comparative feeding ecology of sympatric solea solea

8/2/2019 Comparative Feeding Ecology of Sympatric Solea Solea

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Journal of Fish Biology (2000) 57, 15501562doi:10.1006/jfbi.2000.1408, available online at http://www.idealibrary.com on

Comparative feeding ecology of sympatric Solea soleaand S. senegalensis, within the nursery areas of the

Tagus estuary, Portugal

H. N. C

Instituto de Oceanografia, 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 themain food items ofS. solea were Corophium spp. and Hediste diversicolor, and ofS. senegalensiswere Corophium spp., H. diversicolor and Scrobicularia plana. For both species, the importanceof larger prey items in the diet, namely H. diversicolor and Crangon crangon, increased with fishsize. 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 inintertidal areas. Dietary differences between the two nursery areas reflected prey availabilitymainly. Although intra- and interspecific length classes overlapped in diet, potentialinterspecific competition was probably minimized by a differential habitat use pattern.

2000 The Fisheries Society of the British Isles

Key words: feeding ecology; Solea; dietary overlap; nursery; Tagus estuary; Portugal.

INTRODUCTION

Few fish 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 different life history patterns(Haedrich, 1983).

Juveniles of some fish species occur sometimes at high densities in localizedareas, 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 abundancepatterns of fish species as well as resource partitioning within estuarine fishassemblages are important and interesting issues for understanding the structureand dynamics of these communities.

Two species of sole, Solea solea (L., 1758) and S. senegalensis Kaup, 1858, areabundant within the Tagus estuary and use this habitat as a nursery ground.Within this estuary, two important nursery areas were identified: in one the twospecies co-occurred while in the other only S. senegalensis was found. Theirdistribution and abundance differed (Cabral & Costa, 1999). The highestdensities of S. solea were recorded in deeper, warmer, low salinity areas and

where the sediment consisted of a high proportion of fine sand and whereamphipods were abundant, while S. senegalensis had a wider distribution and its

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abundance was related to food availability. 0-group S. solea colonized theestuary 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;

Lagardere, 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 inareas of sympatry (i.e. from Bay of Biscay to North Africa and the westernMediterranean) are scarce.

This study compared the feeding ecology of S. solea and S. senegalensis in theTagus estuary. The feeding strategies were related to spatial and temporalpatterns of habitat use, to evaluate the potential for competition between thesetwo sympatric species.

MATERIALS AND METHODS

STUDY AREA

The 325 km2 Tagus estuary is partially mixed with a tidal range of 4 6 m. About 40%of the estuarine area is intertidal. The two main nursery areas for fish (A, Vila Franca deXira; B, Alcochete) identified by Cabral & Costa (1999) are in the upper areas of theestuary which is


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using the 2 distance and the UPGMA method and SPSS software (Norusis, 1992).Cluster analysis results were used to avoid redundancy defining wider length classes basedon diet similarities. Diet differences between length classes and between nursery areaswere tested using the G-test of independence (Sokal & Rohlf, 1982; Zar, 1996) and witha 005 significance level.

Feeding activity was evaluated by the vacuity index (IV) defined as the percent of emptystomachs (Hyslop, 1980). Similar test procedures to those described above wereconducted to evaluate the differences in the number of empty stomachs according to hourof 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 tideuntil high and low tide, respectively) were considered.

Food selectivity was evaluated by comparing prey availability (in subtidal andintertidal grounds in both nursery areas) and diet composition in numerical terms usingSpearman rank correlations. Diet overlap was measured using the Schoener index (IS),

defined as IS=105( n

i=1/pi

Dpi

E/), where pi

Dand pi

Eand 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 sameproportional use of all food resources. Although there are no critical levels with whichoverlap values can be compared, Wallace (1981) and Wallace & Ramsey (1983) suggestedthat values >06 should be considered as biologically significant.

A

38N

36N

40N

10W

LisbonP

ortugal

AtlanticO

cean

B

10 km

8W 6W

F. 1. Location of the two sampling areas within the Tagus estuary.

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RESULTS

GENERAL FOOD HABITS

S. solea ate chiefly Polychaeta, mainly Hediste diversicolor, and Amphipoda,particularly Corophium spp. (Table I). H. diversicolor was most important byweight (IW) and Corophium spp. by number (IN) and occurrence (IO). 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 toS. senegalensis, as was S. plana (high IN and IO: Table I) and Spionidae (high IN).

T I. Numerical (IN), occurrence (IO) and gravimetric (IW) index values of prey foundin stomachs of S. solea and S. senegalensis in the Tagus estuary

Species S. solea S. senegalensis

Index IN IO IW IN IO IW

PolychaetesHediste diversicolor 73 154 579 118 370 645Nephthys hombergi 02 08 17Glycera convoluta 01 05 03Diopatra neapolitana 01 03 69Stresblospio shrubsolii 11 08 00Spionidae n.i. 125 63 03 95 56 03Polychaeta n.i. 21 84 49 13 54 12OligochaetesOligochaeta n.i. 09 21 07 04 11 01MolluscsScrobicularia plana 105 84 37 409 275 100Peringia ulvae 01 03 00MysidsNeomysis integer 01 02 00Mysidae n.i. 07 14 01 04 06 00IsopodsCyathura carinata 05 21 02 08 32 02Sphaeroma sp. 04 14 00 02 05 01Saduriella lozadai 04 14 07 01 05 03Haustorius arenarius 01 03 01

Orchestria sp. 01 03 00Gammarus sp. 05 07 00Melita palmata 02 07 00Corophium spp. 568 365 175 306 69 91Amphipoda n.i. 02 12 00 01 03 00DecapodsCarcinus maenas 01 03 02Crangon crangon 36 63 128 07 24 36FishesPomatoschistus microps 02 05 13Unidentified 34 70 04 08 38 01

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DIET VARIATION WITH FISH LENGTH AND NURSERY AREA

Cluster analysis ofS. solea stomach contents data identified three major lengthgroups: fish >250 mm; 101 mm; and 250 mm, only two groups (100 mmlength) were compared. The numbers of each food item differed between thetwo length classes (GW=2342, d.f.=6, P 100 mm

F. 3. Relative importance of food items in the diet ofS. solea based on numerical (IN), occurrence (IO)and gravimetric (IW) indices.

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individuals of S. senegalensis consumed mainly S. plana and H. diversicolorwhile larger fish (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 levelswere slightly higher in S. senegalensis, and 100% in the 2 S. solea caught at thisseason. IV did not differ between the periods of the day (GW=038, d.f.=3,P>005; and GW=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 IV lower during high tides (GW=833, d.f.=3, P 250

(a)

0

< 76

5 10 15 20 25

76100126150151175101125176200

> 225201225

(b)

F. 4. Dendrogram resulting from the cluster analysis performed on stomach contents data ofS. senegalensis, in nursery A (a) and B (b), grouped in length classes (mm).

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DISCUSSION

Previous studies on S. solea have reported their most important prey items asPolychaeta, Crustacea and Mollusca (Quiniou, 1978; Ramos, 1981; Lagardere,1987; Henderson et al., 1992), differing relatively by site (North Sea, English

0II

100

Length classes

IN

I

25

50

75

III II I

IO IW

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

0II

100

I

25

50

75

III II I

(b)

III III III

F. 5. Relative importance of food items in the diet ofS. senegalensis, in nursery A (a) and B (b), basedon numerical (IN), occurrence (IO) and gravimetric (IW) indices.

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Channel, North France and the western Mediterranean). The variety of habitats(e.g. shallow coastal areas, continental shelf, estuarine systems) and range of fishlengths analysed in these studies probably account for these slight dietarydissimilarities.

Molinero et al. (1991), in the western Mediterranean, reported that the diets ofS. senegalensis and S. solea were very similar. The number of prey taxa in thediet of S. senegalensis was similar to that in the Tagus estuary. In numericalterms Crustacea, Polychaeta and Mollusca were the most important food items,in decreasing order of importance.

Ramos (1981), Lagardere (1987) and Molinero & Flos (1991) all noted thatlarger soles ate larger prey, as was evident in the present study.

Likewise, patterns of seasonal variation in feeding activity ofS. solea similar tothose in the Tagus have been reported by several authors. Vacuity values weregenerally 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 valueswere certainly related to a fast gastric evacuation. De Groot (1971) outlinedthat, due to the characteristics of the alimentary tract and to a fast digestiveprocess, 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 digestionin the stomach (Lagardere, 1987), as in Pleuronectes platessa L., 1758 (Kuipers,1975). So, stomach emptiness may not give a good picture of the feeding

T II. Ranks of abundance of benthic prey taxa and sediment composition in subtidaland 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 0063 mm;


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activity. The measurement of food weight along all the digestive tract could beused alternatively to improve food consumption estimates (Lagardere, 1987).

Kruuk (1963), de Groot (1971) and Lagardere (1987) suggested that S. soleafed actively at night. However, as Lagardere (1987) pointed out, most of thesestudies were conducted only in subtidal areas. Both sole species in the Tagusestuary showed a strong relationship between feeding activity and the tidal cycle.The decrease in vacuity values during high tide suggests that both species useintertidal areas as feeding grounds, as do Pleuronectes flesus (L., 1758) andP. platessa (Gibson, 1973; Burrows et al., 1994; Nash et al., 1994).

Comparing prey availability in the environment and in the diet of the soles inthe Tagus estuary suggests a different importance of intertidal areas according tonursery area. At area A, the diet composition of both soles was correlated withprey availability in both subtidal and intertidal grounds, indicating opportunisticutilization and low selectivity (Miller et al., 1985). However, at area B, diet of

S. senegalensis suggested selection of the intertidal areas for feeding. As thebenthic invertebrates in the intertidal mudflats in those nursery areas are moreabundant than in the adjoining subtidal areas (Cabral, 1998), the differences in

0(179)

Summer1996

100

(56)Spring1995

25

50

75

(33)Autumn

1995

(43)Summer

1995

(2)Winter1996

(99)Spring1996

(13)Autumn

1996

IV

(%)

(a)

0(64)(114)Summer

1996

100

(27) (32)Spring1995

25

50

75

(194)(105)Autumn

1995

(31) (28)Summer

1995

(78)Winter1996

(207)(39)Spring1996

(20)Autumn

1996

IV

(%)

(b)

n

n

F. 6. Vacuity index (IV) values determined for S. solea (a) and S. senegalensis (b) according to season(n=sample size). , Nursery A; , nursery B.

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the feeding activity pattern of S. senegalensis according to nursery area may bedue to morphological features of intertidal flats, which are much more extendedat nursery B.

Intra- and interspecific diet overlap was low for S. solea and S. senegalensiswithin the Tagus estuary. The few high overlap values observed were betweengroups that do not co-occur spatially or temporally (e.g. smaller individuals ofS. solea and S. senegalensis) or between larger groups of which one was scarce(Cabral & Costa, 1999). Different colonization periods and spatial distributionof the two species must reduce niche overlap. Avoidance of interspecificcompetition by the adoption of different strategies of resource use has also beenreported for several co-occurring flatfish species (Moore & Moore, 1976; Poxtonet 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 toinvestigate in future studies. While the absence of S. solea from nursery B isprobably related to abiotic conditions, since this species is usually more

0

100

I

25

50

75

IIIII IV

IV

(%)

(55)

(117)

(80)

(55)

(31)(162)

(49)

(109)

Low tide High tide Low tide

Tidalphase

F. 7. Vacuity index (IV) values determined for S. solea ( ) and S. senegalensis ( ) according to tidalcycle phase (sample size in brackets).

T III. Spearman rank correlations between numerical abundance of prey in the dietand environment

A subtidal A intertidal B subtidal B intertidal

S. solea 100 mm 064* 054* S. senegalensis 175 mm 050* 057* 042 056*

*Significant correlations for =005.

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TI

V.

Schoenerindexvaluesbetw

eendifferentintra-

andinterspecificlengthclasses(mm)ofS

.soleaandS.senegalensisinnurseryareas

A

andBoftheTagusestuary

S.solea

(100)A

S.senegalen

sis

(

comparative feeding ecology of sympatric solea solea

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