Age, Growth and Feeding Habits of the Brown ComberSerranus hepatus(Linnaeus, 1758) on the Cretan Shelf

Estuarine, Coastal and Shelf Science (1998) 46, 723–732

Age, Growth and Feeding Habits of the Brown Comber Serranus hepatus (Linnaeus, 1758) on the Cretan Shelf M. Labropouloua,b,c, G. Tserpesa and N. Tsimenidesb a b

Institute of Marine Biology of Crete, P.O. Box 2214, GR-71003 Iraklion, Crete, Greece Department of Biology, University of Crete, P.O. Box 2208, GR-71409, Iraklion, Crete, Greece

Received 25 March 1997 and accepted in revised form 5 October 1997 Forty-five samples of the brown comber Serranus hepatus were collected during experimental surveys carried out on a monthly basis (August 1990 to August 1992) along the Cretan continental shelf. A total of 1268 specimens 31–140 mm in total length were analysed. Growth was well described by both standard and seasonalized forms of the von Bertalanffy growth model and the computed parameters were L`=152 mm, k=0·36, t0 =
0·57. Feeding intensity was high throughout the study period and varied significantly among the age classes of fish examined. Stomach content analysis revealed that S. hepatus is carnivorous, feeding mainly on decapods. Diets did not vary seasonally; decapods were the most important prey throughout the year. However, the composition of the prey consumed varied considerably with predator age coupled with differences in mean prey sizes utilized by each age class. The mean weight of stomach contents increased significantly for older specimens, while the mean number of prey items decreased. Age-specific dietary selection was primarily a function of body size of the predator and appears to reduce intra-specific competition among the members of the different age classes. The results suggest that S. hepatus plays an important trophic role as a macrophagic carnivorous species on the Cretan continental shelf.  1998 Academic Press Limited Keywords: Serranus hepatus; age and growth; feeding; prey selection; ontogeny; diet breadth

Introduction The brown comber Serranus hepatus is a small, demersal serranid species which occurs along the coasts of the Eastern Atlantic Ocean from Portugal to the Canaries and the Mediterranean Sea. It is common in Posidonia beds, sandy and muddy bottoms down to 100 m depths (Whitehead et al., 1986). It has been observed in relatively high densities over the Cretan continental shelf and it is considered to be among the 30 most abundant fish species in the area (Tsimenides et al., 1991). The brown comber is a synchronous hermaphrodite which guarantees a maximum homogeneity amongst the populations under study (Brusle´, 1983). Despite its widespread occurrence, S. hepatus is of low commercial value, probably due to its small size. As a consequence, very little is known about the species biology and ecology. Brusle´ (1983) studied the sexuality and the development of ovarian and testicular components in their hermaphroditic gonads. However, no information was found in the literature c Present address: National Center for Marine Research, Agios Kosmas 16604, Athens, Greece.

0272–7714/98/050723+10 $25.00/0/ec970315

on aspects related to age, growth and feeding habits of the species. The aim of the present work was to provide such information for S. hepatus from specimens collected during experimental trawl surveys carried out along the Cretan continental shelf. The feeding habits of S. hepatus were studied by stomach content analysis to identify differences in its diet arising from seasonal changes and variability related to the various lifehistory stages and to investigate feeding trends which may be of consequence when attempting to determine interrelationships and interactions with cohabiting demersal fish species. Materials and methods Study area and sampling procedure Forty-five samples yielding a total of 1268 S. hepatus from trawl surveys over the Cretan continental shelf, in the area of Iraklion Bay, were analysed. This bay occupies an area of 92 km2 on the northern coast of Crete (South Aegean Sea, Eastern Mediterranean, Greece) between 3520 and 3528 N and 2502 and 2520 E. Monthly samples from August 1990 to  1998 Academic Press Limited

724 M. Labropoulou et al.

August 1992, with the exception of January due to inclement weather, were collected from fixed stations covering all the trawlable fishing grounds of the region, between 30 and 100 m depth. Details of survey design and sampling procedure are given by Tsimenides et al. (1991). All samples were taken using a demersal trawl with a cod-end liner of 22 mm stretched mesh size, and subsamples were taken aiming to obtain a sufficient number of fish for all length classes captured with the gear. The duration of each trawl (bottom time) was 30–45 min and the trawling speed fluctuated from 2·5 to 3 knots. All samples were taken during the morning, between 0830 and 0930h.

Age and growth For all fish, the total length (TL) was measured to the nearest millimetre. Six scales from the lateral-line region under the pectoral fin of each specimen were cleaned with water and an imprint made on a 0·3 mm thick cellulose acetate plastic plate at 800 kg cm
2 at 95 C for 2 min with a Carver autopress. The prints of the scales were viewed on an Eberbach projector at 32 magnification. The number of annuli were recorded and the scale radius from the focus to the end of the scale print on the left dorsal rim was measured. Annuli were identified by standard criteria (Bagenal & Tesch, 1978), especially cutting over of circuli in the lateral field, close spacing of circuli followed by wider spacing in the anterior field and consistency of these characteristics in at least two scales out of the six examined per fish. Scale prints were read twice by a single reader at an interval of 2 months between the two readings, to reduce subjectivity. When the two readings of the same print resulted in different age estimates the scales were considered to be unreadable. Age-classes were assigned on the number of scale annuli and the month the fish was collected. Date of birth was set at June because high concentrations of S. hepatus larvae in the Cretan sea have been observed during this month (Tsimenides, unpubl. data). Such concentrations in June have also been reported for other Mediterranean areas (Sabate´s, 1990). In order to examine the periodicity of annuli formation, the marginal increment ratio (MIR) was estimated for each specimen according to the formula: MIR=(S
rn)/S where S=scale radius and rn =radius of the most recent annulus.

The mean MIR and the standard deviation were computed for each month and age separately. Marginal increment analysis was not performed for ages greater than three because of insufficient samples. Estimates of theoretical growth in length were obtained by fitting mean monthly length at age data to two forms of the von Bertalanffy growth equation: (1) the standard form; and (2) the seasonalized form (Sparre & Venema, 1992):

where Lt =TL at age t, L`=asymptotic length, k=growth coefficient, t0 =theoretical age at zero length, C=the amplitude of the fluctuation in seasonal growth (0cCc1) and ts =the commencement of variations in sinusoidal growth with respect to t=0. It is valid that ts =WP+0·5, where WP (winter point)=that point at which minimum growth occurs (0cWPc1). If C=0 the equation reduces to the standard form of the von Bertalanffy growth function implying that there is no seasonality in the growth rate. Mean monthly data were used in order to assign equal weight to all observations. Only mean values from samples of greater than five fish were used. Growth parameters of both models were estimated iteratively using the Simplex minimization algorithm (Wilkinson, 1988). The measure of goodness-of-fit was the coefficient of determination (r2). Back calculations of length at age were estimated from a modified version of the direct proportion formula (Lee, 1920): Ln
c=(Sn/S)(L
c) where Ln =TL when the annulus n was formed, L=TL at time of capture, c=intercept on length axis from linear regression of length on scale radius, Sn =distance from scale focus to annulus n and S=scale radius.

Stomach content analysis Stomach contents of the brown comber were examined up to a total of 20–30 specimens in each haul and station. When catches were higher, the fish were separated into size intervals, then proportionally subsampled until a total of 30 fish were selected for stomach analysis. The samples were fixed on-board immediately after capture, in 10% buffered formalin, measured to the nearest millimetre (total length) and

Serranus hepatus on the Cretan Shelf 725

weighed to the nearest 0·1 g. Thereafter, the stomachs were removed and the contents wet weighed. Where possible, prey items were identified to species or the nearest possible taxonomic level, counted under a binocular microscope and weighed to the nearest 0·01 g. Total length of the fish examined ranged from 31 to 140 mm; mean length was 88·1 mm and standard deviation 13·9. However, specimens larger than 120 mm were excluded from the analysis since they had evidence of regurgitation (everted stomach or partially digested food in the mouth). In order to evaluate variations in food habits as a function of age, specimens were separated into four age classes according to their total length. The quantitative importance of different prey in the diet was expressed as follows (Berg, 1979; Hyslop, 1980): (1) Vacuity index (VI): the percentage of stomachs which were empty; (2) Percentage frequency of occurrence (F): the percentage of non-empty stomachs in which a food item was found; (3) Percentage numerical abundance (Cn): each prey item as percentage of the total number of food items in a sample; (4) Percentage gravimetric composition (Cw): the wet weight of each prey item, as a percentage of the total weight of the stomach contents in a sample. The most important food items were identified using the index of relative importance (IRI) of Pinkas et al. (1971), as modified by Hacunda (1981): IRI=(Cn +Cw)F This index has been expressed as %IRI=(IRI/ &IRI)100. Prey were sorted in decreasing order according to their %IRI contribution and then cumulative %IRI was calculated. Cluster analysis (group average) was performed on the standardized IRI values to describe ontogenetic variations of S. hepatus food habits, using the Bray–Curtis similarity index (Field et al., 1982) and the PRIMER algorithms (Plymouth Marine Laboratory, U.K.). Niche breadth for the utilization of food resources was calculated according to the Shannon–Wiener index (Krebs, 1989):

where pi is the proportion of a specific prey category for the n categories of prey listed. Trophic diversity H

was calculated using the IRI values (Carrasso´n et al., 1992). The Shannon–Wiener index value increases with the number of species. In practice, for biological communities H does not seem to exceed 5·0 (Krebs, 1989). Differences in diet composition and stomach fullness by age and mouth were tested by ÷2 on combined data for both years, because diet composition did not vary significantly between the 2 years. The logit model used to investigate monthly variations in the proportion of full/empty stomachs, as a function of fish size was: log(pd /pd
1)=ad +bdL+e where pd is the probability that a stomach is nonempty in month d, L is the fish length and e is the error term. One-way ANOVAs were used to compare the mean number, the mean weight and the mean size of prey items among the age classes and the a posteriori Tukey’s test was employed to locate the source of any differences (Zar, 1984). The numbers and weights of prey items were log transformed to remove the dependency of the variance on the mean (Zar, 1984). Mean number and mean weight of prey per fish in each age class was based only on specimens with food items in their stomach.

Results Age and growth Of the 1268 samples, 1024 were aged successfully. The lengths of aged individuals ranged from 31 to 140 mm (Table 1). Monthly means of MIR indicate that an annulus is formed during April–June for all ages examined (Figure 1). Up to five marks, assumed to be annuli, were visible on the scales. Two and 3 year-old fish dominated and over 95% were less than 4 years old. Differences in mean size between the successive age classes were calculated to reveal any peculiarities in growth patterns. In theory, absolute growth should be rapid at first and decrease progressively in later life. The pattern observed for S. hepatus generally agrees with these expectations (Table 1). The mean monthly length-at-age data were computed and used to estimate the parameters of both growth functions (Table 2). Results demonstrated that both models provided a good fit to the data (Figure 2).

726 M. Labropoulou et al. T 1. Summary statistics on sizes of aged Serranus hepatus from the Cretan shelf Age (years)

Sample size

Mean TL (mm)

Standard error

TL range (mm)

Mean size increment

162 212 284 340 18 8

52·55 81·34 103·10 117·27 128·22 134·48

9·32 5·26 5·79 4·83 6·69 3·78

31–73 62–92 88–119 103–128 115–139 126–140

— — 21·76 14·17 10·95 6·26

0 1 2 3 4 5 TL=total length.

The computed value of 0·49 for the winter point indicated that the lowest growth rate occurs about 6 months after the date of birth, meaning that the growth rate is reduced during the winter months.

The intercept values used in the back calculation formula were obtained from the linear regression of TL on scale radius: TL=38·52+16·48(S) r=0·95

0.35

Age 1

MIR

0.3 0.25 0.2 0.15

MIR

MIR

0.1

0.35 0.3 0.25 0.2 0.15 0.1 0.05 0

0.35 0.3 0.25 0.2 0.15 0.1 0.05 0

F

M

A

M

J

J A Month

S

O

N

D

where TL=total length (mm), S=scale radius (mm) and r=correlation coefficient. The TL at the end of each year of life was back-calculated for each individual and these lengths were averaged to obtain mean back-calculated lengths at age. The results generally agreed with lengths at age predicted by the growth models (Table 3). Feeding intensity

Age 2

F

M

A

M

J

J A Month

S

O

N

D

S

O

N

D

Age 3

F

M

A

M

J

J A Month

F 1. Mean monthly marginal increment ratio (MIR) for Serranus hepatus aged 1–3 years from the Cretan shelf. Vertical bars represent 1 standard error.

Of the 1045 stomachs of S. hepatus examined, 298 were empty (28·5%). The proportion of empty stomachs varied significantly among the age classes of fish examined (÷2 =23·82, P<0·001), with a maximum of 36·9% for the 3+ age class. The logit model revealed that there was a significant interaction between month and fish size (F=2·52, P<0·001). The slope was always <0, showing the negative allometry on full stomachs. No significant differences on the proportion of full/empty stomachs were detected between the 2 years of this study (t-test=
1·02, P>0·05). Composition of the diet There were at least 62 different prey species belonging to three major groups (decapods, amphipods and fish). Mysids and polychaetes could not be consistently identified to species level. It must also be noted

Serranus hepatus on the Cretan Shelf 727 T 2. Mean monthly length-at-age data used for fitting the von Bertalanffy growth models. Date of birth was set at 1 June (see text) Length (mm)

0·50 0·75 0·92 1·00 1·09 1·17 1·25 1·33 1·42 1·50 1·67 1·75 1·83 1·92 2·00 2·09 2·17 2·25 2·33 2·42 2·50 2·66 2·75 2·83 2·92 3·00 3·08 3·17 3·25 3·33 3·42 3·50 3·67 3·75 3·83 3·92 4·00 4·17 4·50 5·00 5·17 5·50

50·30 51·20 65·36 64·35 70·32 73·58 76·10 77·80 79·20 84·35 81·50 88·00 85·00 95·86 93·35 96·80 89·00 98·80 101·00 102·90 102·00 103·90 94·69 107·20 110·26 111·50 114·80 115·90 117·10 118·80 119·90 119·21 120·00 112·00 121·50 125·63 124·50 126·00 129·40 133·00 136·00 132·18

that the category ‘ varia ’ included exclusively echinoderms and molluscs. Decapods were the most important prey group, constituting 60·9% of the total IRI, followed by mysids (%IRI=12·6) and amphipods (%IRI=10·9) (Table 4). At the species level two natantian shrimps, Alpheus glaber (mean weight per individual: 0·200·01 g) and Processa nouveli (mean weight per individual: 0·060·01 g), the thalassinid Upogebia tipica (mean weight per individual: 0·1850·02 g) and the amphipods Apherusa

120 Total length (mm)

Age (years)

160

80

40

0

1

2

3 4 Age (years)

5

6

7

F 2. Standard (solid line) and seasonal (dashed line) von Bertalanffy growth curves fitted to monthly mean length-at-age data, for Serranus hepatus from the Cretan shelf. T 3. Back-calculated and predicted total lengths (mm) at age for Serranus hepatus from the Cretan shelf Age Standard Seasonalized (years) Back-calculated von Bertalanffy von Bertalanffy 1 2 3 4 5

62·35 90·74 110·23 121·89 129·35

65·47 91·57 109·78 122·49 131·35

66·74 92·92 111·20 123·95 132·84

chiereghinii and Phtisica marina (mean weight per individual: 0·0030·001 g) were the most exploited prey. The relative importance of fish was comparatively low (%IRI=5·88). Among fish prey, Boops boops and Gobius sp. were the species with the highest contribution in S. hepatus diet. S. hepatus exhibited a relatively high trophic diversity, with mean value of the Shannon–Wiener diversity index 2·05 (0·2). Food in relation to fish age Although %IRI of the various prey groups varied with fish age (Figure 3), there were significant differences only between ingestion of amphipods (÷2 =41·13, P<0·001) and the shrimp A. glaber (÷2 =17·27, P<0·001). Amphipods occurred in the diet of the younger specimens (0 and 1 year-old), while A. glaber

728 M. Labropoulou et al. T 4. Percentage contribution of prey groups and species to the total diet of Serranus hepatus from the Cretan shelf Prey category Decapoda Caridea Alpheus glaber Processa nouveli Other species Thalassinidea Upogebia tipica Other species Anomura Paguridae Brachyura Liocarcinus maculatus Liocarcinus sp. Other species (Total decapods) Crustacea Mysidacea Amphipoda Apherusa chiereghinii Phtisica marina Other species (Total amphipods) Polychaetes Fish Boops boops Gobius sp. Other species (Total fish) Varia No. of stomachs examined No. of empty stomachs Mean fish total length (mm) Mean stomach content weight (g) Mean number of prey items per stomach

Cn

Cw

F

IRI

%IRI

6·44 6·81 5·60

24·20 6·26 6·30

34·40 34·60 32·30

1054·0 452·8 384·3

16·30 7·00 5·94

4·00 7·06

13·70 5·95

33·80 32·90

599·8 427·9

9·28 6·62

4·71

4·96

32·50

314·5

4·86

1·89 2·76 3·03 42·30

3·04 5·21 5·13 74·70

33·50 33·90 33·30 35·00

165·3 270·3 272·0 3941·0

2·56 4·18 4·21 60·90

21·40

2·77

33·80

817·7

12·60

9·50 5·60 3·10 18·20 9·90

0·30 0·15 0·12 0·57 3·98

37·80 38·30 38·40 19·40 32·30

370·0 220·0 124·0 214·0 447·9

5·70 3·40 1·90 10·90 6·93

2·11 1·68 1·68 5·46 2·76

7·30 3·49 6·47 17·30 0·70

15·90 14·30 12·40 16·70 42·50

150·0 74·9 101·6 380·2 147·0

2·31 1·14 1·56 5·88 2·27

1045 298 88·10 0·18 2·99

Only prey species with contribution to %IRI >1 are listed. Cn, % numerical composition; Cw, gravimetric composition; F, frequency of occurrence; IRI, index of relative importance.

occurred in high percentages in 2 and 3 year-old fish. This indicates a significant change in the dietary composition of S. hepatus with age. Cluster analysis based on the IRI values for the four age classes of S. hepatus discriminated three groups, linking at 60% similarity: fish of 0 year old and 3 years old formed two different groups, while fish of 1 and 2 years old form the third. The total amount of food ingested varied significantly among the age classes (F=12·4, P<0·001). Pair-wise group comparisons showed three homogeneous groups: the mean consumption rate per individual (i.e. food age class
1) increased with increasing age; 0- and 1-year-old fish exhibited the lowest consumption rate (Table 5). The mean

number of prey items consumed decreased with age (F=6·3, P<0·001). Dietary breadth, based on the Shannon–Wiener diversity index was low in 0+ and elevated in 1+ fish, but did not change in specimens over 1 year old (Table 5). Seasonal variation Diet composition was fairly consistent over the months (Figure 4). Decapods were the most important prey throughout the year, especially during February and March when the diet was dominated by the thalassinid U. tipica. Small crustaceans occurred in the diet throughout the year and their contribution varied from 4·61% in September to 27·31% in May.

Serranus hepatus on the Cretan Shelf 729 100

100

Percent of total IRI

Percent of total IRI

90 80 70 60 50 40 30 20

80 60 40 20 0

10 0

2

1

0

A

S

O

3

D F M Month

Varia Fish Decapods

Age (years) Fish Other decapods L. maculatus Liocarcinus sp. Paguridae P. nouveli

N

U. tipica A. glaber Varia Amphipods Polychaetes Mysids

A

M

J

J

Amphipods Polychaetes Mysids

F 4. Monthly variations of Serranus hepatus diet based on the percentage index of relative importance (%IRI) values of the major prey groups.

F 3. Composition of Serranus hepatus diet from the Cretan shelf as a function of age, based on the percentage index of relative importance (%IRI) values of the major prey groups and species.

Dietary breadth varied little except for low values in February and March when U. tipica dominated (Figure 5). Predator–prey length relationship Significant positive correlations were found between the size of S. hepatus and the mean size of prey consumed (P<0·001, r2 =0·91, n=618). Furthermore, the analysis of variance on the mean prey sizes consumed by the four age classes revealed significant differences (F=176·1; P<0·001). Fish that were 0 and 1 year-old exploited prey with the smallest mean size (5·450·13 mm), 2 year-old fish consumed prey at 13·080·77 m, while the 3 year-old fish fed on the largest prey (32·460·93 mm).

Discussion It seems that the growth pattern of S. hepatus is similar to that observed for other Mediterranean demersal species, i.e. rapid body increase during the first 2 years of life (Caddy, 1988). Marginal increment analysis demonstrated the annual periodicity of rings one to three suggesting the potential use of scales for ageing of the species. However, validation of the ageing method is required to prove the periodicity of all rings observed in the samples (Beamish & McFarlane, 1983). The latter is generally difficult by means of marginal increment analysis as the growth of the different hard-parts used for ageing is significantly reduced at older ages. Despite this drawback, marginal increment analysis remains a useful tool, as it gives at least some evidence about the time of annulus formation. The method has been successfully used in the past to prove the annual periodicity of rings observed on otoliths, scales and spines of different demersal and pelagic species (Davies, 1977; Wenner et al., 1986; Maceina et al., 1987; Tserpes &

T 5. Feeding indices of Serranus hepatus from the Cretan shelf, in relation to age

Age (years) 0 1 2 3

No. of stomachs analysed

No. of full stomachs

29 367 603 46

24 261 433 29

Mean no. of prey items per stomach 3·05 3·83 2·55 2·00

(0·47) (0·31) (0·15) (0·33)

Mean weight of prey items (g) per stomach 0·03 0·11 0·19 0·38

(0·01) (0·01) (0·01) (0·08)

No. of prey species

Diet breadth Shannon–Wiener index

14 52 41 17

1·72 2·39 2·03 2·02

730 M. Labropoulou et al.

Trophic diversity (H' )

2.5 2 1.5 1 0.5 0

A

S

O

N

F D Month

M

A

M

J

J

F 5. Monthly variations of the diet breadth (Shannon–Wiener diversity index H ) for Serranus hepatus from the Cretan shelf. Vertical bars represent 1 SE.

Tsimenides, 1995). If S. hepatus in Cretan waters spawns in spring or early summer, as happens in north-west Mediterranean areas (Sabate´s, 1990), it can be speculated that the formation of annuli from April to June coincides with the reproduction of the species. This suggests that annulus formation is related to the reproductive process which seems to delay the somatic growth. However, since the application of the seasonalized growth function revealed a reduction of the somatic growth in winter, annulus formation in spring could also reflect this reduction. The composition of food suggests that S. hepatus is a carnivorous species that relies on epibenthic invertebrates mainly decapods. Despite the large number of taxa found in the stomach contents, only a few species accounted for most of the %IRI of prey consumed. Furthermore, the fact that the mean number of prey items per stomach was small with a tendency to decrease with fish age, indicates an active selection for prey taxa of large size and supports the predatory character of the species. Although S. hepatus is a small-sized demersal species the morphology of its feeding apparatus (Labropoulou & Eleftheriou, 1996) accounts for its ability to prey upon large, motile crustaceans. Also noteworthy is the fact that the brown comber displayed a high incidence of observable regurgitation, especially the specimens of the oldest year classes. It is recognized that predatory fish which eat large prey have a large distendable oesophagus (Bowen, 1983). These observations made it apparent that the combination of the presence of a closed gas bladder and digestive tract morphology adapted to the ingestion of large organisms influenced observable regurgitation in S. hepatus. Expansion of gas within the bladder, resulting from a decrease in outside pressure as the trawl is rapidly brought to the surface, enlarges the bladder and as a result of the

increase in pressure within the body cavity, food in the stomach is expelled. Almost the same prey taxa occurred in the stomachs of all four age groups. There were, however, differences between the age groups in the relative proportions of each taxon. No two age groups had the same distribution of the major food items. Moreover, specimens of each age class showed a further trend towards segregation of their feeding niches by consuming significantly different prey sizes. There is evidence that the size differences reflect changing food preference with age and the ability of large individuals to capture larger animals as prey. Mean prey size increases with increasing predator size in order to optimize the energy return per unit effort. Trophic ontogeny in brown comber could be explained in terms of fish morphology. Width and height of mouth in the open position are linearly related to fish sizes (Ross, 1978; Stoner, 1980; Gibson & Ezzi, 1987) and increased body and mouth size permit fish to capture a broader range of prey types and sizes. The same characteristics undoubtedly explain increases in number of prey types associated with increasing body size in 0 to 3 year-old specimens. It is the simplest mechanism which could account for these dissimilarities as younger fish feed in identical areas and during the same time as older specimens (Labropoulou, 1995). Similar findings have also been reported for other fish species (Ware, 1972; Ross, 1977; Grossman, 1980; Stoner & Livingston, 1984; Pearre, 1986). The relatively high percentage of empty stomachs found in older fish suggests that feeding intensity is low in older specimens and it is indicative of a decreased rate of metabolism typical of larger (older) fish. Furthermore, there was a general tendency for the mean number of prey eaten to decrease and for food bulk to increase with age; instead of consuming increasing numbers of small prey the fish began to take smaller numbers of larger prey. Larger fish would become satiated more quickly since they consume larger prey. Feeding intensity and frequency are directly correlated with meal size and digestion time (Fange & Grove, 1979; Grove & Crawford, 1980), therefore, larger specimens exhibited a lower feeding frequency than the younger ones. A similar tendency has been reported for many fish species (e.g. Smith & Page, 1969; Martin, 1970; Kislialioglu & Gibson, 1976; Werner, 1979; Robb & Hislop, 1980) and it is related to the energetic cost of obtaining their food. As the metabolic activity decreases with the age or size (Davis & Warren, 1971; Webb, 1978; Brett & Groves, 1979; MacPherson & Duarte, 1991), it becomes more beneficial for the larger fish to obtain more bulk at a

Serranus hepatus on the Cretan Shelf 731

lower rate of energy expenditure. In addition to being cost-effective, in energy terms this change in the food niche with increasing size would tend to reduce intraspecific competition between the members of the different age classes. The low vacuity index of the brown comber throughout the sampling period is indicative of food abundance and probably frequent feeding activity. Sarker et al. (1980) and Stoner (1980) considered the high percentage of stomachs containing food as an indicator of food availability. It is also likely that food availability and possibly food quality may be influencing the growth rates of the fish. Cowen (1986) has found the sheephead, Semicossyphus pulcher, to grow slower and thereby remain smaller at sites with low prey availability. Resource availability has been shown to influence age and size at maturity in genetically similar fish (Reznick, 1990; Fox & Keast, 1991). Further studies could allow these hypotheses to be examined in the case of S. hepatus. References Bagenal, T. B. & Tesch, F. W. 1978 Age and growth. In Methods for Assessment of Fish Production in Fresh Waters (Bagenal, T. B., ed.). Blackwell, Oxford, pp. 101–136. Berg, J. 1979 Discussion of methods of investigation of the food of fishes with reference to a preliminary study of the prey of Gobiusculus flavencens. Marine Biology 50, 263–273. Beamish, R. J. & McFarlane, G. A. 1983 The forgotten requirements for age validation in Fisheries Biology. Transactions of the American Fisheries Society 112, 735–743. Bowen, S. H. 1983 Quantitative description of the diet. In Fisheries Techniques (Nielsen, L. A. & Johnson, D. L., eds). American Fisheries Society, Bethesda, pp. 325–336. Brett, J. R. & Groves, T. D. D. 1979 Physiological energetics. In Fish Physiology (Hoar, W. S., Randall, D. J. & Brett, J. R., eds). Academic Press, New York, pp. 279–352. Brusle´, S. 1983 Contribution to the sexuality of a hermaphroditic teleost, Serranus hepatus L. Journal of Fish Biology 22, 283–292. Caddy, J. F. 1988 Comments of yield calculation presented at recent GFCM Technical Consultations on fish stock assessment. FAO Fisheries Report 412, 201–206. Carrasso´n, M., Steganescu, C. & Cartes, J. E. 1992 Diets and bathymetric distributions of two bathyal sharks of the Catalan deep sea (western Mediterranean). Marine Ecology Progress Series 82, 21–30. Cowen, R. K. 1986 Site-specific difference in the feeding ecology of the California sheephead, Semicossyphus pulcher (Labridae). Environmental Biology of Fishes 16, 193–203. Davies, G. E. & Warren, C. E. 1971 Estimation of food consumption rates. In Methods for Assessment of Fish Production in Fresh Waters (Ricker, W. E., ed.). Blackwell, Oxford, pp. 227–248. Davies, T. L. O. 1977 Age determination and growth of the freshwater catfish Tandanus tandanus Mitchell, in the Gwydir River, Australia. Australian Journal of Marine and Freshwater Research 28, 119–137. Fange, R. & Grove, D. 1979 Digestion. In Fish Physiology (Hoar, W. S., Randall, D. J. & Brett, J. R., eds). Academic Press, New York, pp. 161–260. Field, J. G., Clarke, K. R. & Warwick, R. M. 1982 A practical strategy for analysing multispecies distribution patterns. Marine Ecology Progress Series 8, 37–52.

Fox, M. G. & Keast, J. A. 1991 Effect of overwinter mortality on reproductive life history characteristics of pumpkinseed (Lepomis gibbosus) populations. Canadian Journal of Fisheries and Aquatic Sciences 48, 1792–1799. Gibson, R. N. & Ezzi, I. A. 1987 Feeding relationships of a demersal fish assemblage on the west coast of Scotland. Journal of Fish Biology 31, 55–69. Grossman, G. D. 1980 Ecological aspects of ontogenetic shifts in prey size utilization in the Bay goby (Pisces: Gobiidae). Oecologia 47, 233–238. Grove, D. & Crawford, C. 1980 Correlation between digestion rate and feeding frequency in the stomachless teleost Blennius pholis L. Journal of Fish Biology 16, 235–247. Hacunda, J. S. 1981 Trophic relationships among demersal fishes in a coastal area of the gulf of Maine. Fishery Bulletin 79, 775–788. Hyslop, E. J. 1980 Stomach contents analysis: a review of methods and their application. Journal of Fish Biology 17, 411–429. Kislialioglu, M. & Gibson, R. N. 1976 Prey ‘ handling time ’ and its importance in food selection by the 15-spined stickleback, Spinachia spinachia (L). Journal of Experimental Marine Biology and Ecology 25, 151–158. Krebs, C. J. 1989 Ecological Methodology Harper & Row, New York. Labropoulou, M. 1995 Feeding ecology of the demersal fish species in Iraklion Bay. Doctoral dissertation. University of Crete, Iraklion (in Greek with English abstract). Labropoulou, M. & Eleftheriou, A. 1996 The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. Journal of Fish Biology 50, 324–340. Lee, R. M. 1920 A review of the methods of age and growth determination in fishes by means of scales. Fishery Investigation London Series 2, 32. Maceina, M. J., Hata, D. N., Linton, T. L. & Landry, A. M. Jr. 1987 Age and growth analysis of spotted seatrout from Galveston Bay, Texas. Transactions of the American Fisheries Society 116, 54–59. MacPherson, E. & Duarte, C. M. 1991 Bathymetric trends in demersal fish size: is there a general relationship? Marine Ecology Progress Series 71, 103–112. Martin, N. V. 1970 Long-term effects of diet on the biology of the lake trout and the fisher in Lake Opeongo, Ontario. Journal of the Fisheries Research Board of Canada 27, 125–146. Pearre, S. Jr. 1986 Ratio-based trophic niche breadths of fish, the Sheldon spectrum and the size efficiency hypothesis. Marine Ecology Progress Series 27, 299–314. Pinkas, L., Olipham, M. S. & Iversor, I. L. K. 1971 Food habits of albacore, bluefin tuna and bonito in California waters. Fishery Bulletin 152, 1–105. Reznick, D. N. 1990 Plasticity in age and size maturity in male guppies (Poecilia reticulata): an experimental evaluation of alternative models of development. Journal of Evolutionary Biology 3, 185–203. Robb, A. P. & Hislop, J. R. G. 1980 The food of five gadoid species during the pelagic 0-group phase in the northern North Sea. Journal of Fish Biology 16, 199–217. Ross, S. T. 1977 Patterns of resource partitioning in searobins (Pisces: Triglidae). Copeia 1977, 561–571. Ross, S. T. 1978 Trophic ontogeny of the leopard searobin, Prinotus scitulus (Pisces: Triglidae). Fishery Bulletin 76, 225–234. Sabate´s, A. 1990 Distribution pattern of larval fish populations in the Northwestern Mediterranean. Marine Ecology Progress Series 59, 75–82. Sarker, A. L., Al-Daham, N. K. & Bhatti, M. N. 1980 Food habits of the mudskipper, Pseudapocryptes dentatus (Val.). Journal of Fish Biology 17, 635–639. Smith, P. W. & Page, L. M. 1969 The food of spotted bass in streams of the Wabash River drainage. Transactions of the American Fisheries Society 98, 647–651.

732 M. Labropoulou et al. Sparre, P. & Venema, S. C. 1992 Introduction to tropical fish stock assessment. Part I—Manual. FAO Fisheries Technical Paper 306/1, 376. Stoner, A. W. 1980 Feeding ecology of Lagodon rhomboides (Pisces: Sparidae): variation and functional responses. Fishery Bulletin 78, 337–352. Stoner, A. W. & Livingston, R. J. 1984 Ontogenetic patterns in diet and feeding morphology in sympatric sparid fishes from seagrass meadows. Copeia 1984, 174–187. Tserpes, G. & Tsimenides, N. 1995 Determination of age and growth of swordfish, Xiphias gladius L., 1758, in the eastern Mediterranean using anal-fin spines. Fishery Bulletin 93, 594–602. Tsimenides, N., Tserpes, G., Machias, A. & Kallianiotis, A. 1991 Distribution of fishes on the Cretan shelf. Journal of Fish Biology 39, 661–672. Ware, D. 1972 Predation by rainbow trout (Salmo gairdneri): the influence of hunger, prey density and prey size. Journal of the Fisheries Research Board of Canada 29, 1193–1201.

Wilkinson, L. 1988 Systat: the System for Statistics. Systat Incorporation, Evaston. Webb, P. W. 1978 Partitioning of energy into metabolism and growth. In Ecology of Freshwater Fish Production (Gerking, S. D., ed.). Blackwell, Oxford, pp. 184–214. Wenner, C. A., Roumillat, W. A. & Waltz, C. W. 1986 Contributions to the life history of black sea bass, Centropristis striata, off the southeastern United States. Fishery Bulletin 84, 723–741. Werner, E. E. 1979 Niche partitioning by food size in fish communities. In Predator–prey Systems in Fisheries Management (Stroud, R. & Clepper, H., eds). Sport Fishing Institute, Washington, pp. 311–322. Whitehead, P. J. P., Bauchot, M. L., Hureau, J. C., Nielsen, J. & Tortonese, E. (eds) 1986 Fishes of the North-eastern Atlantic and the Mediterranean. Unesco, Paris. Zar, J. H. 1984 Biostatistical analysis. Prentice-Hall, Englewood Cliffs.