu, 1804)

45
46

Diastylis sp

51

Atelecyclus rotundatus (Olivi, 1792)

Carcinus maenas (Linnaeus, 1758)

Crangon crangon (Linnaeus, 1758)
Diogenes pugilator (Roux, 1829)

48

49
50

Decapoda

Arthropoda

47

Cumacea

Arthropoda

Gammarus sp

44

Amphipoda

Arthropoda

43

Isopoda

Arthropoda

39

38

Gastropoda

Mollusca

Tapes decussatus (Linnaeus, 1758)

Tellimya ferruginosa (Montagu, 1808)

33

34

Scrobicularia plana (da Costa, 1778)

Spisula solida (Linnaeus, 1758)

31

32

Mytilus galloprovincialis (Lamarck, 1819)

Pharus legumen (Linnaeus, 1758)

29

30

Lutraria magna (da Costa, 1778)

Mactra corallina (Linnaeus, 1758)

Mysella bidentata (Montagu, 1803)

26

27
28

4
x
52

x
x

x
8

12

x
x

164

x
x

20

8
4
4

x
x

x
x

116

20
x

28

912

8
x

4
x
x

x
x

x
4

36

x
x

12

x
4

5
x
x

x
x

x
5

50

x
x

25

x
x

x
4
x

x
x

x
x

12

76
x

20

x
x

4
x
x

x
x

4
x

32
4

204

x
20

20
x
x

x
x

x
x

x
x

788

x
12

8
x
x

x
x

x
x

x
x

96

x
x

4
x
x

x
24

40

x
x

x
x

108

x
x

12
x
x

x
x

68

16
x

x
x

36

x
x

x
x
x

x
x

28
x

x
x

x
x

x
x
x

x
x

40
x

x
x

x
x

x
x
x

x
x

16
x

x
x

x
x

x
x
x

x
x

x
x

x
x

x
x

x
x
x

x
x

x
x

x
x

x
x

x
x
x

x
x

12

x
x

x
x

64

x
x

x
x
x

x
x

x
x

x
x

x
x

x
x
x

428
x

x
x

x
x

x
x

x
x
x

656
x

x
x

x
x

x
x

Continued on p. 146

x
x
x

156
x

x
x

x
x

x
x

145

sp

S3

S4

S5

S6

S7

S8

S9

S10

S11 S12

Actinidae

sp

sp

Ampharete grubei (Grube, 1860)

Annelida
Polychaeta

Oligochaeta

Annelida

0.01

sp3

Spinculida

x
x

sp1
sp2

S1

2
3

Nemertini

Cnidaria

Taxa

S2

0.99
0.36

S13 S14 S15 S16 S17 S18 S19 S20

0.05

0.30
x

0.26

S3

x
x

S4

x
x

0.15

S5

x
x

S6

x
x

S7

0.01

x
x

S8

x
x

S9

x
x

S10

0.01

x
x

S11

x
x

S12

x
x

S13

x
x

S14

x
x

S15

x
x

S16

x
x

S17

x
x

S18

x
x

S19

x
x

S20

420 9856 1112 3265 360 628 3124 1196 2632 2268 888 1628 568 516 900 304 212 632 444 664

S2

Appendix 2. List of the taxa identied in the Lima estuary. For each taxa, the average biomass (g AFDW/m2) is given (x absent)

Total

Paracentrotus lividus (Lamarck, 1816)

Echinoidea

54

S1

Amphipholis squamata (Delle Chiaje, 1829) 4

Echinodermata

53

Echinodermata
Ophuroidea

52

Insecta

Arthropoda

Taxa

Appendix 1. (Continued)

146

Euclymene lumbricoides (Quatrefages, 1865) 0.09 0.30

Exogone verugera (Clapare`de, 1868)
0.01 x
Glycera convoluta (Keferstein, 1862)
0.05 0.03

Hediste diversicolor (Muller, 1776)

Heteromastus liformis (Clapare`de, 1864)

Maldane sarsi (Malmgren, 1865)

Melinna palmata (Grube, 1870)

Nephtys cirrosa (Ehlers, 1868)

Nephtys hombergi (Savigny, 1818)

Pectinaria koreni (Malmgren, 1866)

Phyllodoce maculata (Linnaeus, 1767)

Streblospio shrubsolii (Buchanan, 1890)

16

17

18

19

20
21

22

Cerastoderma edule (Linnaeus, 1758)

Corbicula uminea (Muller, 1774)

Lutraria magna (da Costa, 1778)
Mactra corallina (Linnaeus, 1758)

Mysella bidentata (Montagu, 1803)

Mytilus galloprovincialis (Lamarck, 1819)

Pharus legumen (Linnaeus, 1758)

Scrobicularia plana (da Costa, 1778)

Spisula solida (Linnaeus, 1758)

Tapes decussatus (Linnaeus, 1758)

Tellimya ferruginosa (Montagu, 1808)

Tellina tenuis (da Costa, 1778)

Venerupis rhomboides (Pennant, 1777)

Venerupis senegalensis (Gmelin, 1791)

24

25

26
27

28

29

30

31

32

33

34
35

36

37

Mollusca
Gastropoda

Abra alba (Wood, 1802)

23

Bivalvia

Mollusca

15

14

12
13

Eteone picta (Quatrefages, 1865)

11

0.07
x

0.77

0.05

0.04

0.01

x
x

x
x

0.06 x
x
x

0.38 0.88

0.03 x

x
x
0.02 0.04

1.97 x

0.06
0.13

x
x

0.05

0.04
0.05

0.16 0.80

x
x

x
x
x

0.44

0.04 x

0.01 x
x
x

0.03 x

x
x

x
x

0.33 x

x
x

0.13 0.68

0.01 0.01

x
x

0.02 x

0.01 x

x
x
x
0.32 0.05 x

x
x
x

x
x

x
x
x

0.01 x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

0.03 x
0.01 x

0.45 x

0.01 x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

0.07 x

x
x

x
x

x
x

x
x

0.07 0.20 0.07 0.01 x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

5.32 x

x
x

x
x

Continued on p. 148

x
x

1.03 x

x
x

0.01 x

x
x

0.02 3.67 2.25 0.69 1.21 0.36 0.27 0.24 0.52 0.12 0.34 x

x
x
0.20 x

0.01 x

0.31 0.01 x
x

0.04 263.73 0.02 0.76 0.04 x

0.19 0.01 x

0.02 x
x
x

0.39 x

x
x

0.03

x
0.06

0.01 x

0.35 x

0.03 x

0.01

0.01 0.01
x

x
x
0.02 x

0.12 19.01 3.92 25.32 x

x
x

x
x

10

Eteone longa (Fabricius, 1780)

Capitella capitata (Fabricius, 1780)

147

Polinices catenus (da Costa, 1778)

42

Cyathura carinata (Kroyer, 1847)

Melitta palmata (Montagu, 1804)

46

Diastylis sp

Crangon crangon (Linnaeus, 1758)

Diogenes pugilator (Roux, 1829)

50

51

sp

0.01

0.33 0.03

x
x
0.02 0.01

0.01 x

0.03 x
x
x

0.08 x

0.63 1.72
x
x

S2

Total

54

Paracentrotus lividus (Lamarck, 1816)

Echinoidea

Echinodermata
x

S4

x
x

0.14 x

0.11 x
0.01 0.39

x
x

0.04 0.54

0.75 0.70
x
x

0.02 x

S3
x

S6

S7

0.1

x
x

x
x

x
x

x
x
0.01 0.09

x
x

0.62 0.01 x
x
0.01 x

0.08 x

S5

x
x

S9

x
x

0.03 x

x
x

x
x

x
x
x
x
2.36 0.03 0.01 x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x
x
x
x
0.01 0.01 0.02 0.01 x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

x
x

0.02 x

x
x

x
x

x
x

x
x

x
x

0.02

x
x

x
x
x
0.10 0.23 0.28

x
x

S10 S11 S12 S13 S14 S15 S16 S17 S18 S19 S20

0.01 0.06 0.08 x

x
x

S8

1.55 24.53 8.14 28.31 2.13 0.70 264.62 3.58 4.76 2.46 0.73 1.23 0.37 0.27 0.24 1.58 0.12 0.44 5.55 0.30

Ophuroidea
53
Amphipholis squamata (Delle Chiaje, 1829) 0.01 x

Echinodermata

52

Insecta

Arthropoda

Atelecyclus rotundatus (Olivi, 1792)

Carcinus maenas (Linnaeus, 1758)

48
49

Decapoda

Arthropoda

47

Cumacea

Arthropoda

Gammarus sp
Corophium multisetosum (Stock, 1952)

44
45

Amphipoda

Arthropoda

43

Isopoda

Arthropoda

Hinia reticulata (Linnaeus, 1758)

Hydrobia ulvae (Pennant, 1777)

40
41

Hinia incrassata (Strom, 1768)

Hinia nitidus (Jereys, 1867)

38

39

S1

Taxa

Appendix 2. (Continued)

148