Diets of thornback ray (Raja clavata) and tope shark (Galeorhinus galeus) in the bottom longline fishery of the Azores, northeastern Atlantic.
The thornback ray (Raja clavata L.), is a shallow water bottom-living elasmobranch found in the Atlantic from Iceland and Norway southwards to South Africa, including Madeira and Azores islands. This species is also found in the Mediterranean, western Black Sea, and southwestern Indian Ocean (Stehmann and Burkel, 1984). The thornback ray is commercially exploited in several countries. In the Azores it is a bycatch of the bottom longline fishery directed toward demersal and deepwater teleost species. Food and feeding habits of the thornback ray have been intensively studied since the end of the 19th century (e.g. Day, 1880-84) and more recently (e.g. Smale and Cowley, 1992; Ellis et al., 1996; Daan et al (1)). However, only two studies have been conducted on the thornback ray off Portuguese continental waters (Marques and Re, 1978; Cunha et al., 1986), and none exists for populations inhabiting waters around the oceanic islands or seamounts in the northeastern Atlantic.
The tope shark (Galeorhinus galeus (L.)), is a cosmopolitan species that can be found from about 70[degrees]N to about 55[degrees]S. Distribution of this species in eludes the Atlantic, Pacific and Indian Oceans (Compagno, 1984). Tope shark is also commercially exploited by several countries around the world, including the Azores, where it is a bycatch of the bottom longline fishery. Compagno (1984) and Olsen (1984) reviewed the biology of this shark; however, there have been relatively few studies on their feeding habits. The diet of tope shark was described by Ford (1921) for individuals landed at Plymouth U.K., by Olsen (1954) in southeastern Australia, and by Ellis et al. (1996) in the northeastern Atlantic Ocean.
Elasmobranchs are among the top predators in marine environments (Ellis et al., 1996); thus they affect the populations of both fish and invertebrates at lower trophic levels. However, feeding studies of elasmobranches in the Azores have been limited to the blue shark (Prionace glauca) (Clarke et al., 1996). Tope shark and thornback ray are the two most abundant elasmobranch species landed by the Azorean bottom longline fishery. Information on the feeding habits of these two species contributes to a better understanding of trophic dynamics and food webs--information which is needed as fisheries scientists advance ecosystem principles to fisheries management (Pauly et al., 2000; Pitcher, 2000; Whipple et al., 2000). The purpose of this study was to examine the diet of thornback ray and tope shark, to describe their feeding patterns and the effect of sex, size, depth, and location on their diet.
Materials and methods
Thornback rays and tope sharks were collected between March and May (spring) of 1996 and 1997 during a study on demersal fisheries in Azorean waters (Fig. 1). Fishes were caught by longline onboard the RV Arquipelago. Line setting began before sunrise (approx. 05:00 h) and hauling started about two hours after setting. From the fish sampled, total length (TL, to the nearest cm) was measured, and sex and maturity were determined by macroscopic examination of gonads and claspers with maturity scales, as proposed by Stehmann (1987). Stomachs were removed and classified as either everted, regurgitated, with bait, empty, or with contents. Individuals falling in any of the first three categories, as well as those that had obviously eaten fish hooked on the longline, were excluded from further analysis. Stomachs with contents were placed in plastic bags and frozen (within about 2 h of capture) for subsequent analysis. Stomach contents, which partly consisted of a turbid suspension, were washed with water in a nylon net of approximately 0.5-mm mesh size to allow easier examination. The items were carefully separated, weighed (after removing the surface water by blotting them in tissue paper), and identified to the lowest possible taxonomic level. Individuals of each identified taxon were counted. Whenever fragments were found, the number of individuals was taken as the smallest possible number of individuals from which fragments could have originated.
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Precision estimates in diet studies have been advocated and used by several authors (Ferry and Cailliet, 1996; Morato et al., 1999). We used the cumulative trophic diversity, measured with the Shannon-Wiener index [as [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII], where [P.sub.i] is the proportion of individuals in the ith species] to measure sample size sufficiency (Hurtubia, 1973). Cumulative numbers of randomly pooled stomachs were plotted against the cumulative trophic diversity. The asymptote of the curve indicates the minimum number of stomachs required. Frequency of occurrence (%O), percentage number (%N), and weight (%W) for each prey type were used to describe the diet of both species (for a review see Hyslop, 1980; Cortes, 1997). Wet weight was used to determine the latter value. The index of relative importance [IRI=(%N + %W) x %O] (Pinkas et al., 1971) and the %IRI (as [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]) were calculated for each prey category and used in diet comparisons. Prey taxa occurring in less than five stomachs were grouped into higher taxonomic categories. Outogenetic differences in the diet of thornback rays were examined by grouping fish into four size classes (49-60, 61-70, 71-80, and 81-93 cm TL). The diet of thornback rays was also analyzed by sex, depth (0-100, 101-200, 201-350 m), and area of capture (coastal areas and offshore banks). No further analyses were performed for tope shark because their diet was dominated by only one prey category (see "Results" section). To determine if the most important preys were similar for different groups of rays, weighted correlation and concordance analyses were used (Zar, 1999). These methods were preferred to conventional rank correlation methods (e.g. Spearman) because they emphasize the high ranking given to the most important prey categories. Differences in the rankings of IRI values for prey categories between three or more groups (e.g. three size classes) were tested for significance with the top-down concordance method ([C.sub.T]= top-down concordance coefficient) (Zar, 1999). For paired groups (e.g. males and females) the top-down correlation method ([r.sub.T]= top-down correlation coefficient) was used (Quade and Salama, 1992; Zar, 1999). Schoener's dietary overlap index (Schoener, 1970) (as [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII], where [P.sub.xi] was the proportion (based on %IRI) of food category i in the diet of x; and Pyi was the proportion of food category i in the diet of y) was used to measure the diet overlap between sex, size classes, depth strata, and area of capture.
Cluster analysis was used to describe geographic similarities in the feeding habits of thornback rays. A predator-prey matrix was built from published data. When more than one index was available, the following criteria were used to choose between indexes: IRI or %IRI, %0, %N, %W, %Volume. The number of prey categories included was based on the quality of the description found in the published sources. Eleven different categories were obtained. A distance matrix was then calculated by using Euclidean distance, and the hierarchical form of analysis was applied (Clarke and Warwick, 1994). The grouping of predators was based on the "average linkage method," and a dendrogram was used as a graphic form of representation. Finally, trophic levels (TL[v.sub.k]) were estimated for each of the samples (k) by using the method proposed by Cortes (1999) [as [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII], where TL[v.sub.i] is the trophic level of each prey category as estimated by the author, [P.sub.ik] is the proportion of prey category i in sample k]. Mean trophic levels were also estimated for groups resulting from the cluster analysis, and differences between them were tested by using oneway ANOVA (Zar, 1999).
Thornback rays were caught at depths ranging from 10 to 350 m, but primarily (95%) shallower than 250 m. Out of 237 stomachs examined, the contents of four appeared to have been regurgitated (1.7%), seven contained bait only (2.9%), 88 were empty (37.1%), and 138 contained prey (58.2%). Rays with stomachs containing food measured from 49.0 to 93.0 cm TL. All tope sharks were caught between 10 and 150 m depth, except for one individual taken at 300 m. Out of 365 stomachs examined, 174 (47.7%) were empty, seven (1.9%) contained fish hooked on the longline and 184 stomachs (50.4%) contained prey. Sharks with stomachs containing food ranged from 58.0 to 153.0 cm TL. The cumulative trophic diversity curves of both species appeared to reach an asymptote, suggesting that a sufficient number of stomachs were analyzed for both the thornback ray and tope shark (Fig. 2).
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The main diet components of thornback rays were fish (%IRI=81.6) and crustaceans reptants (%IRI=17.4) (Fig. 3). Fish occurred in 84.1% of stomachs that contained food, and represented 78.0% of total prey weight and 50.2% of total prey number (Table 1). Two benthopelagic species, the snipefish (Macroramphosus scolopax [%IRI=34.0]) and the boarfish (Capros aper [%IRI=26.8]), were by far the predominant fish prey items. However, some pelagic fish prey were also recorded in the stomachs of thornback rays: the chub mackerel, (Scomber japonicus [%IRI=0.3]) and the blue jack mackerel (Trachurus picturatus [%IRI=0.3]). Some individuals also fed upon mesopelagic myctophids (%IRI<0.1) and upon shallow water benthic fish such as the red striped mullet (Mullus surmuletus [%IRI<0.1]) and the Azorean chromis (Chromis limbata [%IRI<0.1]).
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Reptants occurred in 47.1% of the stomachs examined and represented 17.0% by weight and 31.9% by number of the total prey found (Fig. 3A). Swimming crabs (Liocarcinus spp. [%IRI=5.5]), which include both L. marmoreus (%IRI=2.8) and L. corrugatus (%IRI=0.8), were the most important reptant prey item in the diet of thornback ray (Table 1). Other important reptants included the lesser locust lobster (Scyllarus arctus [%IRI=0.9]), the shamefaced crab (Calappa granulata [%IRI=0.5]), as well as some unidentified Diogenidae (%IRI=0.3) and brachyura (%IRI=1.5).
Polychaetes (%IRI=0.8) were the third most important prey category and occurred in 9.4% of the stomachs with food (Fig. 3A). Mysids (%IRI=0.5), natants (%IRI=0.3), isopods (%IRI=0.2), and cephalopods (%IRI=0.1) also occurred in stomachs of thornback rays sampled in the Azores (Table 1).
A comparison of thornback ray's diet in relation to sex, length, depth and area of capture (Table 2) suggests that C. aper and M. scolopax were by far the most important prey for all subgroups examined. The diets of both sexes were significantly correlated ([r.sub.T]=0.70, P<0.01), indicating a high degree of similarity in the diets of males and females. Both sexes fed primarily upon two benthopelagic fish species (M. scolopax and C. aper) and reptants (Table 2). Schoener's diet overlap index between males and females was 0.72, also indicating a high level of similarity between diets.
Significant concordance ([C.sub.T]=0.74,P<0.01) was displayed among thornback rays of different size classes (49-60, 61-70, 71-80 and 81-93 cm TL). Prey categories had similar %IRI values for the different size classes (Table 2), with the exception of reptants (both Liocarcinus spp. and "other reptants"), which were more important in the diet of the two middle size classes. Schoener's index also suggested a high degree of overlap (>0.60) among all size classes (Table 3).
Examination of depth-related differences was limited by the small sample size of rays from deeper waters ([n.sub.201-350m]=13). However, the top-down concordance coefficient suggested that individuals captured at different depths (0-100, 101-200, and 201-350 m) do not feed upon the same most important prey categories ([C.sub.T]=0.52, P>0.05). Reptants (both Liocarcinus spp. and "other reptants") and the fish species T. picturatus were more important in the diet of rays captured in shallow waters (0-100 m); whereas polychaetes, cephalopods, penaeids, mysids, seabreams (Pagellus sp.), and myctophids were consumed more by rays caught in deeper waters (Table 2). Schoener's overlap index for individuals captured at different depth intervals (Table 3) indicated low overlap (=0.50), supporting the results ot the top-down concordance coefficient analysis.
Finally, the diet of rays caught in coastal areas and offshore banks were not significantly correlated ([C.sub.T]=0.44, P>0.05), indicating that thornback rays feed upon different prey depending on the environment. The Diogenidae, Liocarcinus spp., "other reptants," and "other Pisces" were more important prey for rays in coastal areas, whereas polychaetes, penaeids, cephalopods, mysids, seabreams (Pagellus sp.), and myctophids were more important for rays caught at offshore banks (Table 2). However, Schoener's index showed a high level of overlap (0.69) between the diets of rays caught in the different locations--most likely due to the high dominance of two benthopelagic fishes in their diets (75,4% and 69.1% for coastal areas and offshore banks, respectively).
Published information on the diet of thornback rays is summarized in Table 4. Estimations of mean trophic levels vary from 3.1, for the smallest size class (South Wales: <25 cm TL), to 4.2 for the Azorean thornback ray (this study; size classes 49-60 and 81-93 cm TL). The arbitrarily chosen cutoff in the cluster analysis was set at 60% dissimilarity, which divided the dendrogram into three groups with similar feeding patterns (Fig. 4). Cluster group I grouped the Azorean populations (all size classes) and had an estimated trophic level of 4.14 ([+ or -] 0.09 SD). Cluster group II contained all other medium and large size classes (i.e. >40 cm TL), with the exception of small rays from the Cantabrian Sea, North Spain (17-49 cm TL), and one small-to medium-size class of South Wales (35-45 cm TL). Cluster group III grouped small rays from several geographic regions, from South Africa (which also includes some large individuals) to NE Atlantic. Estimates of trophic levels were 3.46 ([+ or -] 0.84 SD) for the rays of the cluster group II (i.e. medium and large), and 3.35 ([+ or -] 0.21 SD) for the rays composing cluster group III (i.e. small). The estimated trophic levels for the three cluster groups were significantly different (P<0.001).
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The diet of tope shark consisted almost exclusively of fish (%IRI=99.95), along with a few crustaceans (%IRI=0.03) and cephalopods (%IRI=0.02) (Fig. 3B). Recognizable prey from 14 different taxa were identified (Table 5). The boarfish (C. aper) was the most important prey item (%IRI=93.2), accounting for 65.0% of food by number (%N), 25.6% by weight (%W), and occurred in 38.6% of stomachs that contained food (%0). The second most important prey item was the snipefish (M. scolopax [%IRI=3.0]), which represented 11.2% of food by number and 2.7% by weight. Some commercially important fish species were also found in the stomachs of tope shark; sparids (%IRI=4.5, which included Pagellus acarne, P. bogaraveo, and Pagrus pagrus), the chub mackerel (S. japonicus [%IRI=0.9]), and the blue jack mackerel (T. picturatus [%IRI--0.6]). These species were more important by weight than by number or occurrence. The stomachs of tope sharks also contained 493 pairs of eye lens and fish that were heavily digested, as well as unidentifiable otoliths.
In general, the percentage of empty stomachs for thornback rays and tope sharks was relatively high compared to the percentage from literature reports. The percentage of empty stomachs for tope shark was 47.7%--much higher than the 4.3% observed by Ellis et al. (1996). The percentage of empty thornback ray stomachs was high (37.1%) when compared to values reported for the North Sea (9%, Daan et al. (1); and 3.7%, Ellis et al., 1996), Carmarthen Bay, South Wales (4.5%, Ajayi, 1982), west coast of Southern Africa (4.5%, Ebert et al., 1991; and 2.6%, Smale and Cowley, 1992) and the Portuguese mainland coast (2.5%, Cunha et al., 1986). We attribute the high percentage of empty stomachs found in our study to the use of longlines to catch the fish in the Azores (trawls were used in the other studies). Longlining is a passive fishing method, which suggests that fish that feed to satiation have a reduced response to bait odor (Lokkeborg et al., 1995), meaning that fish with full stomachs tend not to eat the bait and be caught. Thus, only those fish with empty stomachs or partial stomach fullness were caught.
Thornback rays captured by longline in the Azores during the spring of 1996 and 1997 fed upon a wide variety of organisms. Fishes (81.6 %IRI) and reptants (17.4 %IRI) dominated the diet, which also consisted of polychaetes, mysids, natants, isopods, and cephalopods. In general, thornback rays in the Azores preyed more heavily upon fish in comparison with the predation patterns described in other studies. Ajayi et al. (1982) reported a predominance of crustaceans (83%W) for all size classes and a low importance of fish (11.6%W) in the diet of thoruback rays in Carmarthen Bay, Bristol Channel. They also reported amphipods, polychaetes, and some natants as food items. Using the points method of Hyslop (1980), Ellis et al. (1996) reported that thornback rays from the North Sea fed primarily on crustaceans (78.9%) compared to mollusks (10.2%) and fish (7.3%). Several others have also reported a dominance of crustaceans and low importance of fish in the diet of thornback ray (Fitzmaurice, 1974; Marques and Re, 1978; Quiniou and Andriamirado, 1979; Cunha et al., 1986; Gibson and Ezzi, 1987; Smale and Cowley, 1992; Olaso and Rodriguez-Marin, 1995; Daan et al. (1); Ebeling (2)). Polychaetes (Holden and Tucker, 1974; Marques and Re, 1978), bivalves (Quiniou and Andriamirado, 1979), halothurians (Ebeling (2)), and cephalopods (Holden and Tucker, 1974; Marques and Re, 1978; Smale and Cowley, 1992; Olaso and Rodriguez-Marin, 1995) that were considered important prey items in the other studies mentioned were not recorded or were insignificant in our samples.
Differences in diet composition of several predators may reflect the geographic peculiarities in fauna composition (e.g. Smale and Cowley 1992), but when comparing diets based on higher taxonomic levels (such as fish, reptants, and natants categories), such geographic differences should not be so obvious. Our geographic analysis (see Fig. 4) distinguished three major groups: I) the Azorean individuals; II) other large individuals; and III) other small individuals. Further, the estimated mean trophic levels for these three major groups were significantly different: 4.14 ([+ or -] 0.09 SD) for the Azores; 3.46 ([+ or -] 0.84 SD) for other large rays; and 3.35 ([+ or -] 0.21 SD) for smaller rays. The higher trophic level for the Azores is a result of a higher degree of piscivory in this region and an increased consumption of decapods and fish by larger rays, compared with small rays. Notwithstanding the difference in sampling methods (longline vs. trawl caught), it appears that the Azores can be considered a separate group. In other studies, predator size played the major role in controlling feeding patterns.
The diet of the thornback ray in the Azores consists of a greater proportion of fish than in any other area and may reveal differences in the function of different environments, because seamounts and oceanic islands are the major topographic feature of the Azores region and the other studies were conducted on continental shelves. The general function of oceanic seamount environments is still not completely understood but they are characterized by substantial enhancement of primary production due to topographic effects on local hydrographic conditions (Genin and Boehlert, 1985). However, evidence for enhanced primary production leading to concentrations offish over seamounts is sparse (Rogers, 1994). Additionally, the availability and relative abundance of the two most important fish prey items found in our work (the benthopelagic species C. aper and M. scolopax) vary considerably both seasonally (Granadeiro et al., 1998) and annually. Therefore, the high degree of piscivory in the Azores may result from environmental features and exceptional fish prey availability during the sampled years or seasons.
Thornback rays also fed on pelagic fish, as indicated by the presence of chub mackerel and jack mackerel in stomachs--a finding that confirms previous suggestions (see Daan et al. (1); Ebeling (2)) that thornback rays are active predators and able to feed semipelagically. The most important reptants in the diet, Liocarcinus spp., were also reported as the main prey item for thornback rays by Ellis et al. (1996). The level of importance of isopods and amphipods, mysids, cephalopods, and polychaetes in the diet of thornback rays in the Azores was similar to values reported by other authors (Ellis et al., 1996; Daan et al. (1); Ebeling (2)).
Differences in the dentition of females and males were reported by Quiniou and Andriamirado (1979) but we and Smale and Cowley (1992) observed no differences in the major prey consumed between sexes. Therefore, sexual dimorphism in dentition does not appear to be manifested in dietary preferences between sexes, as was initially expected.
Several studies have demonstrated differences in predation patterns for rays of different size classes--primarily a decrease in importance of crustaceans and an increase of fish with size (e.g. Smale and Cowley, 1992; Ellis et al., 1996; Daan et al. (1); Ebeling (2)). Some authors attribute these differences to the ability of large predators to prey upon larger prey (Smale and Cowley, 1992); others suggest the difference is due to a pronounced shift from a benthic to a benthopelagic feeding behavior (Skjraasen and Bergstad, 2000; Ebeling (2)) or the reverse (Quiniou and Andriamirado, 1979). We found no significant size-related differences in diet. Quiniou and Andriamirado (1979) reported shifts in diet at a size of 30 to 40 cm TL but we could not verify these conclusions because our sample included only rays larger than 49 cm.
There have been few data indicating dietary differences between thornback rays collected at different depths. Smale and Cowley (1992) reported that bottom type used by rays varies with depth and predicted that the prey spectrum would thus also vary, but no depth-related analyses of diet composition were preformed in their study. Despite similarities in size (i.e. no differences in the mean size by depth strata; Menezes (3)), we found that rays inhabiting different depths prey upon different resources. The decreasing consumption of Liocarcinus spp., "other reptants," and T picturatus, and the increasing consumption of penaeids, seabreams, and myctophids with depth of capture of rays, appears to be in general agreement with the relative abundance of prey with depth. Therefore, such depth-related variations in diet may simply reflect differences in prey availability. It is not clear, however, why Scyllarus arctus, a species with a known depth distribution of 4 to 50 meters (e.g. Alvarez, 1968; Castellon and Abello, 1983), appears in stomachs of thornback rays caught between 201 and 350 meters (see Table 2). There is no evidence of vertical migrations of thornback ray associated with feeding activity; therefore this prey was likely eaten at deep water. Thus, the depth distribution range of S. arctus in the Azores may be significantly greater than what was previously known. The only study that could corroborate this hypothesis (Fransen, 1991) reported one S. arctus caught between 420 and 700 meters depth in the Canary Islands.
Our comparisons between areas (coastal and offshore banks) were unable to clearly separate the influence of depth because nearly all coastal samples were obtained from shallow waters, and offshore bank samples were collected from much deeper waters. Hence, we were incapable of determining whether the high level of polychaetes, penaeids, cephalopods, mysids, seabreams, and myctophids in the diet of rays caught at offshore banks reflects the availability of these prey in these areas, or in deeper waters, or both. Nevertheless, our findings indicate that coastal rays have different diets from rays taken in offshore banks.
Tope sharks preyed almost exclusively upon teleosts, along with very few crustaceans and cephalopods. Previous observations on the feeding behavior of this species suggested that fish and cephalopods are the main prey categories (Ellis et al., 1996; Olsen, 1954). The diet of tope shark in the Azores consists of fewer species (mainly small shoaling fish, mainly boarfish and snipefish) compared to the diet of tope shark documented in previous studies. These two fish were also important diet components of other piscivorous species around the Azores between 1993 and 1997, namely cephalopods (Pierce et al., 1994), elasmobranchs (Clarke et al., 1996), fishes (Clarke et al., 1995; Morato et al., 1999, 2000, 2001) and seabirds (Granadeiro et al., 1998; Ramos et al., 1998a, 1998b). The role of these two small shoaling fish in the marine food web of the Azores is not yet fully understood. The fact that these prey may exhibit strong variation in abundance, raises the question of how well predators can adapt to extensive changes in their availability.
Stomach-content data offer a good snapshot of the feeding habits of fish species, but diets may vary substantially with food availability, depth, location, and season. Caution is, therefore, required when drawing conclusions about the trophic ecology of marine predators. The trophic role of thornback rays and tope sharks in the Azores could be further clarified by year round sampling and by an analysis of stable isotopes (Gu et al., 1996; Jennings et al., 1997; Pinnegar and Polunin, 2000), which could provide a less biased average estimate of predator trophic level.
Table 1 Values for percentage by number (%N), weight (%W), occurrence (%O), and index of relative importance (IRI and %IRI) for prey items observed in stomachs (n=138) of thornback rays (Raja clavata) caught off the Azores during the spring of 1996 and 1997. Total values are given in bold font. Prey items %N %W Algae 0.3 0.0 Bivalvia--Chlamys sp. 0.1 0.0 Total Cephalopoda# 1.1# 1.1# Octopodoidea unidentified 0.1 0.1 Scaeurgus unicirrhus 0.7 0.8 Cephalopoda unidentified 0.3 0.2 Total Polychaeta# 3.4# 0.8# Hirudinea 0.1 0.0 Crustacea Stomatopoda 0.1 0.0 Total Natantia# 3.1# 1.0# Penaeidea unidentified 1.4 0.3 Solenocera membranacea 0.1 0.1 Solenocera sp. 0.1 0.1 Pandalidae 0.3 0.1 Processa intermedia 0.1 0.0 Processa sp. 0.1 0.0 Caridea unidentified 0.1 0.0 Natantia unidentified 0.9 0.4 Total Reptantia# 31.9# 17.0# Anomura unidentified 0.1 0.1 Scyllaridae Scyllarus arctus 4.0 0.8 Diogenidae 1.1 1.7 Paguridea 0.3 0.3 Galatheidae Galathea sp. 0.3 0.1 Homolidae Paromola cuvieri 0.6 0.1 Calappidae Calappa granulata 1.8 1.3 Parthenopidae Parthenope sp. 2.8 0.7 Portunidae 0.1 0.0 Total Liocarcinus spp.# 14.9# 8.3# Liocarcinus marmoreus 9.8 5.1 Liocarcinus corrugatus 3.8 2.7 Liocarcinus spp. 1.3 0.5 Brachyura 4.1 2.4 Reptantia unidentified 0.6 0.4 Decapoda unidentified 0.1 0.0 Total Mysidacea# 6.6# 0.7# Isopoda 1.6 0.3 Amphipoda-Vibilia sp. 0.1 0.0 Crustacea unidentified 1.1 0.8 Total Pisces# 50.2# 78.0# Myctophidae 0.6 0.3 Moridae Gadella maraldi 0.1 0.2 Caproidae Capros aper 13.7 24.7 Macroramphosidae Macroramphosus scolopax 16.7 19.3 Sparidae Pagellus spp. 1.0 5.4 Mullidae Mullus surmuletus 0.1 3.0 Pomacentridae Chromis limbata 0.1 0.2 Carangidae Trachurus picturatus 0.9 2.6 Scombridae Scomber japonicus 0.4 6.0 Pisces unidentified 16.6 16.3 Rocks 1.0 0.3 Tissue unidentified 0.4 0.8 Prey items %0 (1) IRI Algae 1.5 0.5 Bivalvia--Chlamys sp. 0.7 0.1 Total Cephalopoda# 5.1# 11.2# Octopodoidea unidentified 0.7 0.1 Scaeurgus unicirrhus 2.9 4.4 Cephalopoda unidentified 1.5 0.8 Total Polychaeta# 9.4# 39.5# Hirudinea 0.7 0.1 Crustacea Stomatopoda 0.7 0.1 Total Natantia# 10.1# 41.4# Penaeidea unidentified 2.9 4.9 Solenocera membranacea 0.7 0.1 Solenocera sp. 0.7 0.1 Pandalidae 0.7 0.3 Processa intermedia 0.7 0.1 Processa sp. 0.7 0.1 Caridea unidentified 0.7 0.1 Natantia unidentified 2.9 3.8 Total Reptantia# 47.1# 2303.2# Anomura unidentified 0.7 0.1 Scyllaridae Scyllarus arctus 9.4 45.1 Diogenidae 5.8 16.2 Paguridea 1.5 0.9 Galatheidae Galathea sp. 1.5 0.6 Homolidae Paromola cuvieri 2.9 2.0 Calappidae Calappa granulata 7.3 22.6 Parthenopidae Parthenope sp. 0.7 2.5 Portunidae 0.7 0.1 Total Liocarcinus spp.# 16.6# 385.1# Liocarcinus marmoreus 9.4 140.1 Liocarcinus corrugatus 6.5 42.3 Liocarcinus spp. 2.2 4.0 Brachyura 11.6 75.4 Reptantia unidentified 2.9 2.9 Decapoda unidentified 0.7 0.1 Total Mysidacea# 3.6# 26.3# Isopoda 5.1 9.7 Amphipoda-Vibilia sp. 0.7 0.1 Crustacea unidentified 4.4 8.4 Total Pisces# 84.1# 10811.2# Myctophidae 2.2 2.0 Moridae Gadella maraldi 0.7 0.2 Caproidae Capros aper 34.8 1336.3 Macroramphosidae Macroramphosus scolopax 47.1 1695.6 Sparidae Pagellus spp. 4.4 28.2 Mullidae Mullus surmuletus 0.7 2.2 Pomacentridae Chromis limbata 0.7 0.2 Carangidae Trachurus picturatus 3.6 12.6 Scombridae Scomber japonicus 2.2 14.1 Pisces unidentified 43.5 1431.2 Rocks 5.1 6.6 Tissue unidentified 2.2 2.6 Prey items %IRI Algae 0.0 Bivalvia--Chlamys sp. 0.0 Total Cephalopoda# 0.1# Octopodoidea unidentified 0.0 Scaeurgus unicirrhus 0.1 Cephalopoda unidentified 0.0 Total Polychaeta# 0.8# Hirudinea 0.0 Crustacea Stomatopoda 0.0 Total Natantia# 0.3# Penaeidea unidentified 0.1 Solenocera membranacea 0.0 Solenocera sp. 0.0 Pandalidae 0.0 Processa intermedia 0.0 Processa sp. 0.0 Caridea unidentified 0.0 Natantia unidentified 0.1 Total Reptantia# 17.4# Anomura unidentified 0.0 Scyllaridae Scyllarus arctus 0.9 Diogenidae 0.3 Paguridea 0.0 Galatheidae Galathea sp. 0.0 Homolidae Paromola cuvieri 0.0 Calappidae Calappa granulata 0.5 Parthenopidae Parthenope sp. 0.0 Portunidae 0.0 Total Liocarcinus spp.# 5.5# Liocarcinus marmoreus 2.8 Liocarcinus corrugatus 0.8 Liocarcinus spp. 0.1 Brachyura 1.5 Reptantia unidentified 0.1 Decapoda unidentified 0.0 Total Mysidacea# 0.5# Isopoda 0.2 Amphipoda-Vibilia sp. 0.0 Crustacea unidentified 0.2 Total Pisces# 81.6# Myctophidae 0.0 Moridae Gadella maraldi 0.0 Caproidae Capros aper 26.8 Macroramphosidae Macroramphosus scolopax 34.0 Sparidae Pagellus spp. 0.6 Mullidae Mullus surmuletus 0.0 Pomacentridae Chromis limbata 0.0 Carangidae Trachurus picturatus 0.3 Scombridae Scomber japonicus 0.3 Pisces unidentified 28.7 Rocks 0.1 Tissue unidentified 0.1 (1) Because the %0 is a nonadditive index (Cortes, 1997) for grouping fish items into higher taxonomic categories (i.e. Pisces, etc), the %0 value was recalculated by considering the number of stomachs with the respective higher taxonomic category. This recalculation affects both the IRI and %IRI values. Note: Total values are given in bold indicated with #. Table 2 Percentage of relative importance (%IRI) of food categories of Raja clavata by sex, total length, depth strata, and areas (coastal and offshore banks). Prey items occurring in less than five stomachs were grouped into higher taxonomic levels. The null hypothesis of not feeding upon the same most important prey categories was tested by using the top-down correlation method (being [r.sub.T] the top-down correlation coefficient) and the top-down concordance method (being [C.sub.T] the top-down concordance coefficeint). NS = non significant, * P<0.01. Sex Total length (cm) F M 49-60 61-70 71-80 81-93 Cephalopoda 0.52 0.03 1.44 0.00 0.38 0.63 Polychaeta 0.62 1.70 0.21 0.43 0.73 6.44 Penaeidea 0.34 0.62 0.72 1.32 0.18 0.00 Other Natantia 0.10 0.15 0.52 0.11 0.06 0.00 Diogenidae 0.07 1.58 1.45 0.00 0.88 0.45 Scyllarus arctus 1.54 0.57 1.12 0.25 2.48 0.64 Calappa granulata 0.73 0.31 0.45 0.30 0.90 0.36 Liocarcinus spp. 8.12 0.60 1.64 3.30 9.49 0.19 Other Reptantia 9.20 8.32 1.43 11.88 22.48 0.00 Mysidacea 0.68 0.50 0.18 0.62 1.02 0.00 Isopoda 0.53 0.00 0.00 0.24 0.30 0.35 Capros aper 41.20 24.16 36.26 38.11 23.39 53.34 Macroramphosus scolopax 35.15 58.88 53.60 41.65 34.91 37.35 Pagellus sp. 0.46 1.07 0.00 1.08 1.24 0.00 Myctophidae 0.04 0.12 0.00 0.14 0.09 0.00 Trachurus picturatus 0.14 0.57 0.34 0.00 0.87 0.26 Other Pisces 0.58 0.82 0.64 0.56 0.61 0.00 [r.sub.T]=0.70 * [C.sub.T]=0.74 * Stomachs with contents (n) 89 49 19 47 60 11 Depth (m) Areas 0-100 101-200 201-350 Banks Coastal Cephalopoda 0.03 0.21 5.60 3.48 0.06 Polychaeta 0.54 0.40 15.13 4.23 0.57 Penaeidea 0.19 0.12 14.72 1.41 0.29 Other Natantia 0.48 0.01 0.00 0.08 0.12 Diogenidae 0.69 0.21 0.00 0.00 0.53 Scyllarus arctus 0.76 0.84 4.35 0.91 1.21 Calappa granulata 0.00 1.52 0.00 0.10 0.64 Liocarcinus spp. 10.44 1.43 0.00 0.00 12.30 Other Reptantia 47.44 0.31 0.00 0.52 6.33 Mysidacea 0.00 1.00 2.21 16.79 0.00 Isopoda 0.02 0.47 0.00 0.00 0.31 Capros aper 20.06 38.26 10.63 35.56 32.53 Macroramphosus scolopax 15.81 54.84 36.72 33.50 42.91 Pagellus sp. 0.56 0.19 9.99 2.27 0.43 Myctophidae 0.03 0.04 0.65 1.16 0.01 Trachurus picturatus 1.25 0.01 0.00 0.00 0.40 Other Pisces 1.71 0.15 0.00 0.00 1.36 [C.sub.T]=[0.51.sup.NS] [r.sub.T]= [0.44.sup.NS] Stomachs with contents (n) 47 78 13 24 110 Table 3 Schoener's diet overlap index for thornback rays (Raja clavata) size classes and for different depth strata. Depth (m) Total length (cm) 101-200 201-350 61-70 71-80 81-93 0-100 0.40 0.29 49-60 0.83 0.66 0.76 201-350 0.50 61-70 0.77 0.77 71-80 0.62 Table 4 Categorized diets of thornback ray in different geographic locations. Estimation of trophic level (TL) following Cortes (1999) is also presented. Abbrevations of prey categories: POL = Polychaeta;BIV = Bivalvia; ECH = Echinodermata; CEP = Cephalopoda; ISO = Isopoda; AMP = Amphipoda; MYS = Mysidacea; STO = Stomatopoda; NAT = Natantia; REP = Reptantia; PIS = Pisces. PM is the point method (Hyslop, 1980). Numbers in the reference (Ref.) list represent the following studies: 1 = Ellis et al. (1996); 2 = Gibson and Ezzi (1987); 3 = Ayayi (1982); 4 = Quiniou and Andriamirado (1979); 5 = Olaso and Rodriguez-Marin (1995); 6 = Cunha et al. (1986); 7 = present study; 8 = Ebert et al. (1991); 9 = Smale and Cowley (1992). TLv = trophic level. Prey categories Size class Location (cm TL) Index POL BIV NE Atlantic <40 PM 5.20 0.50 NE Atlantic 40-69 PM 4.70 3.50 NE Atlantic >69 PM 3.00 2.90 Scotland West Coast <40 %IRI 2.40 0.00 Wales South Coast <25 %W 0.00 0.00 Wales South Coast 25-34.9 %W 3.04 0.00 Wales South Coast 35-44.9 %W 3.80 0.00 Wales South Coast 45-64.9 %W 3.90 0.00 Wales South Coast 65-84.9 %W 1.40 0.00 Wales South Coast >85 %W 1.73 0.00 France NW Coast 10-30 %CN 0.00 2.34 France NW Coast 31-50 %CN 0.00 3.75 France NW Coast 51-70 %CN 0.00 16.53 France NW Coast 71-95 %CN 0.00 21.45 Spain N Coast 17-49 %V 2.26 0.00 Spain N Coast 50-89 %V 0.00 0.00 Portugal West Coast <50 (1) %Q 0.01 0.00 Portugal West Coast >50 (1) %Q 0.03 0.00 Portugal Azores 49-60 %IRI 0.21 0.00 Portugal Azores 61-70 %IRI 0.43 0.00 Portugal Azores 71-80 %IRI 0.73 0.00 Portugal Azores 81-93 %IRI 6.44 0.00 South Africa West coast 30-86 %IRI 0.00 0.00 South Africa Cape South <57 %IRI 0.00 0.00 South Africa Cape South >57 %IRI 0.21 0.00 Prey categories Location ECH CEP ISO AMP MYS NE Atlantic 0.00 4.50 0.20 2.70 2.90 NE Atlantic 0.00 1.60 0.70 3.70 0.80 NE Atlantic 0.30 0.60 0.00 0.00 0.00 Scotland West Coast 3.60 0.00 0.00 32.90 10.50 Wales South Coast 0.00 0.00 0.00 0.00 0.00 Wales South Coast 0.00 0.00 0.00 0.00 0.00 Wales South Coast 0.00 0.00 0.00 0.00 0.00 Wales South Coast 0.00 0.00 0.00 0.00 0.00 Wales South Coast 0.00 0.00 0.00 0.00 0.00 Wales South Coast 0.00 0.00 0.00 0.00 0.00 France NW Coast 0.00 0.00 0.00 12.50 22.46 France NW Coast 0.00 0.00 0.00 19.35 0.81 France NW Coast 0.00 0.00 0.00 2.02 0.00 France NW Coast 0.00 0.00 0.00 0.00 0.00 Spain N Coast 0.00 0.00 0.00 0.00 2.26 Spain N Coast 0.00 4.70 0.00 0.00 0.00 Portugal West Coast 0.00 0.01 0.17 0.09 1.83 Portugal West Coast 0.00 0.52 0.00 0.00 0.00 Portugal Azores 0.00 1.44 0.00 0.00 0.18 Portugal Azores 0.00 0.00 0.24 0.00 0.62 Portugal Azores 0.00 0.38 0.30 0.00 1.02 Portugal Azores 0.00 0.63 0.35 0.00 0.00 South Africa West coast 0.00 0.00 0.00 0.00 1.13 South Africa Cape South 0.00 0.08 0.00 0.00 20.86 South Africa Cape South 0.00 0.31 0.00 3.21 1.33 Prey categories Location STO NAT REP PIS NE Atlantic 0.00 52.40 16.30 2.60 NE Atlantic 0.00 17.00 60.90 5.70 NE Atlantic 0.00 7.10 73.60 11.30 Scotland West Coast 0.00 27.90 16.10 0.00 Wales South Coast 0.00 63.65 16.15 2.88 Wales South Coast 0.00 42.12 38.30 8.68 Wales South Coast 0.00 22.23 64.21 3.98 Wales South Coast 0.00 1.68 72.88 13.76 Wales South Coast 0.00 2.22 85.41 1.33 Wales South Coast 0.00 0.00 67.12 25.08 France NW Coast 0.00 55.97 2.42 0.00 France NW Coast 0.00 27.02 42.94 0.00 France NW Coast 0.00 9.27 70.56 0.00 France NW Coast 0.00 0.32 75.16 0.00 Spain N Coast 0.00 33.87 58.39 0.00 Spain N Coast 0.00 4.41 84.64 6.52 Portugal West Coast 0.00 86.38 3.36 7.63 Portugal West Coast 0.00 24.66 73.23 1.52 Portugal Azores 0.00 1.24 6.09 90.84 Portugal Azores 0.00 1.43 15.73 81.54 Portugal Azores 0.00 0.24 36.23 61.11 Portugal Azores 0.00 0.00 1.64 90.95 South Africa West coast 20.75 41.01 3.01 34.10 South Africa Cape South 12.39 10.59 47.84 8.23 South Africa Cape South 5.71 10.72 72.80 5.71 Prey categories Location Ref. TLv NE Atlantic 1 3.2 NE Atlantic 1 3.5 NE Atlantic 1 3.6 Scotland West Coast 2 3.2 Wales South Coast 3 3.1 Wales South Coast 3 3.4 Wales South Coast 3 3.4 Wales South Coast 3 3.4 Wales South Coast 3 3.3 Wales South Coast 3 3.5 France NW Coast 4 3.3 France NW Coast 4 3.3 France NW Coast 4 3.4 France NW Coast 4 3.4 Spain N Coast 5 3.4 Spain N Coast 5 3.6 Portugal West Coast 6 3.6 Portugal West Coast 6 3.5 Portugal Azores 7 4.2 Portugal Azores 7 4.1 Portugal Azores 7 4.0 Portugal Azores 7 4.2 South Africa West coast 8 3.7 South Africa Cape South 9 3.5 South Africa Cape South 9 3.5 (1) TL was estimated from disk width (DW) and by using the length-length relationship for the Azores; DW=0.1087+0.7002TL (unpubl. data). Table 5 Values for percentage by number (%N), weight (%W), occurrence (%0), and index of relative importance (IRI and %IRI) for prey items observed in stomachs of tope shark (n=184), Galeorhinus galeus, caught off the Azores during the spring of 1996 and 1997. Number (No.) and percent occurrence (%0) of fish lenses, fish remains, and otoliths found in stomach, are also presented. Total values are given in bold font. Prey items %N %W Total Crustacea 1.0# 1.0# Isopoda 3.6 1.1 Crustacea unidentified 1.2 0.0 Total Cephalopoda 0.8# 0.2# Octopodidae 0.6 0.3 Cephalopoda unidentified 3.0 0.0 Total Pisces (2) 98.2# 98.8# Sternoptychidae unidentified 0.6 0.2 Synodontidae Synodus sp. 0.6 11.5 Trichiuridae Lepidopus caudatus 0.6 0.0 Macrouridae unidentified 0.6 0.0 Phycidae Phycis phycis 1.2 0.0 Caproidae Capros aper 65.0 25.6 Macroramphosidae Macraramphosus scolopax 11.2 2.7 Carangidae Trachurus picturatus 2.4 7.6 Total Sparidae 6.5# 32.0# Pagellus acarne 2.4 5.8 Pagellus bogaraveo 2.4 14.4 Pagellus spp. 1.2 11.7 Pagrus pagrus 0.6 0.1 Sparidae unidentified 0.6 0.5 Scombridae Scomber japonicus 2.4 18.4 No. of 0% Pairs of fish lenses 493 103 Otoliths unidentified 118 75 Fish remains 3 2 Prey items %0 (1) IRI Total Crustacea 3.3# 6.5# Isopoda 2.7 12.8 Crustacea unidentified 1.1 1.3 Total Cephalopoda 3.3# 3.2# Octopodidae 0.5 0.5 Cephalopoda unidentified 2.7 8.1 Total Pisces (2) 100.0# 19,700.4# Sternoptychidae unidentified 0.5 0.4 Synodontidae Synodus sp. 0.5 6.5 Trichiuridae Lepidopus caudatus 0.5 0.4 Macrouridae unidentified 0.5 0.3 Phycidae Phycis phycis 1.1 1.4 Caproidae Capros aper 38.6 3494.6 Macroramphosidae Macraramphosus scolopax 8.2 113.5 Carangidae Trachurus picturatus 2.2 21.6 Total Sparidae 4.4# 169.7# Pagellus acarne 1.6 13.3 Pagellus bogaraveo 1.6 27.3 Pagellus spp. 1.1 14.1 Pagrus pagrus 0.5 0.4 Sparidae unidentified 0.5 0.6 Scombridae Scomber japonicus 1.6 33.8 Pairs of fish lenses Otoliths unidentified Fish remains Prey items %IRI Total Crustacea 0.03# Isopoda 0.3 Crustacea unidentified 0.0 Total Cephalopoda 0.02# Octopodidae 0.0 Cephalopoda unidentified 0.2 Total Pisces (2) 99.95# Sternoptychidae unidentified 0.0 Synodontidae Synodus sp. 0.2 Trichiuridae Lepidopus caudatus 0.0 Macrouridae unidentified 0.0 Phycidae Phycis phycis 0.0 Caproidae Capros aper 93.2 Macroramphosidae Macraramphosus scolopax 3.0 Carangidae Trachurus picturatus 0.6 Total Sparidae 4.5# Pagellus acarne 0.4 Pagellus bogaraveo 0.7 Pagellus spp. 0.4 Pagrus pagrus 0.0 Sparidae unidentified 0.0 Scombridae Scomber japonicus 0.9 Pairs of fish lenses Otoliths unidentified Fish remains (1) Because the %0 is a nonadditive index (Cortes, 1997), when grouping fish items into higher taxonomic categories (i.e. Pisces, etc) the %0 value was recalculated considering the number of stomachs with the respective higher taxonomic category. This recalculation will affect both the IRI and %IRI values. (2) Including unidentified fish, pairs of lenses, otoliths, and fish remains. Note: Total values are given in bold indicated with #. Table 5 Values for percentage by number (%N), weight (%W), occurrence (%0), and index of relative importance (IRI and %IRI) for prey items observed in stomachs of tope shark (n=184), Galeorhinus galeus, caught off the Azores during the spring of 1996 and 1997. Number (No.) and percent occurrence (%0) of fish lenses, fish remains, and otoliths found in stomach, are also presented. Total values are given in bold font. Prey items %N %W Total Crustacea 1.0# 1.0# Isopoda 3.6 1.1 Crustacea unidentified 1.2 0.0 Total Cephalopoda 0.8# 0.2# Octopodidae 0.6 0.3 Cephalopoda unidentified 3.0 0.0 Total Pisces (2) 98.2# 98.8# Sternoptychidae unidentified 0.6 0.2 Synodontidae Synodus sp. 0.6 11.5 Trichiuridae Lepidopus caudatus 0.6 0.0 Macrouridae unidentified 0.6 0.0 Phycidae Phycis phycis 1.2 0.0 Caproidae Capros aper 65.0 25.6 Macroramphosidae Macraramphosus scolopax 11.2 2.7 Carangidae Trachurus picturatus 2.4 7.6 Total Sparidae 6.5# 32.0# Pagellus acarne 2.4 5.8 Pagellus bogaraveo 2.4 14.4 Pagellus spp. 1.2 11.7 Pagrus pagrus 0.6 0.1 Sparidae unidentified 0.6 0.5 Scombridae Scomber japonicus 2.4 18.4 No. of 0% Pairs of fish lenses 493 103 Otoliths unidentified 118 75 Fish remains 3 2 Prey items %0 (1) IRI Total Crustacea 3.3# 6.5# Isopoda 2.7 12.8 Crustacea unidentified 1.1 1.3 Total Cephalopoda 3.3# 3.2# Octopodidae 0.5 0.5 Cephalopoda unidentified 2.7 8.1 Total Pisces (2) 100.0# 19,700.4# Sternoptychidae unidentified 0.5 0.4 Synodontidae Synodus sp. 0.5 6.5 Trichiuridae Lepidopus caudatus 0.5 0.4 Macrouridae unidentified 0.5 0.3 Phycidae Phycis phycis 1.1 1.4 Caproidae Capros aper 38.6 3494.6 Macroramphosidae Macraramphosus scolopax 8.2 113.5 Carangidae Trachurus picturatus 2.2 21.6 Total Sparidae 4.4# 169.7# Pagellus acarne 1.6 13.3 Pagellus bogaraveo 1.6 27.3 Pagellus spp. 1.1 14.1 Pagrus pagrus 0.5 0.4 Sparidae unidentified 0.5 0.6 Scombridae Scomber japonicus 1.6 33.8 Pairs of fish lenses Otoliths unidentified Fish remains Prey items %IRI Total Crustacea 0.03# Isopoda 0.3 Crustacea unidentified 0.0 Total Cephalopoda 0.02# Octopodidae 0.0 Cephalopoda unidentified 0.2 Total Pisces (2) 99.95# Sternoptychidae unidentified 0.0 Synodontidae Synodus sp. 0.2 Trichiuridae Lepidopus caudatus 0.0 Macrouridae unidentified 0.0 Phycidae Phycis phycis 0.0 Caproidae Capros aper 93.2 Macroramphosidae Macraramphosus scolopax 3.0 Carangidae Trachurus picturatus 0.6 Total Sparidae 4.5# Pagellus acarne 0.4 Pagellus bogaraveo 0.7 Pagellus spp. 0.4 Pagrus pagrus 0.0 Sparidae unidentified 0.0 Scombridae Scomber japonicus 0.9 Pairs of fish lenses Otoliths unidentified Fish remains (1) Because the %0 is a nonadditive index (Cortes, 1997), when grouping fish items into higher taxonomic categories (i.e. Pisces, etc) the %0 value was recalculated considering the number of stomachs with the respective higher taxonomic category. This recalculation will affect both the IRI and %IRI values. (2) Including unidentified fish, pairs of lenses, otoliths, and fish remains. Note: Total values are given in bold indicated with #.
This work is part of a more comprehensive study supported by the European Union (Design optimization and implementation of demersal cruise survey in the Macaronesian Archipelagos (study contract DG XIV/94/034 and DG XIV/ 95/095). We thank Joao Goncalves, Ricardo Serrao Santos, Filipe Porteiro for help with identification of stomach contents, and Helena Krug for help with the identification of otoliths. Special thanks are due to the scientific staff and to the crew of the RV Arquipelago for working overtime at sea. We are also grateful to Malcolm J. Smale, Pedro Afonso, Joel Carlin, and Natacha Carvalho for reviewing the manuscript. Comments and suggestions of anonymous reviewers greatly improved the quality of the manuscript.
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Manuscript approved for publication 19 February 2003 by Scientific Editor.
Manuscript received 4 April 2003 at NMFS Scientific Publications Office. Fish. Bull. 101:590-602 (2003).
Maria P. Gros
Departamento de Oceanografia e Pescas
Universidade dos Acores
PT-9901-862 Horta, Portugal
E-mail address: email@example.com
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|Author:||Morato, Telmo; Sola, Encarnacion; Gros, Maria P.; Menezes, Gui|
|Date:||Jul 1, 2003|
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