- Email: [email protected]
Feeding habits of red mullet (Mullus barbatus) in a gulf in western Greece
Fisheries Research, 16 (1993) 69-83
69
Elsevier Science Publishers B.V., Amsterdam
Feeding habits of red mullet (Mullus a gulf in western Greece
barbatus) in
V. Vassilopoulou and C. Papaconstantinou National Centre for Marine Research, Agios Kosmas Hellinikon, Athens 166 04, Greece (Accepted 29 June 1992)
ABSTRACT Vassilopoulou, V. and Papaconstantinou, C., 1993. Feeding habits of red mullet (Mullus barbatus) in a gulf in western Greece. Fish, Res., 16: 69-83. The stomach contents of red mullet collected in the Amvrakikos Gulf of Greece during five samplings between November 1986 and February 1987 were analysed. Fullness indices fluctuated in relation to month and area of capture. Significantly greater quantities of food were found in the stomachs of specimens in the western part of the Gulf in September. Polychaetes were the primary food item in three of the five samplings. Bivalves, the second most important prey, showed great seasonal fluctuations. Crustaceans were third, while gastropods, echinoids and sipunculids, although occurring frequently in the stomachs, were of minor importance. There were differences in quantity and, to a lesser degree, quality between the diet of male and female red mullet, possibly related to sexual differences in growth rate. Cluster analysis revealed that the prey species composition in the stomachs of red mullet was influenced by area of capture rather than fish length. Possible relations of food availability to the migration pattern of the species are also discussed.
INTRODUCTION
Estuaries and enclosed bays frequently form essential feeding and/or breeding grounds for commercially important fish (UNESCO, 1977). Red mullet from the Amvrakikos Gulf provide a considerable income for fishermen in the area. However, there is an emigration from the Gulf of individuals having completed their second year of life (fork length, >150 mm), thus limiting the local fishery. Among the factors influencing fish migrations are feeding habits and/or starvation (Harden-Jones, 1968; Nikolsky, 1976). Information on the feeding habits of juvenile red mullet along the Mediterranean coast is limited (Froglia, 1988), but adult specimens have been studied by several authors (Planas and Vives, 1956; Haidar, 1970; Jukic, 1972; Caragitsou and Tsimenidis, 1982; Papaconstantinou and Caragitsou, 1987 ). Correspondence to: V. Vassilopoulou, National Centre for Marine Research, Agios Kosmas Hellinikon, Athens 166 04, Greece.
© 1993 Elsevier Science Publishers B.V. All rights reserved 0165-7836/93/$06.00
70
V. VASSILOPOULOUAND C. PAPACONSTANTINOU
The objectives of this study were to describe the feeding habits of red mullet in the Amvrakikos Gulf, evaluating possible effects of season, area of capture and fish size on stomach contents. MATERIALS AND METHODS
Amvrakikos Gulf is a semi-enclosed bay in western Greece, with a maximum depth of approximately 60 m (Fig. 1 ). It connects with the Ionian Sea by a 600 m wide channel at its northern end and the Louros and Arachthos rivers discharge into its northern part. The stomachs of 403 red mullets, landed by trammel bottom nets in the Amvrakikos Gulf, were examined (Fig. 1 and Table 1 ). Five samplings took place at 22 sites with depths ranging from 3 to 18 m from November 1986 to September 1987. The abdominal cavity of each fish was opened and the whole fish was immediately immersed and preserved in a 6% buffered formaldehyde solution. In the laboratory, samples were segregated by month, area of capture (western-outer and eastern-inner parts), sex and size of fish (three length groups were formed according to fork lengths of fish; 100-120 mm, 120-140 mm and 140-160 m m ) . For each specimen, length to the nearest millimetre, weight .
z
° I
~:..:
I
I
.'i'. . .-.'~
..
o
•
."
'!..-.....
W ""1~
®
: : "•:' ~ ,• ' '~°~ • : • :
®
20.45
ii : ....
20.50 I
j
::
"
20.55 I
LONGITUDE
I
;..'~(:..~
•
"::
I
I
I
":A..'::..
,, ..'.'.:.""
:'.:, ~i~" ®
®~)'l,'~'.:;i" :®~~i ':;i:;'i"~i~'."!:'}'|':;'.....
"".-i:e
2!.00 I
i:.i..
21.05 I
2"1.10 I
(°E)
Fig. I. Location of sampling stations for red mullet in the Amvrakikos Gulf. ( • western-outer, ® eastern-inner parts).
FEEDING HABITSOF RED MULLET IN WESTERN GREECE
71
TABLE1
Total numbers of individual red mullet examined, number of empty stomachs, mean degree (L) and mean index (B) of stomach fullness with 95% confidence intervals (a) from November 1986 to September 1987, (b) for each length group and (c) for the eastern and western part of the Amvrakikos Gulf November
February
May
July
September
63 0 1.87-+0.22 0.59_+0.11
93 0 2.48_+0.19 1.15+0.08
(a) No. of stomachs No. of empty stomachs Degree of fullness (L) Index of fullness (B)
92 0 2.39-+0.23 0.91_+0.08
84 0 2.15+0.19 0.85+0.09
71 5 1.38+0.18 0.42_+0.15
(b) No. of stomachs No. of empty stomachs Degree of fullness (L) Index of fullness (B)
10-12 cm 79 0 2.44_+0.21 1.07_+0.12
12-14 cm 285 2 2.24+0.12 0.76+0.06
14-16 cm 39 3 2.05-+0.39 0.69-+0.13
(c) No. of stomachs No. of empty stomachs Degree of fullness (L) Index of fullness (B)
Western 270 1 2.17_+0.13 0.90_+0.07
Eastern 128 4 2.02+0.17 0.65_+0.07
to the nearest gram and sex were recorded. Gonadal maturity was determined according to Nikolsky's scale (1976) (Stages I, II, III immature gonads; IV, V mature; VI spent). The degree of fullness (L) was estimated for individual stomachs according to Lebedev's scale (1946), ranging from 0 (empty) to 5 (stomach fully distended with food). Measures of food intake were determined by calculating an index of fullness (B: wet weight of stomach contents as a percentage of total body weight of each predator; Hyslop, 1980). Index values were loglo transformed and subjected to multiple analysis of variance (MANOVA) to evaluate the orders of importance of the key factors (season, area of capture and size of fish) determining variability in the stomach contents. Prey items were identified to the most precise taxonomic level possible and counted and weighed to the nearest 0.01 g. Frequency of occurrence as a percentage (F), number (Cn) and weight (Cw) of each prey item were calculated. Complementary clustering (group average strategy) using the Bray-Curtis similarity coefficient (Bray and Curtis, 1957) was performed on the Cw of each prey item in each season and in each length group in the two areas of the Amvrakikos Gulf, using the PRIMER algorithms (Clarke and Warwick, 1989). Diet similarity was determined using Schoener's index (1970) S= 1-0.5
(,SIPxi-PyiI)
V. VASSILOPOULOUANDC. PAPACONSTANTINOU
72
where Px~ and Px were the proportions by weight (Cw) of prey i in seasons or areas or length groups x and y, respectively. The index values were compared with Langton's convention (1982), in which values of 0.00-0.29, 0.30-0.60 and greater than 0.60 reveal low, medium and high similarity, respectively. RESULTS
Feeding intensity The length frequency distributions of male and female red mullet are presented in Fig. 2. Among the 403 specimens examined, none exhibited signs of starvation (small and reddish liver because of fat loss, darker colour of the gall, gall bladder increased in volume). Five red mullet, all from the May sampling, had empty stomachs. The degree (L) and the index (B) of stomach fullness in each month, area of capture and length group are presented in Table 1. Multiple analysis of variance applied to the data revealed that both month and area of capture had a significant effect on L and B (MANOVA: FL=7.356, FB=7.031, P<0.001 ). The application of the five month data of analysis of variance (ANOVA: FL= 18.32, P<0.001; FB=23.351, P<0.01 ) and multiple range tests showed that both L and B were significantly lower in May and July. Geographically, red mullet from the western part of the Gulf exhibited significantly higher L and B values, as compared with those from the eastern part. On the other hand, the fish length had an insignificant influence on fullness indices in relation to month (MANOVA: FL = 0.695, P = 0.6963; Fu= 1.393, P=0.1977) and area of capture (MANOVA: FL=0.162, P=0.8508; Fs= 0.411, P=0.663). Mal~s~
(%)
F~mal~sI
30-
Nm :159 NF :244
252015-
._L
1o. 5o 9
F L
(crn]
Fig. 2. Length frequency distributions of male and female red mullet caught in the Amvrakikos Gulf, November 1986-September 1987.
FEEDING HABITS OF RED MULLET IN WESTERN GREECE
73
General feeding trends Red mullets feed by the 'slurp' method; they swim over muddy bottoms, sucking up and sifting through large quantities of mud. Mud and small stones were found in the stomachs of many of the specimens. Overall, in terms of percentage by weight, the stomach contents consisted mostly of polychaetes (51.9%), bivalves (30.2%), crustaceans ( 8.92% ) and sipunculids (3.6%) (Table 2 ). Among the identified polychaetes, Pectinaria koreni, Sternaspis scutata, Sabella pavonina, Lumbriconereis impatiens and Sthenelais boa made up the 19.2% of the estimated weight of the stomach contents. Tellina spp. and Loripes spp. were dominated by weight among the identified bivalves. Crustaceans were represented mainly by amphipods (almost exclusively Ampelisca diadema, 0.71%), decapods (0.09% each of Callianassa tyrrheni and Processa canaliculata ) and mysids (mostly Leptomysis mediterranea, 0.18%). The sipunculid Aspidosiphon muelleri accounted for the 3.6% of the weight of the stomach contents. The Foraminifera sp. Elphidium crispum was quite numerous but did not contribute much to the weight.
Monthly variations in stomach contents Polychaetes predominated in terms of percentage number (Cn), weight
(Cw) and frequency of occurrence (F) in February, May and July. Bivalves dominated the stomach contents in September but were not present in May; they were, however, the second most important prey during the other months investigated (Table 3 ). In November, both polychaetes and bivalves were of similar importance. Crustaceans, the third major taxon, increased in importance in May. Relatively small seasonal fluctuations existed within the rest of the prey taxa. Cluster analysis at the 60% similarity level indicated three major groupings of months (Fig. 3 ). The major group (Group I) comprised July, September and November, while February (Group II) and May (Group III) formed separate groups. The major difference separating Groups I and II was due to sedentary polychaetes, particularly Sternaspis scutata, which was quite important in terms of weight (27.2%) in February, but was non-existent in stomachs during the rest of the year. Groups I and III were mainly separated on the basis of bivalves that displayed the greater differences of presence in the stomach contents, as compared with other prey taxa. The separation of Groups II and III was primarily due to the high percentage by weight (74%) of sedentary polychaetes (Sternaspidae, Amphictenidae and Sabellidae) in February, while in May the stomach contents mainly consisted (67%) of errant polychaetes (Eunicidae and Glyceridae) and crustaceans (Amphipoda and Decapoda).
74
v. VASSILOPOULOUANDC. PAPACONSTANTINOU
TABLE2 Per cent by weight (Cw) of items in the stomachs of red mullet in the Amvrakikos Gulf, November 1986 to September 1987 Prey Mycophyta Lyngbya spp. Rhizopoda Foraminifera Elphidium crispum Cnidaria Anthozoa Annelida Polychaeta unidentified Aphroditidae unidentified Leanira spp. Sthenelais boa Eunicidae unidentified Eunice vittata E. rousseaui Hyafinoecia bifineata H. brementi Lumbriconereis impatiens L. gracilis Glyceridae unidentified Glycera con voluta Goniada spp. G. maculata Nereidae unidentified Micronereis variegata Nereis caudata Nepthydidae Nepthys spp. Syllidae unidentified Exogonia spp. Syllis variegata S. cornuta Ampharetidae unidentified Amphictenidae Pectinaria koreni Capitellidae Notomastus latericeus Maldanidae unidentified Maldane sarsi Sabellaridae unidentified Pallacia spp. P. cirrata Sabeilidae unidentified Sabella pavonina Spionidae Laonice cirrata Sternaspidae Sternaspis scutata Terebellidae unidentified Amphitrite spp. Terebellides stroemi
Cw 0.02
0.93 0.02 18.92 2.00 0.11 0.55 2.37 0.07 0.07 0.04 0.02 0.71 0.47 2.73 O.13 0.04 0.02 0.67 0.04 0.07 0.02 1.26 0.04 0.16 0.04 0.04 9.94 0.22 O.13 0.04 0.24 0.47 O.18 1.82 2.21 0.04 5.73 0.20 0.02 0.03
Prey
Trichobranchus glacialis Sipunculida Aspidosiphon mulleri Arthropoda Crustacea unidentified Copepoda unidentified Ostracoda unidentified Amphipoda unidentified Gammaridae unidentified .4mpelisca diadema Hyale schmidti Caprellidae unidentified Phtisica marina Anisopoda unidentified Apseudes latreilli Cumacea unidentified Pseudocuma longicorniz Euphausiacea unidentified Euphausia krohni Isopoda unidentified Eurydice truncata Mysidacea unidentified Paramysis helleri Leptomysis mediterranea Siriella clausi Anchialina agilis Decapoda unidentified Brachyura unidentified Callianassa tyrrhena Processa canaliculata MoUusca Bivalvia unidentified Nuculana fragilis N. pella Loripes spp. Tellina spp. Thracia spp. Gastropoda unidentified Turitella communis Philine spp. Scaphopoda Dentalium spp. Echinodermata Echinoidea unidentified Echinocyamus pusillus Asteroidea Astropecten spp. Ophiuroidea unidentified Ophioderma longicauda Vertebrata Osteichthyes
Cw 0.04 3.63 3.03 0.08 0.09 0.26 0.22 O.71 0.02 0.11 0.09 0.09 O.11 0.09 0.02 0.04 0.02 0.33 0.07 0.60 0.01 O.18 0.02 O.11 2.35 0.09 0.09 0.09 28.12 O.11 0.04 0.20 1.62 0.11 1.97 0.04 0.01 0.02 0.80 0.93 0.11 0.01 0.02 0.40
F E E D I N G H A B I T S O F R E D M U L L E T IN W E S T E R N G R E E C E
TABLE
75
3
Seasonal variation of the Cw ( % by weight) of prey in stomach contents of the red mullet in the A m v r a k i k o s Gulf, November 1986 to September 1 9 8 7 Prey
November Cn Cw
Oscillatoriaceae Foraminifera Anthozoa Polychaeta
February Cn Cw
*
*
7.9
*
*
*
*
.
May Cn
July Cn
Cw
September Cn Cw
Cw
-
-
-
*
*
*
*
*
5.3
*
37.0
4.5
9.9
*
.
.
.
.
.
.
18.1
23.6
12.1
9.0
18.8
23.4
12.7
24.6
11.8
19.6
Errantia
7.6
7.4
15.2
7.4
27.0
31.5
6.3
8.2
17.3
15.8
Sedentaria
9.7
7.5
53.8
63.2
12.7
18.7
2.3
8.1
3.4
2.4
Sipunculida
3.5
4.9
.
*
1.2
6.0
6.6
Crustacea
7.8
3.1
-
7.6
7.2
4.1
1.7
Copepoda
*
*
.
.
.
.
*
*
-
-
Ostracoda
*
*
.
.
.
.
*
*
*
*
Amphipoda
2.6
*
4.8
1.2
7.1
3.7
5.4
3.9
1.2
*
Anisopoda
*
*
-
-
2.5
2.0
1.0
*
*
*
Cumacea
*
*
-
-
*
*
*
*
-
-
Euphausiacea
.
. -
. 21.3
15.6
-
-
-
*
*
-
-
*
*
Isopoda
1.0
*
-
*
*
*
-
-
*
Mysidacea
3.3
1.0
3.6
1.0
2. 1
1.2
2.6
2.1
*
*
Decapoda
*
3.3
4.4
3.4
2.1
2.4
2.9
5.5
*
*
21.9
38.8
4.0
5.8
-
-
10.2
27.1
31.5
47.0
Gastropoda
6.0
1.6
1.2
-
-
7.8
3.0
12.2
3.7
Scaphopoda
*
*
.
.
.
.
*
1.0
-
-
Echinoidea
7.5
5.5
.
.
.
.
1.2
1.4
*
*
Asteroidea
*
*
.
.
.
Ophiuroidea
.
*
*
Osteichthyes
*
-
-
Bivalvia
*Prey category
.
. *
present, but less than
*
. .
* 1.0%
. .
8.7
of the total
.
. .
-
-
*
1.0
v~6ight.
Differences in stomach contents between males and females The stomach contents of males and females mainly differed in quantity and only to a lesser degree in species of the ingested food. Within the same length group the mean stomach content weights of the two sexes (Fig. 4) were significantly different at the 95% significance level; stomachs of females contained more food than those of males (tll-12 cm=2.008, t12-13 cm=2.313, tl 3-14c m "~- 2.077, t14-15 cm = 2.692 ). The t test was not applied on data derived from specimens smaller than 11 cm and larger than 15 cm because of their small numbers. Small qualitative differences appeared between the two sexes. Although polychaetes dominated in all stomachs they were relatively reduced in males, which also seemed to prefer crustaceans and molluscs (Table 4 (a)).
76
V. VASSILOPOULOUANDC. PAPACONSTANTINOU
0" 10" 2030~ 40~
>-
50~
F-
E< .J
60 ~ 70~
80-
90-
100 \5
J
/
M
F
ml
Group ]
Group liT Group
Fig. 3. Dendrogram showing groupings of months, using Bray-Curtis index, based on prey (Cw) in the stomach of red mullet in the Amvrakikos Gulf. (N, November; F, February; M, May; J, July; S, September. )
Variations in stomach contents relative to fish length There were small qualitative differences in the stomach contents of the three length groups; an increase in the proportion by weight of molluscs and crustaceans and a decrease of polychaetes existed within specimens of lengths 1014 cm compared with larger ones (Table 4(b) ). Cluster analysis was performed on the stomach contents of the three length groups at the two areas (Fig. 5 ). High qualitative similarity of the stomach contents in relation to fish length was found in the western part of the Gulf (Group I ). On the other hand, in the eastern Amvrakikos the few larger specimens ( N = 7 ) belonging to the 14-16 cm length group (Group III ) were separated from the smaller ones (Group II), mainly due to the high proportion by weight of Sternaspis scutata in the stomachs of the larger fish.
FEEDING HABITS OF RED MULLET 1N WESTERN GREECE
"--
"-- Moles
H
77
Fernoles
0.5 0.4 ~o 0.3,.J -C u t3
E
0.2-
0.1
0
0
c0
!
9
I'0
3:
!
11
Fish
12 length
13
I'4
15
(cm)
Fig. 4. Mean weight of stomach contents versus fish length (with 95% confidence intervals) of male and female red mullet from the Amvrakikos Gulf. TABLE 4 Per cent by weight (Cw) of the major prey taxa ingested by red mullet (a) males and females, (b) fish of various lengths and (c) fish collected in the western and eastern Amvrakikos Gulf Prey
For.
Mol.
Pol.
Cru.
Sip.
Ech.
Others
0.77 0.99
35.35 30.15
45.62 61.39
12.28 3.39
2.67 2.75
2.49 1.62
0.84 0.72
0.77 0.96 1.11
40.98 38.76 31.84
42.79 44.56 59.66
8.51 7.04 5.26
3.97 4.06 !.07
1.60 1.98 0.71
1.36 2.68 0.36
1.20 0.2 i
33.79 29.57
48.62 53.96
8.06 11.50
4.13 3.09
1.58 0.88
2.63 0.88
(a) Sex Male Female
(b) Length (cm) 10-12 12-14
14-16
(c) Area Western Eastern
For., Foraminifera; Mol., Mollusca; Pol., Polychaeta; Cru., Crustacea; Sip., Sipunculida; Ech., Echinoidea.
Geographical variations in stomach contents The proportion by weight of the major prey categories in the two parts of the gulf are presented in Table 4(c). In all, 24 prey taxa were identified in the western part and 21 in the eastern. Polychaetes were dominant in both parts of the Amvrakikos, mainly Amphictenidae species in the western part, but with Sternaspidae also in the eastern part. Molluscs, represented almost ex-
78
V. VASSILOPOULOU AND C. PAPACONSTANTINOU OI020-
o~ 30>m 40r~ < .3
5060-
~r
70-
I
tn
80" 90100 EL
\EM
Group 111
E$/ v G r o u p ]I
\WL
WM "v Group
W$/ I
Fig. 5. Dendrogram showing groupings of fish length and area of capture, using Bray-Curtis index, based on prey (Cw) in the stomach of red mullet in the Amvrakikos Gulf. (EL, eastern Amvrakikos, large specimens; EM, eastern, medium; ES, eastern, small; WL, western, large; WM, western, medium; WS, western, small. )
clusively by bivalves, were of equal importance in both parts. Small differences also existed within crustaceans, sipunculids and echinoids. Cluster analysis revealed that at the 73% similarity level, fish from the western part of the Gulf (Group I) were separated from those of the other parts (Fig. 5).
Dietary overlap Dietary overlap, calculated on the basis of percentage by weight (Cw), of prey found in fish stomachs indicated changes in the prey spectrum in relation to season. There was a considerable similarity in November, July and September (Table 5(a) ), the months that form Group I in Fig. 3. The decrease of the species' niche breadth in February and May decreased Schoener's index. In relation to fish length, the overlap index presented high values (Table 5 (b) ), probably due to the small range of fish lengths involved. There was also a high similarity ( S = 0.76) between the mullet collected in the two different parts of the Gulf.
FEEDING HABITS OF RED MULLET IN WESTERN GREECE
79
TABLE 5 Schoener's indices o f dietary overlap between red mullet o f ( a ) different m o n t h s and ( b ) different length groups in the Amvrakikos G u l f f r o m 1986 to 1987 (a)
November
February
May
July
February May July September
0.37 0.63 0.84 0.77
0.43 0.34 0.23
0.49 0.57
0.77
(b)
10-12 cm
12-14 cm
12-14 cm 14-16cm
0.76 0.57
0.65
DISCUSSION
Red mullet in the Amvrakikos Gulf is benthophagous, feeding on infaunal and epifaunal invertebrates, primarily polychaetes, bivalves and crustaceans. Sipunculids, gastropods and echinoids, although eaten regularly, were of minor importance. Daniels ( 1982 ) reported that fish using the 'slurp' method of foraging, usually take sedentary polychaetes and slow-moving invertebrates. Red mullet in Israeli waters fed mainly on polychaetes, molluscs, echinoderms and to a lesser degree fish (Wirszubski, 1953 ). In Spanish waters (Planas and Vives, 1956 ) and in the Adriatic Sea (Haidar, 1970), stomachs of red mullet included primarily decapods, followed by polychaetes and bivalves. The major prey items ingested by red mullet in the Aegean Sea (Caragitsou and Tsimenidis, 1982), as well as in the western Greek Seas (Papaconstantinou and Caragitsou, 1987 ) were amphipods, decapods, mysids and polychaetes. The pattern of activity in the Amvrakikos Gulf throughout the year is intensive feeding in the winter, curtailment of feeding in spring and summer and resumption of feeding in the autumn, but to a higher degree than in the winter. Among polychaetes, Pectinaria koreni dominated in terms of number, weight and frequency of occurrence, except in February, when the higher Cw value was found to coincide with Sternaspis scutata. On the other hand, bivalves, predominating in the stomach contents in September, were not observed in the stomachs in May. Seasonal changes in feeding habits were also found in red mullet from other parts of the Mediterranean (Haidar, 1970; Caragitsou and Tsimenidis, 1982 ). A number of authors have shown that, as the density of a particular prey type declines, a predator may switch to feeding on another prey which is more abundant (Murdoch, 1969; Cornell, 1976;
80
V. VASSILOPOULOU AND C. PAPACONSTANTINOU
Hume and Northcote, 1985; Davidson, 1986 ). Analysis of the benthos in the Amvrakikos Gulf, however, did not reveal corresponding variations in the benthic abundance of the various items found in the stomachs of red mullet (Bogdanos et al., 1989). Quantitative differences mainly existed in the diet of red mullet between the two parts of the Amvrakikos Gulf; larger quantities of food were found in the stomachs of specimens collected in the western Amvrakikos. Qualitatively, in the latter area there were three taxa more in the total stomach contents, as compared with the eastern part. A difference in the diversity and abundance of benthic species was also established between the two parts of the Gulf; higher diversities and abundances coincided with the western part (Bogdanos et al., 1989). The diversity of the benthos in the Amvrakikos may be influenced by the type of bottom sediment (Ignatiades et al., 1981 ), which differs between the eastern and the western parts (Piper et al., 1982) and may account for the dietary differences in red mullet. According to Piper et al. (1982) the sediments accumulating beneath 38%0 salinity water in the Gulf have a foraminiferal fauna. This observation seems to explain the relatively high values of percentage number and frequency of occurrence of Foraminifera in the stomachs. Stomachs of females contained larger quantities of food than those of males of similar size. A similar observation was made for red mullet in the Adriatic Sea (Haidar, 1970). Since growth of fish is directly related to food intake, it is not surprising that females grow faster than males (Scaccini, 1947; Papaconstantinou et al., 1981; Vassilopoulou, 1989). Larger quantities of food in the stomachs of females and faster growth was also reported for the silver hake (Merluccius bilinearis) in the northwestern Atlantic (Schaefer, 1960; Bowman, 1984). Many fish species change diet as they grow (Ross, 1978; MacPherson, 1981 ). This may result from changes in habitat and hence changes in available food sources, or it may simply be a functional response to changes in fish size and/or metabolic needs (Singer, 1985 ). In the Amvrakikos Gulf, small dietary differences appeared between length groups. This was expected, since the red mullet collected, covered a rather small range of body length (FL, 6 cm). Bivalves and crustaceans were more abundant than polychaetes in smaller red mullets. The only exception coincided with the few large specimens collected in the eastern Amvrakikos, which seemed to prefer the polychaete Sternaspis scutata. However, further studies are required to elucidate specific problems associated with prey selection in different size groups, since body length of red mullet collected in the Greek Seas usually covers an interval of 6-23 cm FL. Finally, there were no signs of starvation throughout the year in red mullet collected in the Amvrakikos Gulf, except for a small percentage of individuals
FEEDINGHABITSOF RED MULLETIN WESTERNGREECE
81
with empty stomachs in May. Hence starvation is not the reason for the migration of larger red mullets ( > 15 cm) out of the Gulf. However, the small depth of the Amvrakikos ( m a x i m u m < 60 m) and the decreased values of dissolved oxygen in the deeper waters (Friligos and Koussouris, 1977 ) create hypoxic conditions seriously affecting the benthic fauna (Bogdanos et al., 1989; Papaconstantinou and Caragitsou, 1990 ). These conditions suggest the existence of a depth limit for the distribution of red mullet in the Amvrakikos Gulf, since the species usually extends to a depth of approximately 200 m in the Greek Seas (Papaconstantinou et al., 1988 ) with an obvious trend of larger specimens to exist in deeper waters (Vassilopoulou and Papaconstantinou, 1988 ). Moreover, the shift of the species towards the Ionian Sea takes place during the second year of its life, coinciding with its first sexual maturity (Vassilopoulou, 1987). The few mature specimens collected in the framework of the present study, as well as the eggs and larvae of the species (Caragitsou et al., 1989 ) were found at sites close to the Ionian Sea channel. Hence, the Amvrakikos Gulf seems to offer a favourable habitat to relatively small ( < 16 cm) and sexually immature red mullet.
REFERENCES Bogdanos, C., Panagiotidis, P., Simboura, N. and Mastori, V., 1989. Study of the Benthos of the Amvrakikos Gulfi In: Final Report on the Oceanographic Study of the Amvrakikos Gulf 4. Biological Oceanography. National Centre for Marine Research Editions, Athens, pp. 38-47 (in Greek). Bowman, R.E., 1984. Food of silver hake, Merluccius bilinearis. Fish. Bull., 82 ( 1 ): 21-35. Bray, J.R. and Curtis, J.T., 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr., 27: 325-349. Caragitsou, E. and Tsimenidis, N., 1982. Seasonal changes of food spectrum and daytime rhythm of feeding of the red mullet (Mullus barbatus) in the Thracian Sea. Thalassographica, 5 ( 2 ): 105-115. Caragitsou, E., Vassiiopoulou, V., Petrakis, G., Papaconstantinou, C. and Fourtouni, A., 1989. The Fishery of the Amyrakikos Gulf. In: Final Report on the Oceanographic Study of the Amvrakikos Gulf. 5~, Fisheries. National Centre for Marine Research Editions, Athens, pp. 1-72 (in Greek). Clarke, K.R. and Warwick, R.M., 1989. Lecture notes prepared for the training workshop on the statistical treatment and interpretation of marine community data. FAO/IOC/UNEP, Athens, September 1989, Part II, 84 pp. Cornell, H., 1976. Search strategies and the adaptive significance of switching in some general predators. Am. Nat., 110: 317-320. Daniels, R.A., 1982. Feeding ecology of some fishes of the Antarctic peninsula. Fish. Bull., 80 ( 3 ): 575-588. Davidson, R.J., 1986. Mussel selection by the paddle crab Ovalipes catharus: evidence of a flexible foraging behaviour. J. Exp. Mar. Biol. Ecol., 102: 281-299. Friligos, N. and Koussouris, T., 1977. Preliminary chemical, physical and biological observations in the gulf of Amvrakikos (April 1974). Thalassia Jugos., 13 ( 1/2 ): 53- 58. Froglia, C., 1988. Food preferences of juvenile Red Mullet Mullus barbatus in western Adriatic
82
v. VASSILOPOULOUANDC. PAPACONSTANTINOU
nursery ground (Osteichthyes: Mullidae). Rapp. P.-V. Rfun. Inter. Comm. Sc. Expl. Medit., 3(2): 263. Haidar, Z., 1970. L'oecologie du rouget (Mullet barbatus) en Adriatique orientale. Acta Adfiat., 14 ( 1 ): 1-94. Harden-Jones, F., 1968. Fish Migration. Edward Arnold, London, 325 pp. Hume, J.M.B. and Northcote, T.G., 1985. Initial changes in use of space and food by experimentally segregated populations of Doily varden (Salvelinus malma) and cutthroat trout (Salmo clarki). Can. J. Fish. Aquat. Sci., 42: 101-109. Hyslop, E.J., 1980. Stomach content analysis - - a review of methods and their application. J. Fish Biol., 17:411-429. Ignatiades, L., Moraitou-Apostolopoulou, M. and Nikolaidou, A., 1981. Biotic Conditions. In: J. Szijj (Editor), Ecological Assessment of the Delta Area of the rivers Louros and Arachthos at the Gulf of Amvrakia. Univ. Essen Publications, Essen, pp. 31-49. Jukic, S., 1972. Nutrition of the hake (Merluccius merluccius), bogue (Boops boops), striped mullet (Mullus barbatus) and pandora (Pagellus erythrinus) in the bay of Kastela. Acta Adriat., 14 (4): 3-40. Langton, R.W., 1982. Diet overlap between Atlantic cod, Gadus rnorhua, silver hake, Merluccius bilinearis, and fifteen other northwest Atlantic finfish. Fish. Bull., 80: 745-759. Lebedev, N.V., 1946. Elementary populations offish. Zool. Zhur., 25(2): 121-135 (in Russian). MacPherson, E., 1981. Resource partitioning in a Mediterranean demersal fish community. Mar. Ecol. Prog. Ser., 4: 183-193. Murdoch, W.W., 1969. Switching in general predators: experiments on predator specificity and stability of prey predations. Ecol. Monogr., 39: 335-354. Nikolsky, G.V., 1976. The Ecology ofFish. 6th edn. Academic Press, New York, 352 pp. Papaconstantinou, C., Tsimenidis, N. and Daoulas, C., 1981. Age and reproduction of red mullet (Mullus barbatus L., 1758 ) in the gulfs of Saronikos and Thermaikos. Thalassographica, 4( l ): 39-66. Papaconstantinou, C. and Caragitsou, E., 1987. Preliminary study on the trophic relationship of red mullet (Mullus barbatus) off the western coast of Greece. Proc. 2nd Hell. Congr. Oceanogr. Fish., 14-17 May 1990, National Centre for Marine Research, Athens, pp. 577583 (in Greek). Papaconstantinou, C., Caragitsou, E., Mytilineou, C., Petrakis, G. and Vassilopoulou, V., 1988. Dynamics of demersal fish stocks in the Korinthiakos and Patraikos Gulfs and in the Ionian Sea. Part II. Thalassographica Sp. Publ. No. 16., National Centre for Marine Research, Athens, 277 p. (in Greek). Papaconstantinou, C. and Caragitsou, E., 1990. Abiotic parameters affected on the abundance offish population in the Amvrakikos Gulf. Proc. 2nd Hellemic Cypriotic Congr. Chem. Environ., 28 September-2 October 1990. Greek and Cypriotic Union of Chemists, Athens, pp. 416-420 (in Greek). Piper, D.J.W., Panagos, A.G. and Kontopoulos, N., 1982. Some observations on surficial sediments and physical oceanography of the gulf of Amvrakia. Thalassographica, 5 (2): 63-80. Planas, A. and Vives, F., 1956. Notas preliminares sobre la biologia del salmonete (Mullus barbatus). Invest. Pesq., 5:31-50. Ross, S.T., 1978. Trophic ontogeny of the leopard searobin Prionotus scitulus (Pisces: Triglidae). Fish. Bull., 76: 225-234. Scaccini, A., 1947. Contributo alia conoscenza della biologia dei Mullidi nell Adriatico medio Occidentale. Note Lab. Biol. Mar. Fano, 1: 1-8. Schaefer, R.H., 1960. Growth and feeding habits of the whiting or silver hake in the New York Bight. N.Y. Fish Game J., 7: 85-98. Schoener, T.W., 1970. Non synchronous spatial overlap of lizards in patchy habitats. Ecology, 51: 408-418. Singer, M., 1985. Food habits of juvenile rockfishes (Sebastes) in a central California kelp forest. Fish. Bull., 83(4): 531-541.
FEEDING HABITS OF RED MULLET IN WESTERN GREECE
83
UNESCO Report, 1977. Marine ecosystem modelling in the Mediterranean. Report of the second workshop on marine ecosystem modelling, UNESCO Publications, Dubrovnic, 111 pp. Vassilopoulou, V., 1987. Sexual maturity of red mullet (Mullus barbatus) in the gulfs of Korinthiakos and Patraikos and in the Ionian Sea. Proc. 2nd Hell. Symp. Oceanogr. Fish., 14-17 May 1990, National Centre for Marine Research, Athens, pp. 565-570 (in Greek). Vassilopoulou, V. and Papaconstantinou, C., 1988. Distribution with depth and catches per unit effort of the hake and the red mullet in the western coasts of Greece. FAO Fish. Res., 394: 174-180. Vassilopoulou, V., 1989. Biological aspects of red mullet, Mullus barbatus, off the coasts of central Greece. Proc. Int. Semin. Combat Poll. Conserv. Mar. Wealth Mediter. Sea, 5-8 June 1989, General People's Committee for Marine Wealth (in press). Wirszubski, A., 1953. On the biology and biotope of red mullet Mullus barbatus. Bull. Sea Fish. Research Stn. Haifa, 7: 1-20.
69
Elsevier Science Publishers B.V., Amsterdam
Feeding habits of red mullet (Mullus a gulf in western Greece
barbatus) in
V. Vassilopoulou and C. Papaconstantinou National Centre for Marine Research, Agios Kosmas Hellinikon, Athens 166 04, Greece (Accepted 29 June 1992)
ABSTRACT Vassilopoulou, V. and Papaconstantinou, C., 1993. Feeding habits of red mullet (Mullus barbatus) in a gulf in western Greece. Fish, Res., 16: 69-83. The stomach contents of red mullet collected in the Amvrakikos Gulf of Greece during five samplings between November 1986 and February 1987 were analysed. Fullness indices fluctuated in relation to month and area of capture. Significantly greater quantities of food were found in the stomachs of specimens in the western part of the Gulf in September. Polychaetes were the primary food item in three of the five samplings. Bivalves, the second most important prey, showed great seasonal fluctuations. Crustaceans were third, while gastropods, echinoids and sipunculids, although occurring frequently in the stomachs, were of minor importance. There were differences in quantity and, to a lesser degree, quality between the diet of male and female red mullet, possibly related to sexual differences in growth rate. Cluster analysis revealed that the prey species composition in the stomachs of red mullet was influenced by area of capture rather than fish length. Possible relations of food availability to the migration pattern of the species are also discussed.
INTRODUCTION
Estuaries and enclosed bays frequently form essential feeding and/or breeding grounds for commercially important fish (UNESCO, 1977). Red mullet from the Amvrakikos Gulf provide a considerable income for fishermen in the area. However, there is an emigration from the Gulf of individuals having completed their second year of life (fork length, >150 mm), thus limiting the local fishery. Among the factors influencing fish migrations are feeding habits and/or starvation (Harden-Jones, 1968; Nikolsky, 1976). Information on the feeding habits of juvenile red mullet along the Mediterranean coast is limited (Froglia, 1988), but adult specimens have been studied by several authors (Planas and Vives, 1956; Haidar, 1970; Jukic, 1972; Caragitsou and Tsimenidis, 1982; Papaconstantinou and Caragitsou, 1987 ). Correspondence to: V. Vassilopoulou, National Centre for Marine Research, Agios Kosmas Hellinikon, Athens 166 04, Greece.
© 1993 Elsevier Science Publishers B.V. All rights reserved 0165-7836/93/$06.00
70
V. VASSILOPOULOUAND C. PAPACONSTANTINOU
The objectives of this study were to describe the feeding habits of red mullet in the Amvrakikos Gulf, evaluating possible effects of season, area of capture and fish size on stomach contents. MATERIALS AND METHODS
Amvrakikos Gulf is a semi-enclosed bay in western Greece, with a maximum depth of approximately 60 m (Fig. 1 ). It connects with the Ionian Sea by a 600 m wide channel at its northern end and the Louros and Arachthos rivers discharge into its northern part. The stomachs of 403 red mullets, landed by trammel bottom nets in the Amvrakikos Gulf, were examined (Fig. 1 and Table 1 ). Five samplings took place at 22 sites with depths ranging from 3 to 18 m from November 1986 to September 1987. The abdominal cavity of each fish was opened and the whole fish was immediately immersed and preserved in a 6% buffered formaldehyde solution. In the laboratory, samples were segregated by month, area of capture (western-outer and eastern-inner parts), sex and size of fish (three length groups were formed according to fork lengths of fish; 100-120 mm, 120-140 mm and 140-160 m m ) . For each specimen, length to the nearest millimetre, weight .
z
° I
~:..:
I
I
.'i'. . .-.'~
..
o
•
."
'!..-.....
W ""1~
®
: : "•:' ~ ,• ' '~°~ • : • :
®
20.45
ii : ....
20.50 I
j
::
"
20.55 I
LONGITUDE
I
;..'~(:..~
•
"::
I
I
I
":A..'::..
,, ..'.'.:.""
:'.:, ~i~" ®
®~)'l,'~'.:;i" :®~~i ':;i:;'i"~i~'."!:'}'|':;'.....
"".-i:e
2!.00 I
i:.i..
21.05 I
2"1.10 I
(°E)
Fig. I. Location of sampling stations for red mullet in the Amvrakikos Gulf. ( • western-outer, ® eastern-inner parts).
FEEDING HABITSOF RED MULLET IN WESTERN GREECE
71
TABLE1
Total numbers of individual red mullet examined, number of empty stomachs, mean degree (L) and mean index (B) of stomach fullness with 95% confidence intervals (a) from November 1986 to September 1987, (b) for each length group and (c) for the eastern and western part of the Amvrakikos Gulf November
February
May
July
September
63 0 1.87-+0.22 0.59_+0.11
93 0 2.48_+0.19 1.15+0.08
(a) No. of stomachs No. of empty stomachs Degree of fullness (L) Index of fullness (B)
92 0 2.39-+0.23 0.91_+0.08
84 0 2.15+0.19 0.85+0.09
71 5 1.38+0.18 0.42_+0.15
(b) No. of stomachs No. of empty stomachs Degree of fullness (L) Index of fullness (B)
10-12 cm 79 0 2.44_+0.21 1.07_+0.12
12-14 cm 285 2 2.24+0.12 0.76+0.06
14-16 cm 39 3 2.05-+0.39 0.69-+0.13
(c) No. of stomachs No. of empty stomachs Degree of fullness (L) Index of fullness (B)
Western 270 1 2.17_+0.13 0.90_+0.07
Eastern 128 4 2.02+0.17 0.65_+0.07
to the nearest gram and sex were recorded. Gonadal maturity was determined according to Nikolsky's scale (1976) (Stages I, II, III immature gonads; IV, V mature; VI spent). The degree of fullness (L) was estimated for individual stomachs according to Lebedev's scale (1946), ranging from 0 (empty) to 5 (stomach fully distended with food). Measures of food intake were determined by calculating an index of fullness (B: wet weight of stomach contents as a percentage of total body weight of each predator; Hyslop, 1980). Index values were loglo transformed and subjected to multiple analysis of variance (MANOVA) to evaluate the orders of importance of the key factors (season, area of capture and size of fish) determining variability in the stomach contents. Prey items were identified to the most precise taxonomic level possible and counted and weighed to the nearest 0.01 g. Frequency of occurrence as a percentage (F), number (Cn) and weight (Cw) of each prey item were calculated. Complementary clustering (group average strategy) using the Bray-Curtis similarity coefficient (Bray and Curtis, 1957) was performed on the Cw of each prey item in each season and in each length group in the two areas of the Amvrakikos Gulf, using the PRIMER algorithms (Clarke and Warwick, 1989). Diet similarity was determined using Schoener's index (1970) S= 1-0.5
(,SIPxi-PyiI)
V. VASSILOPOULOUANDC. PAPACONSTANTINOU
72
where Px~ and Px were the proportions by weight (Cw) of prey i in seasons or areas or length groups x and y, respectively. The index values were compared with Langton's convention (1982), in which values of 0.00-0.29, 0.30-0.60 and greater than 0.60 reveal low, medium and high similarity, respectively. RESULTS
Feeding intensity The length frequency distributions of male and female red mullet are presented in Fig. 2. Among the 403 specimens examined, none exhibited signs of starvation (small and reddish liver because of fat loss, darker colour of the gall, gall bladder increased in volume). Five red mullet, all from the May sampling, had empty stomachs. The degree (L) and the index (B) of stomach fullness in each month, area of capture and length group are presented in Table 1. Multiple analysis of variance applied to the data revealed that both month and area of capture had a significant effect on L and B (MANOVA: FL=7.356, FB=7.031, P<0.001 ). The application of the five month data of analysis of variance (ANOVA: FL= 18.32, P<0.001; FB=23.351, P<0.01 ) and multiple range tests showed that both L and B were significantly lower in May and July. Geographically, red mullet from the western part of the Gulf exhibited significantly higher L and B values, as compared with those from the eastern part. On the other hand, the fish length had an insignificant influence on fullness indices in relation to month (MANOVA: FL = 0.695, P = 0.6963; Fu= 1.393, P=0.1977) and area of capture (MANOVA: FL=0.162, P=0.8508; Fs= 0.411, P=0.663). Mal~s~
(%)
F~mal~sI
30-
Nm :159 NF :244
252015-
._L
1o. 5o 9
F L
(crn]
Fig. 2. Length frequency distributions of male and female red mullet caught in the Amvrakikos Gulf, November 1986-September 1987.
FEEDING HABITS OF RED MULLET IN WESTERN GREECE
73
General feeding trends Red mullets feed by the 'slurp' method; they swim over muddy bottoms, sucking up and sifting through large quantities of mud. Mud and small stones were found in the stomachs of many of the specimens. Overall, in terms of percentage by weight, the stomach contents consisted mostly of polychaetes (51.9%), bivalves (30.2%), crustaceans ( 8.92% ) and sipunculids (3.6%) (Table 2 ). Among the identified polychaetes, Pectinaria koreni, Sternaspis scutata, Sabella pavonina, Lumbriconereis impatiens and Sthenelais boa made up the 19.2% of the estimated weight of the stomach contents. Tellina spp. and Loripes spp. were dominated by weight among the identified bivalves. Crustaceans were represented mainly by amphipods (almost exclusively Ampelisca diadema, 0.71%), decapods (0.09% each of Callianassa tyrrheni and Processa canaliculata ) and mysids (mostly Leptomysis mediterranea, 0.18%). The sipunculid Aspidosiphon muelleri accounted for the 3.6% of the weight of the stomach contents. The Foraminifera sp. Elphidium crispum was quite numerous but did not contribute much to the weight.
Monthly variations in stomach contents Polychaetes predominated in terms of percentage number (Cn), weight
(Cw) and frequency of occurrence (F) in February, May and July. Bivalves dominated the stomach contents in September but were not present in May; they were, however, the second most important prey during the other months investigated (Table 3 ). In November, both polychaetes and bivalves were of similar importance. Crustaceans, the third major taxon, increased in importance in May. Relatively small seasonal fluctuations existed within the rest of the prey taxa. Cluster analysis at the 60% similarity level indicated three major groupings of months (Fig. 3 ). The major group (Group I) comprised July, September and November, while February (Group II) and May (Group III) formed separate groups. The major difference separating Groups I and II was due to sedentary polychaetes, particularly Sternaspis scutata, which was quite important in terms of weight (27.2%) in February, but was non-existent in stomachs during the rest of the year. Groups I and III were mainly separated on the basis of bivalves that displayed the greater differences of presence in the stomach contents, as compared with other prey taxa. The separation of Groups II and III was primarily due to the high percentage by weight (74%) of sedentary polychaetes (Sternaspidae, Amphictenidae and Sabellidae) in February, while in May the stomach contents mainly consisted (67%) of errant polychaetes (Eunicidae and Glyceridae) and crustaceans (Amphipoda and Decapoda).
74
v. VASSILOPOULOUANDC. PAPACONSTANTINOU
TABLE2 Per cent by weight (Cw) of items in the stomachs of red mullet in the Amvrakikos Gulf, November 1986 to September 1987 Prey Mycophyta Lyngbya spp. Rhizopoda Foraminifera Elphidium crispum Cnidaria Anthozoa Annelida Polychaeta unidentified Aphroditidae unidentified Leanira spp. Sthenelais boa Eunicidae unidentified Eunice vittata E. rousseaui Hyafinoecia bifineata H. brementi Lumbriconereis impatiens L. gracilis Glyceridae unidentified Glycera con voluta Goniada spp. G. maculata Nereidae unidentified Micronereis variegata Nereis caudata Nepthydidae Nepthys spp. Syllidae unidentified Exogonia spp. Syllis variegata S. cornuta Ampharetidae unidentified Amphictenidae Pectinaria koreni Capitellidae Notomastus latericeus Maldanidae unidentified Maldane sarsi Sabellaridae unidentified Pallacia spp. P. cirrata Sabeilidae unidentified Sabella pavonina Spionidae Laonice cirrata Sternaspidae Sternaspis scutata Terebellidae unidentified Amphitrite spp. Terebellides stroemi
Cw 0.02
0.93 0.02 18.92 2.00 0.11 0.55 2.37 0.07 0.07 0.04 0.02 0.71 0.47 2.73 O.13 0.04 0.02 0.67 0.04 0.07 0.02 1.26 0.04 0.16 0.04 0.04 9.94 0.22 O.13 0.04 0.24 0.47 O.18 1.82 2.21 0.04 5.73 0.20 0.02 0.03
Prey
Trichobranchus glacialis Sipunculida Aspidosiphon mulleri Arthropoda Crustacea unidentified Copepoda unidentified Ostracoda unidentified Amphipoda unidentified Gammaridae unidentified .4mpelisca diadema Hyale schmidti Caprellidae unidentified Phtisica marina Anisopoda unidentified Apseudes latreilli Cumacea unidentified Pseudocuma longicorniz Euphausiacea unidentified Euphausia krohni Isopoda unidentified Eurydice truncata Mysidacea unidentified Paramysis helleri Leptomysis mediterranea Siriella clausi Anchialina agilis Decapoda unidentified Brachyura unidentified Callianassa tyrrhena Processa canaliculata MoUusca Bivalvia unidentified Nuculana fragilis N. pella Loripes spp. Tellina spp. Thracia spp. Gastropoda unidentified Turitella communis Philine spp. Scaphopoda Dentalium spp. Echinodermata Echinoidea unidentified Echinocyamus pusillus Asteroidea Astropecten spp. Ophiuroidea unidentified Ophioderma longicauda Vertebrata Osteichthyes
Cw 0.04 3.63 3.03 0.08 0.09 0.26 0.22 O.71 0.02 0.11 0.09 0.09 O.11 0.09 0.02 0.04 0.02 0.33 0.07 0.60 0.01 O.18 0.02 O.11 2.35 0.09 0.09 0.09 28.12 O.11 0.04 0.20 1.62 0.11 1.97 0.04 0.01 0.02 0.80 0.93 0.11 0.01 0.02 0.40
F E E D I N G H A B I T S O F R E D M U L L E T IN W E S T E R N G R E E C E
TABLE
75
3
Seasonal variation of the Cw ( % by weight) of prey in stomach contents of the red mullet in the A m v r a k i k o s Gulf, November 1986 to September 1 9 8 7 Prey
November Cn Cw
Oscillatoriaceae Foraminifera Anthozoa Polychaeta
February Cn Cw
*
*
7.9
*
*
*
*
.
May Cn
July Cn
Cw
September Cn Cw
Cw
-
-
-
*
*
*
*
*
5.3
*
37.0
4.5
9.9
*
.
.
.
.
.
.
18.1
23.6
12.1
9.0
18.8
23.4
12.7
24.6
11.8
19.6
Errantia
7.6
7.4
15.2
7.4
27.0
31.5
6.3
8.2
17.3
15.8
Sedentaria
9.7
7.5
53.8
63.2
12.7
18.7
2.3
8.1
3.4
2.4
Sipunculida
3.5
4.9
.
*
1.2
6.0
6.6
Crustacea
7.8
3.1
-
7.6
7.2
4.1
1.7
Copepoda
*
*
.
.
.
.
*
*
-
-
Ostracoda
*
*
.
.
.
.
*
*
*
*
Amphipoda
2.6
*
4.8
1.2
7.1
3.7
5.4
3.9
1.2
*
Anisopoda
*
*
-
-
2.5
2.0
1.0
*
*
*
Cumacea
*
*
-
-
*
*
*
*
-
-
Euphausiacea
.
. -
. 21.3
15.6
-
-
-
*
*
-
-
*
*
Isopoda
1.0
*
-
*
*
*
-
-
*
Mysidacea
3.3
1.0
3.6
1.0
2. 1
1.2
2.6
2.1
*
*
Decapoda
*
3.3
4.4
3.4
2.1
2.4
2.9
5.5
*
*
21.9
38.8
4.0
5.8
-
-
10.2
27.1
31.5
47.0
Gastropoda
6.0
1.6
1.2
-
-
7.8
3.0
12.2
3.7
Scaphopoda
*
*
.
.
.
.
*
1.0
-
-
Echinoidea
7.5
5.5
.
.
.
.
1.2
1.4
*
*
Asteroidea
*
*
.
.
.
Ophiuroidea
.
*
*
Osteichthyes
*
-
-
Bivalvia
*Prey category
.
. *
present, but less than
*
. .
* 1.0%
. .
8.7
of the total
.
. .
-
-
*
1.0
v~6ight.
Differences in stomach contents between males and females The stomach contents of males and females mainly differed in quantity and only to a lesser degree in species of the ingested food. Within the same length group the mean stomach content weights of the two sexes (Fig. 4) were significantly different at the 95% significance level; stomachs of females contained more food than those of males (tll-12 cm=2.008, t12-13 cm=2.313, tl 3-14c m "~- 2.077, t14-15 cm = 2.692 ). The t test was not applied on data derived from specimens smaller than 11 cm and larger than 15 cm because of their small numbers. Small qualitative differences appeared between the two sexes. Although polychaetes dominated in all stomachs they were relatively reduced in males, which also seemed to prefer crustaceans and molluscs (Table 4 (a)).
76
V. VASSILOPOULOUANDC. PAPACONSTANTINOU
0" 10" 2030~ 40~
>-
50~
F-
E< .J
60 ~ 70~
80-
90-
100 \5
J
/
M
F
ml
Group ]
Group liT Group
Fig. 3. Dendrogram showing groupings of months, using Bray-Curtis index, based on prey (Cw) in the stomach of red mullet in the Amvrakikos Gulf. (N, November; F, February; M, May; J, July; S, September. )
Variations in stomach contents relative to fish length There were small qualitative differences in the stomach contents of the three length groups; an increase in the proportion by weight of molluscs and crustaceans and a decrease of polychaetes existed within specimens of lengths 1014 cm compared with larger ones (Table 4(b) ). Cluster analysis was performed on the stomach contents of the three length groups at the two areas (Fig. 5 ). High qualitative similarity of the stomach contents in relation to fish length was found in the western part of the Gulf (Group I ). On the other hand, in the eastern Amvrakikos the few larger specimens ( N = 7 ) belonging to the 14-16 cm length group (Group III ) were separated from the smaller ones (Group II), mainly due to the high proportion by weight of Sternaspis scutata in the stomachs of the larger fish.
FEEDING HABITS OF RED MULLET 1N WESTERN GREECE
"--
"-- Moles
H
77
Fernoles
0.5 0.4 ~o 0.3,.J -C u t3
E
0.2-
0.1
0
0
c0
!
9
I'0
3:
!
11
Fish
12 length
13
I'4
15
(cm)
Fig. 4. Mean weight of stomach contents versus fish length (with 95% confidence intervals) of male and female red mullet from the Amvrakikos Gulf. TABLE 4 Per cent by weight (Cw) of the major prey taxa ingested by red mullet (a) males and females, (b) fish of various lengths and (c) fish collected in the western and eastern Amvrakikos Gulf Prey
For.
Mol.
Pol.
Cru.
Sip.
Ech.
Others
0.77 0.99
35.35 30.15
45.62 61.39
12.28 3.39
2.67 2.75
2.49 1.62
0.84 0.72
0.77 0.96 1.11
40.98 38.76 31.84
42.79 44.56 59.66
8.51 7.04 5.26
3.97 4.06 !.07
1.60 1.98 0.71
1.36 2.68 0.36
1.20 0.2 i
33.79 29.57
48.62 53.96
8.06 11.50
4.13 3.09
1.58 0.88
2.63 0.88
(a) Sex Male Female
(b) Length (cm) 10-12 12-14
14-16
(c) Area Western Eastern
For., Foraminifera; Mol., Mollusca; Pol., Polychaeta; Cru., Crustacea; Sip., Sipunculida; Ech., Echinoidea.
Geographical variations in stomach contents The proportion by weight of the major prey categories in the two parts of the gulf are presented in Table 4(c). In all, 24 prey taxa were identified in the western part and 21 in the eastern. Polychaetes were dominant in both parts of the Amvrakikos, mainly Amphictenidae species in the western part, but with Sternaspidae also in the eastern part. Molluscs, represented almost ex-
78
V. VASSILOPOULOU AND C. PAPACONSTANTINOU OI020-
o~ 30>m 40r~ < .3
5060-
~r
70-
I
tn
80" 90100 EL
\EM
Group 111
E$/ v G r o u p ]I
\WL
WM "v Group
W$/ I
Fig. 5. Dendrogram showing groupings of fish length and area of capture, using Bray-Curtis index, based on prey (Cw) in the stomach of red mullet in the Amvrakikos Gulf. (EL, eastern Amvrakikos, large specimens; EM, eastern, medium; ES, eastern, small; WL, western, large; WM, western, medium; WS, western, small. )
clusively by bivalves, were of equal importance in both parts. Small differences also existed within crustaceans, sipunculids and echinoids. Cluster analysis revealed that at the 73% similarity level, fish from the western part of the Gulf (Group I) were separated from those of the other parts (Fig. 5).
Dietary overlap Dietary overlap, calculated on the basis of percentage by weight (Cw), of prey found in fish stomachs indicated changes in the prey spectrum in relation to season. There was a considerable similarity in November, July and September (Table 5(a) ), the months that form Group I in Fig. 3. The decrease of the species' niche breadth in February and May decreased Schoener's index. In relation to fish length, the overlap index presented high values (Table 5 (b) ), probably due to the small range of fish lengths involved. There was also a high similarity ( S = 0.76) between the mullet collected in the two different parts of the Gulf.
FEEDING HABITS OF RED MULLET IN WESTERN GREECE
79
TABLE 5 Schoener's indices o f dietary overlap between red mullet o f ( a ) different m o n t h s and ( b ) different length groups in the Amvrakikos G u l f f r o m 1986 to 1987 (a)
November
February
May
July
February May July September
0.37 0.63 0.84 0.77
0.43 0.34 0.23
0.49 0.57
0.77
(b)
10-12 cm
12-14 cm
12-14 cm 14-16cm
0.76 0.57
0.65
DISCUSSION
Red mullet in the Amvrakikos Gulf is benthophagous, feeding on infaunal and epifaunal invertebrates, primarily polychaetes, bivalves and crustaceans. Sipunculids, gastropods and echinoids, although eaten regularly, were of minor importance. Daniels ( 1982 ) reported that fish using the 'slurp' method of foraging, usually take sedentary polychaetes and slow-moving invertebrates. Red mullet in Israeli waters fed mainly on polychaetes, molluscs, echinoderms and to a lesser degree fish (Wirszubski, 1953 ). In Spanish waters (Planas and Vives, 1956 ) and in the Adriatic Sea (Haidar, 1970), stomachs of red mullet included primarily decapods, followed by polychaetes and bivalves. The major prey items ingested by red mullet in the Aegean Sea (Caragitsou and Tsimenidis, 1982), as well as in the western Greek Seas (Papaconstantinou and Caragitsou, 1987 ) were amphipods, decapods, mysids and polychaetes. The pattern of activity in the Amvrakikos Gulf throughout the year is intensive feeding in the winter, curtailment of feeding in spring and summer and resumption of feeding in the autumn, but to a higher degree than in the winter. Among polychaetes, Pectinaria koreni dominated in terms of number, weight and frequency of occurrence, except in February, when the higher Cw value was found to coincide with Sternaspis scutata. On the other hand, bivalves, predominating in the stomach contents in September, were not observed in the stomachs in May. Seasonal changes in feeding habits were also found in red mullet from other parts of the Mediterranean (Haidar, 1970; Caragitsou and Tsimenidis, 1982 ). A number of authors have shown that, as the density of a particular prey type declines, a predator may switch to feeding on another prey which is more abundant (Murdoch, 1969; Cornell, 1976;
80
V. VASSILOPOULOU AND C. PAPACONSTANTINOU
Hume and Northcote, 1985; Davidson, 1986 ). Analysis of the benthos in the Amvrakikos Gulf, however, did not reveal corresponding variations in the benthic abundance of the various items found in the stomachs of red mullet (Bogdanos et al., 1989). Quantitative differences mainly existed in the diet of red mullet between the two parts of the Amvrakikos Gulf; larger quantities of food were found in the stomachs of specimens collected in the western Amvrakikos. Qualitatively, in the latter area there were three taxa more in the total stomach contents, as compared with the eastern part. A difference in the diversity and abundance of benthic species was also established between the two parts of the Gulf; higher diversities and abundances coincided with the western part (Bogdanos et al., 1989). The diversity of the benthos in the Amvrakikos may be influenced by the type of bottom sediment (Ignatiades et al., 1981 ), which differs between the eastern and the western parts (Piper et al., 1982) and may account for the dietary differences in red mullet. According to Piper et al. (1982) the sediments accumulating beneath 38%0 salinity water in the Gulf have a foraminiferal fauna. This observation seems to explain the relatively high values of percentage number and frequency of occurrence of Foraminifera in the stomachs. Stomachs of females contained larger quantities of food than those of males of similar size. A similar observation was made for red mullet in the Adriatic Sea (Haidar, 1970). Since growth of fish is directly related to food intake, it is not surprising that females grow faster than males (Scaccini, 1947; Papaconstantinou et al., 1981; Vassilopoulou, 1989). Larger quantities of food in the stomachs of females and faster growth was also reported for the silver hake (Merluccius bilinearis) in the northwestern Atlantic (Schaefer, 1960; Bowman, 1984). Many fish species change diet as they grow (Ross, 1978; MacPherson, 1981 ). This may result from changes in habitat and hence changes in available food sources, or it may simply be a functional response to changes in fish size and/or metabolic needs (Singer, 1985 ). In the Amvrakikos Gulf, small dietary differences appeared between length groups. This was expected, since the red mullet collected, covered a rather small range of body length (FL, 6 cm). Bivalves and crustaceans were more abundant than polychaetes in smaller red mullets. The only exception coincided with the few large specimens collected in the eastern Amvrakikos, which seemed to prefer the polychaete Sternaspis scutata. However, further studies are required to elucidate specific problems associated with prey selection in different size groups, since body length of red mullet collected in the Greek Seas usually covers an interval of 6-23 cm FL. Finally, there were no signs of starvation throughout the year in red mullet collected in the Amvrakikos Gulf, except for a small percentage of individuals
FEEDINGHABITSOF RED MULLETIN WESTERNGREECE
81
with empty stomachs in May. Hence starvation is not the reason for the migration of larger red mullets ( > 15 cm) out of the Gulf. However, the small depth of the Amvrakikos ( m a x i m u m < 60 m) and the decreased values of dissolved oxygen in the deeper waters (Friligos and Koussouris, 1977 ) create hypoxic conditions seriously affecting the benthic fauna (Bogdanos et al., 1989; Papaconstantinou and Caragitsou, 1990 ). These conditions suggest the existence of a depth limit for the distribution of red mullet in the Amvrakikos Gulf, since the species usually extends to a depth of approximately 200 m in the Greek Seas (Papaconstantinou et al., 1988 ) with an obvious trend of larger specimens to exist in deeper waters (Vassilopoulou and Papaconstantinou, 1988 ). Moreover, the shift of the species towards the Ionian Sea takes place during the second year of its life, coinciding with its first sexual maturity (Vassilopoulou, 1987). The few mature specimens collected in the framework of the present study, as well as the eggs and larvae of the species (Caragitsou et al., 1989 ) were found at sites close to the Ionian Sea channel. Hence, the Amvrakikos Gulf seems to offer a favourable habitat to relatively small ( < 16 cm) and sexually immature red mullet.
REFERENCES Bogdanos, C., Panagiotidis, P., Simboura, N. and Mastori, V., 1989. Study of the Benthos of the Amvrakikos Gulfi In: Final Report on the Oceanographic Study of the Amvrakikos Gulf 4. Biological Oceanography. National Centre for Marine Research Editions, Athens, pp. 38-47 (in Greek). Bowman, R.E., 1984. Food of silver hake, Merluccius bilinearis. Fish. Bull., 82 ( 1 ): 21-35. Bray, J.R. and Curtis, J.T., 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr., 27: 325-349. Caragitsou, E. and Tsimenidis, N., 1982. Seasonal changes of food spectrum and daytime rhythm of feeding of the red mullet (Mullus barbatus) in the Thracian Sea. Thalassographica, 5 ( 2 ): 105-115. Caragitsou, E., Vassiiopoulou, V., Petrakis, G., Papaconstantinou, C. and Fourtouni, A., 1989. The Fishery of the Amyrakikos Gulf. In: Final Report on the Oceanographic Study of the Amvrakikos Gulf. 5~, Fisheries. National Centre for Marine Research Editions, Athens, pp. 1-72 (in Greek). Clarke, K.R. and Warwick, R.M., 1989. Lecture notes prepared for the training workshop on the statistical treatment and interpretation of marine community data. FAO/IOC/UNEP, Athens, September 1989, Part II, 84 pp. Cornell, H., 1976. Search strategies and the adaptive significance of switching in some general predators. Am. Nat., 110: 317-320. Daniels, R.A., 1982. Feeding ecology of some fishes of the Antarctic peninsula. Fish. Bull., 80 ( 3 ): 575-588. Davidson, R.J., 1986. Mussel selection by the paddle crab Ovalipes catharus: evidence of a flexible foraging behaviour. J. Exp. Mar. Biol. Ecol., 102: 281-299. Friligos, N. and Koussouris, T., 1977. Preliminary chemical, physical and biological observations in the gulf of Amvrakikos (April 1974). Thalassia Jugos., 13 ( 1/2 ): 53- 58. Froglia, C., 1988. Food preferences of juvenile Red Mullet Mullus barbatus in western Adriatic
82
v. VASSILOPOULOUANDC. PAPACONSTANTINOU
nursery ground (Osteichthyes: Mullidae). Rapp. P.-V. Rfun. Inter. Comm. Sc. Expl. Medit., 3(2): 263. Haidar, Z., 1970. L'oecologie du rouget (Mullet barbatus) en Adriatique orientale. Acta Adfiat., 14 ( 1 ): 1-94. Harden-Jones, F., 1968. Fish Migration. Edward Arnold, London, 325 pp. Hume, J.M.B. and Northcote, T.G., 1985. Initial changes in use of space and food by experimentally segregated populations of Doily varden (Salvelinus malma) and cutthroat trout (Salmo clarki). Can. J. Fish. Aquat. Sci., 42: 101-109. Hyslop, E.J., 1980. Stomach content analysis - - a review of methods and their application. J. Fish Biol., 17:411-429. Ignatiades, L., Moraitou-Apostolopoulou, M. and Nikolaidou, A., 1981. Biotic Conditions. In: J. Szijj (Editor), Ecological Assessment of the Delta Area of the rivers Louros and Arachthos at the Gulf of Amvrakia. Univ. Essen Publications, Essen, pp. 31-49. Jukic, S., 1972. Nutrition of the hake (Merluccius merluccius), bogue (Boops boops), striped mullet (Mullus barbatus) and pandora (Pagellus erythrinus) in the bay of Kastela. Acta Adriat., 14 (4): 3-40. Langton, R.W., 1982. Diet overlap between Atlantic cod, Gadus rnorhua, silver hake, Merluccius bilinearis, and fifteen other northwest Atlantic finfish. Fish. Bull., 80: 745-759. Lebedev, N.V., 1946. Elementary populations offish. Zool. Zhur., 25(2): 121-135 (in Russian). MacPherson, E., 1981. Resource partitioning in a Mediterranean demersal fish community. Mar. Ecol. Prog. Ser., 4: 183-193. Murdoch, W.W., 1969. Switching in general predators: experiments on predator specificity and stability of prey predations. Ecol. Monogr., 39: 335-354. Nikolsky, G.V., 1976. The Ecology ofFish. 6th edn. Academic Press, New York, 352 pp. Papaconstantinou, C., Tsimenidis, N. and Daoulas, C., 1981. Age and reproduction of red mullet (Mullus barbatus L., 1758 ) in the gulfs of Saronikos and Thermaikos. Thalassographica, 4( l ): 39-66. Papaconstantinou, C. and Caragitsou, E., 1987. Preliminary study on the trophic relationship of red mullet (Mullus barbatus) off the western coast of Greece. Proc. 2nd Hell. Congr. Oceanogr. Fish., 14-17 May 1990, National Centre for Marine Research, Athens, pp. 577583 (in Greek). Papaconstantinou, C., Caragitsou, E., Mytilineou, C., Petrakis, G. and Vassilopoulou, V., 1988. Dynamics of demersal fish stocks in the Korinthiakos and Patraikos Gulfs and in the Ionian Sea. Part II. Thalassographica Sp. Publ. No. 16., National Centre for Marine Research, Athens, 277 p. (in Greek). Papaconstantinou, C. and Caragitsou, E., 1990. Abiotic parameters affected on the abundance offish population in the Amvrakikos Gulf. Proc. 2nd Hellemic Cypriotic Congr. Chem. Environ., 28 September-2 October 1990. Greek and Cypriotic Union of Chemists, Athens, pp. 416-420 (in Greek). Piper, D.J.W., Panagos, A.G. and Kontopoulos, N., 1982. Some observations on surficial sediments and physical oceanography of the gulf of Amvrakia. Thalassographica, 5 (2): 63-80. Planas, A. and Vives, F., 1956. Notas preliminares sobre la biologia del salmonete (Mullus barbatus). Invest. Pesq., 5:31-50. Ross, S.T., 1978. Trophic ontogeny of the leopard searobin Prionotus scitulus (Pisces: Triglidae). Fish. Bull., 76: 225-234. Scaccini, A., 1947. Contributo alia conoscenza della biologia dei Mullidi nell Adriatico medio Occidentale. Note Lab. Biol. Mar. Fano, 1: 1-8. Schaefer, R.H., 1960. Growth and feeding habits of the whiting or silver hake in the New York Bight. N.Y. Fish Game J., 7: 85-98. Schoener, T.W., 1970. Non synchronous spatial overlap of lizards in patchy habitats. Ecology, 51: 408-418. Singer, M., 1985. Food habits of juvenile rockfishes (Sebastes) in a central California kelp forest. Fish. Bull., 83(4): 531-541.
FEEDING HABITS OF RED MULLET IN WESTERN GREECE
83
UNESCO Report, 1977. Marine ecosystem modelling in the Mediterranean. Report of the second workshop on marine ecosystem modelling, UNESCO Publications, Dubrovnic, 111 pp. Vassilopoulou, V., 1987. Sexual maturity of red mullet (Mullus barbatus) in the gulfs of Korinthiakos and Patraikos and in the Ionian Sea. Proc. 2nd Hell. Symp. Oceanogr. Fish., 14-17 May 1990, National Centre for Marine Research, Athens, pp. 565-570 (in Greek). Vassilopoulou, V. and Papaconstantinou, C., 1988. Distribution with depth and catches per unit effort of the hake and the red mullet in the western coasts of Greece. FAO Fish. Res., 394: 174-180. Vassilopoulou, V., 1989. Biological aspects of red mullet, Mullus barbatus, off the coasts of central Greece. Proc. Int. Semin. Combat Poll. Conserv. Mar. Wealth Mediter. Sea, 5-8 June 1989, General People's Committee for Marine Wealth (in press). Wirszubski, A., 1953. On the biology and biotope of red mullet Mullus barbatus. Bull. Sea Fish. Research Stn. Haifa, 7: 1-20.