Journal of Fish Biology (2000) 57, 15501562

doi:10.1006/jfbi.2000.1408, available online at http://www.idealibrary.com on

Comparative feeding ecology of sympatric Solea solea
and S. senegalensis, within the nursery areas of the
Tagus estuary, Portugal
H. N. C:n:i
Instituto de Oceanograa, Faculdade de Ciencias da Universidade de Lisboa,
Campo Grande, 1700 Lisboa, Portugal
(Received 1 March 2000, accepted 20 July 2000)
Among the stomach contents of 609 individuals of Solea solea and 1104 of S. senegalensis the
main food items of S. solea were Corophium spp. and Hediste diversicolor, and of S. senegalensis
were Corophium spp., H. diversicolor and Scrobicularia plana. For both species, the importance
of larger prey items in the diet, namely H. diversicolor and Crangon crangon, increased with sh
size. Feeding activity of S. solea and S. senegalensis increased in spring and summer.
Short-term variations were particularly related to the tidal cycle and the two species fed in
intertidal areas. Dietary dierences between the two nursery areas reected prey availability
mainly. Although intra- and interspecic length classes overlapped in diet, potential
interspecic competition was probably minimized by a dierential habitat use pattern.
2000 The Fisheries Society of the British Isles
Key words: feeding ecology; Solea; dietary overlap; nursery; Tagus estuary; Portugal.
INTRODUCTION
Few sh species can complete their life cycle within estuarine environments.
Nevertheless, mainly due to high food availability and to low predation pressure,
estuaries are used temporarily by other species with dierent life history patterns
(Haedrich, 1983).
Juveniles of some sh species occur sometimes at high densities in localized
areas, and the ecological niches of several similar morphological types (e.g.
species of Soleidae, Mugilidae, Gobiidae) overlap within these communities (Day
et al., 1981). Therefore, the spatial and temporal distribution and abundance
patterns of sh species as well as resource partitioning within estuarine sh
assemblages are important and interesting issues for understanding the structure
and dynamics of these communities.
Two species of sole, Solea solea (L., 1758) and S. senegalensis Kaup, 1858, are
abundant within the Tagus estuary and use this habitat as a nursery ground.
Within this estuary, two important nursery areas were identied: in one the two
species co-occurred while in the other only S. senegalensis was found. Their
distribution and abundance diered (Cabral & Costa, 1999). The highest
densities of S. solea were recorded in deeper, warmer, low salinity areas and
where the sediment consisted of a high proportion of ne sand and where
amphipods were abundant, while S. senegalensis had a wider distribution and its
Tel.: +351 21 750 00 00; fax: +351 21 750 00 09; email: hcabral@fc.ul.pt
1550
00221112/00/121550+13 $35.00/0 2000 The Fisheries Society of the British Isles
abundance was related to food availability. 0-group S. solea colonized the
estuary in April and S. senegalensis from June to August.
The feeding ecology of S. solea has been studied in coastal areas of north-
western Europe (de Groot, 1971; Braber & de Groot, 1973; Quiniou, 1978;
Lagarde`re, 1987; Henderson et al., 1992) and of the western Mediterranean
(Ramos, 1981; Molinero & Flos, 1991, 1992; Molinero et al., 1991). Unlike S.
solea, the diet of S. senegalensis is known only from the western Mediterranean
(Molinero et al., 1991). Studies on the ecology of these two particular species in
areas of sympatry (i.e. from Bay of Biscay to North Africa and the western
Mediterranean) are scarce.
This study compared the feeding ecology of S. solea and S. senegalensis in the
Tagus estuary. The feeding strategies were related to spatial and temporal
patterns of habitat use, to evaluate the potential for competition between these
two sympatric species.
MATERIALS AND METHODS
STUDY AREA
The 325 km
2
Tagus estuary is partially mixed with a tidal range of 46 m. About 40%
of the estuarine area is intertidal. The two main nursery areas for sh (A, Vila Franca de
Xira; B, Alcochete) identied by Cabral & Costa (1999) are in the upper areas of the
estuary which is<10 m deep and bordered by saltmarshes (Fig. 1). The two nursery areas
are similar environmentally, except that the upper (A) is deeper (mean 44 m), mean
salinity is 5 and there is c. 40% of ne sand in the sediment, while B is 19 m deep,
mean salinity is 207 and the sediment has 604% of mud (Cabral & Costa, 1999).
SAMPLING PROCEDURES AND DATA ANALYSIS
Fish were sampled monthly in areas A and B (Fig. 1) using a 4-m beam trawl with one
tickler chain and 10 mm mesh, from April 1995 to November 1996. Trawls were towed
for 15 min, during daylight, at low water on spring tides. To study the diel variation of
feeding activity other samples were taken at c. 4 h intervals for 24 h, in four periods, in
May and July 1995 and 1996.
Fish were identied, counted, measured (nearest 1 mm L
T
) and weighed (wet weight to
001 g). Stomachs were removed and contents preserved in 4% buered formalin for later
identication. Diet characterization was based on only the stomach contents, to avoid
overestimation of prey with exoskeletons or other hard structures. There may be
disadvantages in this method due to the rapid gastric evacuation, but most previous
studies on the food of Solea spp. have been based on stomach contents (Ramos, 1981;
Lagarde`re, 1987; Molinero & Flos, 1991, 1992).
The stomach contents of 609 S. solea (19262 mm) and 1104 S. senegalensis (23
304 mm) were analysed. Each prey item was identied to the lowest taxonomic level
possible, counted and weighed (wet weight to 0001 g).
As soles generally eat benthic invertebrates, prey availability was determined from
sediment samples taken in spring and summer 1996, when sole were abundant. In each
period and nursery area, four sediment samples were collected evenly spaced along the
line of each tow using a Van Veen grab. A total of 56 sediment samples were collected
in subtidal areas. For the same periods and areas, 10 sediment samples were taken also
in the adjoining intertidal mudats, using a 12 cm core. Prey abundance in the sediment
was expressed as the number of individuals per m
2
.
The relative importance of each prey item in the diet was expressed as percent of
numerical abundance (I
N
), occurrence of food items in stomachs (I
O
) and weight (I
W
)
(Hyslop, 1980). To study diet variation with sh size, data were grouped in 25 mm length
classes. A cluster analysis based on the I
N
values for each length class was performed,
rrrniNc rcoiocx or 1vo sxxi:1ic soirs 1551
using the
2
distance and the UPGMA method and SPSS software (Norusis, 1992).
Cluster analysis results were used to avoid redundancy dening wider length classes based
on diet similarities. Diet dierences between length classes and between nursery areas
were tested using the G-test of independence (Sokal & Rohlf, 1982; Zar, 1996) and with
a 005 signicance level.
Feeding activity was evaluated by the vacuity index (I
V
) dened as the percent of empty
stomachs (Hyslop, 1980). Similar test procedures to those described above were
conducted to evaluate the dierences in the number of empty stomachs according to hour
of the day and tidal phase. Four periods of the day (08001400, 14002000, 20000200,
and 02000800 hours) and four phases of tidal cycle (half periods from low and high tide
until high and low tide, respectively) were considered.
Food selectivity was evaluated by comparing prey availability (in subtidal and
intertidal grounds in both nursery areas) and diet composition in numerical terms using
Spearman rank correlations. Diet overlap was measured using the Schoener index (I
S
),
dened as I
S
=105(
n
i=1
/p
i
D
p
i
E
/), where p
i
D
and p
i
E
and were the numerical frequencies
of item i in the diet and in the environment, respectively (Linton et al., 1981). Values of
diet overlap vary from 0, when no food is shared, to 1, when there is the same
proportional use of all food resources. Although there are no critical levels with which
overlap values can be compared, Wallace (1981) and Wallace & Ramsey (1983) suggested
that values >06 should be considered as biologically signicant.
A
38N
36N
40N
10W
Lisbon
P
o
r
t
u
g
a
l
A
t
l
a
n
t
i
c

O
c
e
a
n
B
10 km
8W 6W
Fic. 1. Location of the two sampling areas within the Tagus estuary.
1552 n. N. c:n:i
RESULTS
GENERAL FOOD HABITS
S. solea ate chiey Polychaeta, mainly Hediste diversicolor, and Amphipoda,
particularly Corophium spp. (Table I). H. diversicolor was most important by
weight (I
W
) and Corophium spp. by number (I
N
) and occurrence (I
O
). Spionidae,
Scrobicularia plana (only siphons were ingested) and Decapoda were also
common prey but their index values were lower than those of Corophium spp.
and H. diversicolor. Corophium spp. and H. diversicolor were important also to
S. senegalensis, as was S. plana (high I
N
and I
O
: Table I) and Spionidae (high I
N
).
T:nir I. Numerical (I
N
), occurrence (I
O
) and gravimetric (I
W
) index values of prey found
in stomachs of S. solea and S. senegalensis in the Tagus estuary
Species S. solea S. senegalensis
Index I
N
I
O
I
W
I
N
I
O
I
W
Polychaetes
Hediste diversicolor 73 154 579 118 370 645
Nephthys hombergi 02 08 17
Glycera convoluta 01 05 03
Diopatra neapolitana 01 03 69
Stresblospio shrubsolii 11 08 00
Spionidae n.i. 125 63 03 95 56 03
Polychaeta n.i. 21 84 49 13 54 12
Oligochaetes
Oligochaeta n.i. 09 21 07 04 11 01
Molluscs
Scrobicularia plana 105 84 37 409 275 100
Peringia ulvae 01 03 00
Mysids
Neomysis integer 01 02 00
Mysidae n.i. 07 14 01 04 06 00
Isopods
Cyathura carinata 05 21 02 08 32 02
Sphaeroma sp. 04 14 00 02 05 01
Saduriella lozadai 04 14 07 01 05 03
Haustorius arenarius 01 03 01
Orchestria sp. 01 03 00
Gammarus sp. 05 07 00
Melita palmata 02 07 00
Corophium spp. 568 365 175 306 69 91
Amphipoda n.i. 02 12 00 01 03 00
Decapods
Carcinus maenas 01 03 02
Crangon crangon 36 63 128 07 24 36
Fishes
Pomatoschistus microps 02 05 13
Unidentied 34 70 04 08 38 01
rrrniNc rcoiocx or 1vo sxxi:1ic soirs 1553
DIET VARIATION WITH FISH LENGTH AND NURSERY AREA
Cluster analysis of S. solea stomach contents data identied three major length
groups: sh >250 mm; <250 but >101 mm; and <101 mm (Fig. 2). As there
were few individuals >250 mm, only two groups (<101 mm and >100 mm
length) were compared. The numbers of each food item diered between the
two length classes (G
W
=2342, d.f.=6, P<005). Smaller individuals fed mainly
on Spionidae and larger ones mostly on Corophium spp., H. diversicolor and
C. crangon (Fig. 3). For S. senegalensis, the cluster analyses for each nursery
area were not consistent (Fig. 4). To standardize length groups between nursery
areas and sole species three length classes were chosen: <101 mm; 101175 mm;
and >175 mm. Prey numbers diered between these length classes for both
nursery A (G
W
=2576, d.f.=6, P<005) and nursery B (G
W
=837, d.f.=6,
P<005). At nursery area A, Spionidae decreased in importance with increasing
sh size (Fig. 5), I
N
was highest for S. plana in sh between 101 and 175 mm, and
for Corophium spp. in sh >175 mm (Fig. 5). For nursery area B, smaller
0
101125
5 10 15 20 25
126150
151175
226250
176200
201225
< 51
5175
76100
> 250
Fic. 2. Dendrogram resulting from the cluster analysis performed on stomach contents data of S. solea
grouped in length classes (mm).
0
II
100
Length classes
I
N
I
25
50
75
I II II I
I
O
I
W
Other
Oligochaeta
C. crangon
Spionidae
S. plana
H. diversicolor
Corophium spp.
Food item
Length classes:
I < 101 mm
II > 100 mm
Fic. 3. Relative importance of food items in the diet of S. solea based on numerical (I
N
), occurrence (I
O
)
and gravimetric (I
W
) indices.
1554 n. N. c:n:i
individuals of S. senegalensis consumed mainly S. plana and H. diversicolor
while larger sh (101175 mm; >175 mm) showed higher levels of Decapoda,
especially C. crangon (Fig. 5).
SEASONAL AND DIEL VARIATION IN FEEDING ACTIVITY
Vacuity was high at all times (mean values 69 and 68%, respectively for S.
solea and S. senegalensis), with lowest values in summer (Fig. 6). Winter levels
were slightly higher in S. senegalensis, and 100% in the 2 S. solea caught at this
season. I
V
did not dier between the periods of the day (G
W
=038, d.f.=3,
P>005; and G
W
=592, d.f.=3, P>005; respectively for S. solea and S.
senegalensis). Feeding activity in relation to tidal phase was similar in both
species with I
V
lower during high tides (G
W
=833, d.f.=3, P<005; and
G
W
=9198, d.f.=3, P<005; respectively for S. solea and S. senegalensis) (Fig. 7).
FOOD SELECTIVITY
Diet reected prey availability in both subtidal and intertidal areas (Table II)
for S. solea and for S. senegalensis at nursery area A (Table III). For nursery
area B, diet reected prey availability only on intertidal grounds.
NICHE OVERLAP
Judged by Schoener index values >06 (Table IV), niche overlap occurred at
area A between the two smallest sizes of the two sole species, and between the
two largest sizes. At area B, it occurred between the largest size group of
S. senegalensis and each of the other two sizes, but not between the latter two.
0
176200
5 10 15 20 25
201225
226250
< 76
76100
126150
151175
101125
> 250
(a)
0
< 76
5 10 15 20 25
76100
126150
151175
101125
176200
> 225
201225
(b)
Fic. 4. Dendrogram resulting from the cluster analysis performed on stomach contents data of
S. senegalensis, in nursery A (a) and B (b), grouped in length classes (mm).
rrrniNc rcoiocx or 1vo sxxi:1ic soirs 1555
DISCUSSION
Previous studies on S. solea have reported their most important prey items as
Polychaeta, Crustacea and Mollusca (Quiniou, 1978; Ramos, 1981; Lagarde`re,
1987; Henderson et al., 1992), diering relatively by site (North Sea, English
0
II
100
Length classes
I
N
I
25
50
75
I II II I
I
O
I
W
Other
Pomatoschistus spp.
C. crangon
Spionidae
S. plana
H. diversicolor
Corophium spp.
Food item
Length classes:
I < 101 mm
II 101 175 mm
III > 175 mm
(a)
III III III
0
II
100
I
25
50
75
I II II I
(b)
III III III
Fic. 5. Relative importance of food items in the diet of S. senegalensis, in nursery A (a) and B (b), based
on numerical (I
N
), occurrence (I
O
) and gravimetric (I
W
) indices.
1556 n. N. c:n:i
Channel, North France and the western Mediterranean). The variety of habitats
(e.g. shallow coastal areas, continental shelf, estuarine systems) and range of sh
lengths analysed in these studies probably account for these slight dietary
dissimilarities.
Molinero et al. (1991), in the western Mediterranean, reported that the diets of
S. senegalensis and S. solea were very similar. The number of prey taxa in the
diet of S. senegalensis was similar to that in the Tagus estuary. In numerical
terms Crustacea, Polychaeta and Mollusca were the most important food items,
in decreasing order of importance.
Ramos (1981), Lagarde`re (1987) and Molinero & Flos (1991) all noted that
larger soles ate larger prey, as was evident in the present study.
Likewise, patterns of seasonal variation in feeding activity of S. solea similar to
those in the Tagus have been reported by several authors. Vacuity values were
generally high (mean values 6285%), with a decrease in spring and summer
(Quiniou, 1978; Ramos, 1981; Henderson et al., 1992). For S. senegalensis,
Molinero et al. (1991) reported a mean vacuity of 40%. The high vacuity values
were certainly related to a fast gastric evacuation. De Groot (1971) outlined
that, due to the characteristics of the alimentary tract and to a fast digestive
process, S. solea fed on small quantities of prey very often. This suggests a high
evacuation rate between the stomach and the intestine and the lack of digestion
in the stomach (Lagarde`re, 1987), as in Pleuronectes platessa L., 1758 (Kuipers,
1975). So, stomach emptiness may not give a good picture of the feeding
T:nir II. Ranks of abundance of benthic prey taxa and sediment composition in subtidal
and intertidal areas of nursery areas A and B (ranks are in decreasing order of
importance)
A subtidal A intertidal B subtidal B intertidal
% large sand (>035 mm) 42 3 32 <1
% ne sand (>0063 mm; <035 mm) 41 29 8 <1
% mud (<0063 mm) 17 68 60 100
Hediste diversicolor 6 2 9 3
Glycera convoluta 12 12 7 8
Polydora spp. 8 12 11 8
Other Polychaeta 8 9 6 8
Spionidae 5 3 1 2
Oligochaeta 6 7 2 4
Scrobicularia plana 1 9 3 1
Peringia ulvae 10 12 11 8
Sphaeroma spp. 12 12 11 8
Cyathura carinata 4 7 9 7
Idotea neglecta 12 11 11 8
Saduriella losadai 12 5 11 8
Haustorius arenarius 12 4 11 8
Melita palmata 3 12 4 8
Gammaridae 10 6 5 8
Corophium spp. 2 1 7 5
Dolicopodidae 12 12 11 6
rrrniNc rcoiocx or 1vo sxxi:1ic soirs 1557
activity. The measurement of food weight along all the digestive tract could be
used alternatively to improve food consumption estimates (Lagarde`re, 1987).
Kruuk (1963), de Groot (1971) and Lagarde`re (1987) suggested that S. solea
fed actively at night. However, as Lagarde`re (1987) pointed out, most of these
studies were conducted only in subtidal areas. Both sole species in the Tagus
estuary showed a strong relationship between feeding activity and the tidal cycle.
The decrease in vacuity values during high tide suggests that both species use
intertidal areas as feeding grounds, as do Pleuronectes esus (L., 1758) and
P. platessa (Gibson, 1973; Burrows et al., 1994; Nash et al., 1994).
Comparing prey availability in the environment and in the diet of the soles in
the Tagus estuary suggests a dierent importance of intertidal areas according to
nursery area. At area A, the diet composition of both soles was correlated with
prey availability in both subtidal and intertidal grounds, indicating opportunistic
utilization and low selectivity (Miller et al., 1985). However, at area B, diet of
S. senegalensis suggested selection of the intertidal areas for feeding. As the
benthic invertebrates in the intertidal mudats in those nursery areas are more
abundant than in the adjoining subtidal areas (Cabral, 1998), the dierences in
0
(179)
Summer
1996
100
(56)
Spring
1995
25
50
75
(33)
Autumn
1995
(43)
Summer
1995
(2)
Winter
1996
(99)
Spring
1996
(13)
Autumn
1996
I
V

(
%
)
(a)
0
(64)(114)
Summer
1996
100
(27) (32)
Spring
1995
25
50
75
(194)(105)
Autumn
1995
(31) (28)
Summer
1995
(78)
Winter
1996
(207)(39)
Spring
1996
(20)
Autumn
1996
I
V

(
%
)
(b)
n
n
Fic. 6. Vacuity index (I
V
) values determined for S. solea (a) and S. senegalensis (b) according to season
(n=sample size). , Nursery A; , nursery B.
1558 n. N. c:n:i
the feeding activity pattern of S. senegalensis according to nursery area may be
due to morphological features of intertidal ats, which are much more extended
at nursery B.
Intra- and interspecic diet overlap was low for S. solea and S. senegalensis
within the Tagus estuary. The few high overlap values observed were between
groups that do not co-occur spatially or temporally (e.g. smaller individuals of
S. solea and S. senegalensis) or between larger groups of which one was scarce
(Cabral & Costa, 1999). Dierent colonization periods and spatial distribution
of the two species must reduce niche overlap. Avoidance of interspecic
competition by the adoption of dierent strategies of resource use has also been
reported for several co-occurring atsh species (Moore & Moore, 1976; Poxton
et al., 1983; Burke, 1995). The assessment of the relative importance for soles of
each of the nurseries of the Tagus estuary would be particularly interesting to
investigate in future studies. While the absence of S. solea from nursery B is
probably related to abiotic conditions, since this species is usually more
0
100
I
25
50
75
III II IV
I
V

(
%
)
(55)
(117)
(80)
(55)
(31)
(162)
(49)
(109)
Low tide High tide Low tide
Tidal
phase
Fic. 7. Vacuity index (I
V
) values determined for S. solea ( ) and S. senegalensis ( ) according to tidal
cycle phase (sample size in brackets).
T:nir III. Spearman rank correlations between numerical abundance of prey in the diet
and environment
A subtidal A intertidal B subtidal B intertidal
S. solea <101 mm 058* 049*
S. solea >100 mm 064* 054*
S. senegalensis <101 mm 045 063* 040 052*
S. senegalensis 101 mm175 mm 072* 054* 049 069*
S. senegalensis >175 mm 050* 057* 042 056*
*Signicant correlations for =005.
rrrniNc rcoiocx or 1vo sxxi:1ic soirs 1559
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abundant in mesohaline areas (Riley et al., 1981; Marchand, 1988), the question
of which area is a better nursery for S. senegalensis is of particular relevance.
Some of the key aspects to investigate would be those related with habitat
segregation by juveniles, nursery colonization processes and movement patterns
between nurseries. Also, further studies on the use of intertidal areas by
potential competitors of soles in the Tagus estuary (e.g. estuarine resident shes,
waders) would aid better understanding of the structure and dynamics of
estuarine nurseries.
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rrrniNc rcoiocx or 1vo sxxi:1ic soirs 1561
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