© 2006 International Council for the Exploration of the Sea
Trophic ecology of the Patagonian skate, Bathyraja macloviana, on the Argentine continental shelf
a Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), and Universidad Nacional de Mar del Plata (UNMdP), Facultad de Ciencias Exactas y Naturales, Departamento de Ciencias Marinas Funes 3350, Mar del Plata B7602AYL, Argentina
b UNMdP, Departamento de Ciencias Marinas Argentina
c CONICET, UNMdP, Departamento de Ciencias Marinas Argentina
d Instituto Nacional de Investigación y Desarrollo Pesquero Paseo Victoria Ocampo No 1, Mar del Plata B7602HSA, Argentina
*Correspondence to L. B. Scenna: tel: +54 223 4751107; fax: +54 223 4753150. e-mail: lscenna{at}mdp.edu.ar.
The diet, feeding strategy, and dentition of the Patagonian skate, Bathyraja macloviana, on the northern continental shelf of Argentina were studied from specimens collected during research cruises in September and October 2001. Of a total of 81 stomachs examined, only 3.7% were empty. Cumulative prey curves showed that sample sizes were adequate to describe the main prey items of the diet. Quantitative analysis, a graphical method, and trophic niche breadth indicated the species to be a specialized feeder. The most important prey items were polychaetes, followed by gammarid amphipods, isopods, and crabs. Cumaceans, ophiuroids, and hydrozoans were likely incidentally consumed by mature females. Sexual dimorphism in dentition was observed; mature males had longer and sharper tooth cusps than females or immature males. However, there was a high degree of dietary overlap between mature males and mature females, indicating that dental sexual dimorphism in the species is more important in reproductive behaviour than in differential prey consumption.
Keywords: Argentine waters, Bathyraja macloviana, dentition, diet, feeding strategy, Rajidae, trophic niche breadth
Received 31 May 2005; accepted 2 February 2006.
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Introduction |
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 Top Introduction Material and methodsResultsDiscussionReferences |
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Skate, family Rajidae, constitute the most diverse family of cartilaginous fish (Nelson, 1994; McEachran and Dunn, 1998). Bathyraja (softnose skate) is the most speciose genus (Stehmann, 1986) of the family, and has a particularly high diversity of species in the northern Pacific and southwestern Atlantic (McEachran and Miyake, 1990). Eight species of Bathyraja (Bathyraja macloviana, B. brachyurops, B. albomaculata, B. magellanica, B. scaphiops, B. multispinis, B. griseocauda, and B. cousseauae) occur on the Argentine continental shelf (Cousseau et al., 2000; Díaz de Astarloa and Mabragaña, 2004). Of these, the Patagonian skate B. macloviana (Norman, 1937) is probably the most common in the region, and it also inhabits the Uruguayan and Chilean waters (Pequeño and Lamilla, 1993).
Although skate are increasingly targeted in fisheries conducted on the Argentine continental shelf (Massa and Hozbor, 2003), their ecology is still poorly known. Most reports on Bathyraja in the region deal with taxonomy and distribution (Stehmann, 1978; Bellisio et al., 1979; Menni and Gosztonyi, 1982; Menni and López, 1984; Cousseau et al., 2000; Menni and Stehmann, 2000; Díaz de Astarloa and Mabragaña, 2004). Recently, the feeding habits of six species of Bathyraja from the southern waters of Argentina were described, revealing that polychaetes and crustaceans were the most important prey items in the diet of Patagonian skate (Sánchez and Mabragaña, 2002).
Differences in feeding habits among skate appear to be correlated with differences in size and morphology of the feeding apparatus, especially in the morphology of the dentition and strength of jaws (Smale and Cowley, 1992). Orlov (1998) found that larger species of Bathyraja in the northern Pacific (B. aleutica, B. maculata, B. parmifera, and B. matsubarai) preyed on large crustaceans, cephalopods, and fish, while smaller species (B. interrupta, B. minispinosa, and B. violacea) fed on small benthic organisms. The same trend has been observed in three species (B. albomaculata, B. brachyurops, and B. griseocauda) from the southwestern Atlantic (Brickle et al., 2003). Moreover, sexual differences in the diet and dietary changes with sexual maturation were reported (Orlov, 1998). Adult dentition of B. griseocauda in the southeastern Pacific has been described by Sáez and Lamilla (2004). However, none of these studies analysed the dentition together with diet.
In the present study, the trophic spectrum and feeding strategy of B. macloviana on the northern Argentine continental shelf are analysed. In addition, dentition is described by sex and maturity stage, and assessed in relation to feeding.
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Material and methods |
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Skate for analysis were collected from two research cruises carried out by the RV "Dr. E. Holmberg" of the Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP, Mar del Plata, Argentina) during September and October 2001. The sampling was randomly stratified and designed for assessment of hake (Merluccius hubbsi), so a bottom trawl of 200-mm mesh in the wings and 20 mm in the codend was employed. The study area was located between 38°S and 44°30'S and from 50-m depth to the edge of the continental shelf, excluding waters within the San Matías Gulf (Figure 1).
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The sex of all specimens of B. macloviana was determined, and total length (TL) was measured to the nearest millimetre. Maturity stage was determined by examination of the reproductive organs (Mabragaña et al., 2002). Stomachs were removed, labelled, and preserved in 4% formalin. In the laboratory, prey were separated and identified to the lowest possible taxonomic level, using published keys and catalogues (Bastida and Torti, 1969, 1973; Escofet, 1973; Soares Moreira, 1973; Boschi et al., 1992), and local reference collections. Prey items were counted and wet weight was measured to the nearest 0.01 g. In each stomach, remains of colonial species were counted as a single individual.
The jaws of immature and mature specimens of both sexes were dissected, thoroughly cleaned, and dried to study the dentition. Tooth rows were counted in upper and lower jaws. In addition, tooth arrangement and external tooth morphology were observed, described, and photographed under a stereoscopic magnifying glass, using a digital camera.
Diet composition was analysed using the percentage frequency of occurrence (%FO), percentage by number (%N), percentage by wet weight (%W), and the Index of Relative Importance expressed on a percentage basis (%IRI; Cortés, 1997). These indices were calculated separately for the lowest taxon identified, and for the prey categories in which prey items were grouped.
Cumulative prey curves were used to determine whether an adequate number of stomachs had been examined to describe the diet precisely (Ferry and Caillet, 1996). The order in which stomachs were analysed was randomized 100 times to minimize bias resulting from sampling order. The mean number of new prey categories found in the stomachs (with standard deviation) was plotted against the total number of stomachs analysed. The asymptote of the curve indicated the minimum sample size required to adequately describe the diet (Ferry and Caillet, 1996). Cumulative prey curves were constructed using the categories in which prey items were grouped.
The feeding strategy of Patagonian skate in terms of specialization and generalization was studied by plotting prey-specific abundance (Pi) against %FO (Amundsen et al., 1996). Pi was calculated as the number of prey i divided by the total number of prey in the stomachs that contained prey i, expressed as a percentage. A single or a few points located at the upper right of the diagram would indicate a specialized diet (i.e. a narrow niche breadth), but if all prey points were located along or below the diagonal from the upper left to the lower right of the plot, the trophic niche breadth would be broad. This graphical representation was also used to analyse prey importance (dominant or rare; Amundsen et al., 1996). In addition, Levins' standardized niche breadth index was estimated using %IRI, and the same prey categories considered for the plot of Pi against %FO. This index ranges from 0 (a highly specific diet) to 1 (the broadest diet; Krebs, 1989).
Fish were grouped by sex and maturity stage (immature and mature). Contingency table (log-likelihood ratio) analysis was used to evaluate dietary differences related to sex, considering the occurrences of the main prey items (Zar, 1984; Cortés, 1997). Dietary overlap between groups was calculated by means of Horn's Index (Krebs, 1989), and the contribution of each prey category to the diet was expressed as %IRI. This index varies between 0 (no categories in common) and 1 (identical proportional composition).
The null hypothesis of no difference in mean number of tooth rows between immature fish, mature males, and mature females was assessed with one-way ANOVA for both upper and lower jaws (Zar, 1984).
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Results |
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In all, 78 bottom trawls were carried out in the study area. However, 29 of them were between 42°20'S and 44°30'S, in depths of 50–100 m, where no B. macloviana were caught (Figure 1). Of a total of 81 stomachs examined, only three were empty (3.7%), and 59% of them had digeneans, mainly in the pyloric portion. In all, 38 mature females ranging in size from 555 mm to 660 mm TL, 25 mature males of TL 544–636 mm, and 15 immature fish (10 females and five males) with a TL range of 329–590 mm were analysed (Figure 2).
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The cumulative prey curve showed a well-defined asymptote (Figure 3), indicating that the total sample size (n = 78) was adequate to describe the diet of the Patagonian skate using the five prey categories listed in Table 1. A total of 952 prey grouped in 24 taxa were identified in the stomach contents (Table 1). %IRI values for prey categories showed that the diet was mainly polychaetes, followed by gammarid amphipods, and isopods. Crabs, cumaceans, ophiuroids, and hydrozoans were not important in the diet (<1%). Unidentified polychaetes had the highest %IRI, but among those taxonomically identified, Travisia sp. was the most important in terms of %W, %N, %FO, and %IRI. The gammarid amphipod Ampelisca sp. was the secondmost important, numerous, and frequent prey item in the diet. It was followed by the isopod Cirolana sp., which had a higher %W but lower %N, %FO, and %IRI values than those of Ampelisca sp. The other prey items were less important in the diet (Table 1).
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B. macloviana fed mainly on polychaetes, as indicated by the %IRI being located at the upper right of the Pi–%FO plot (Figure 4; Pi = 68%, %FO = 100). Gammarid amphipods and isopods were second in dominance as prey items, crabs, and other invertebrates being rare, all with Pi < 42% and %FO < 57 (Figure 4). Levins' standardized value was 0.07.
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Sex differences in diet were examined among mature skate. The cumulative prey curve for mature females attained a well-defined asymptote for four prey categories (polychaetes, amphipods, isopods, and other invertebrates; Figure 3). The slope of the curve for mature males initially increases rapidly, then slows as the asymptote is approached (Figure 3). Dietary comparison between immature males and females was not possible owing to the small number caught. However, the same trend in the variation of %FO, %N, %W, and %IRI was observed in both mature males and females. Polychaetes were the main prey item, followed by gammarid amphipods and isopods (Figure 5). One crab was found in the stomach contents of a mature male. Just 10 crabs (in six stomachs), seven cumaceans (in one stomach), one ophiuroid (in one stomach), and hydrozoans (in three stomachs) were recorded in the diet of mature females. The proportions of food categories were not significantly different between mature males and mature females (G = 4.65; d.f. = 3; p = 0.1992). The high value of Horn's Index (0.98), using the same prey categories, revealed a large degree of dietary overlap between mature males and females.
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B. macloviana had small, monocuspid teeth. Mature males had teeth with long, sharp cusps curved towards the inner side of the mouth, more markedly at the symphysial region in the upper jaw, and arranged in spaced transverse rows (Figure 6). In females and immature males, teeth were rounded, also pointed at the symphysial region and inner side of the mouth (mainly in the upper jaw), but the cusps were lower, thicker, and blunter than those of mature males. Tooth arrangement was in transverse rows in the upper jaw, and in a close-set and loose quincunx pattern in the lower jaw (Figure 6).
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The mean number of tooth rows was higher in the lower jaw than in the upper jaw of skate of both sexes and maturity stages, but it was less variable in the upper jaw of mature males and females (Table 2). No significant differences in the number of tooth rows among the three groups were found (upper jaw: F2,62 = 1.506, p = 0.299; lower jaw: F2,62 = 0.710, p = 0.495).
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Discussion |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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Bathyraja macloviana is widely distributed over the whole study area, but none were caught in shallow water between 42°20'S and 44°30'S. Cousseau et al. (2000) recorded a similar distribution on the basis of data obtained from 12 research cruises between 1993 and 1999. The research surveys were not targeted at the assessment of elasmobranchs, so the sampling designs and sample areas were not based on the known distribution and abundance patterns of skate species (which were taken only as bycatch).
Trawl samples avoided potential sampling bias towards fish with empty stomachs caused by the use of bait (Morato et al., 2003). As a result, the low percentage of empty stomachs found in the present study suggests that B. macloviana eats frequently and/or that gastric evacuation is slow relative to its feeding frequency, as proposed for the bonnethead shark (Cortés et al., 1996). Low frequencies of empty stomachs in other skate species have also been found (Ebert et al., 1991; Smale and Cowley, 1992; Ellis et al., 1996; Paesch, 2000; Koen Alonso et al., 2001; Muto et al., 2001).
The graphical method of Amundsen et al. (1996) and the niche breadth index indicated that the Patagonian skate over the northern Argentine continental shelf is a specialized feeder. All skate fed on polychaetes, the dominant prey item, although small proportions of other benthic invertebrates (gammarid amphipods, isopods, and crabs) were found in the diet of some. Other prey items (cumaceans, ophiuroids, and hydrozoans) were infrequent in the diet of mature females, meaning that they were likely consumed incidentally. The diets of some skate species vary substantially with location and season (Ajayi, 1982; Muto et al., 2001; Morato et al., 2003). However, according to Sánchez and Mabragaña (2002), B. macloviana also preys on polychaetes over the southern Patagonian shelf (48–55°S) during March and April, suggesting that the Patagonian skate is a specialized feeder, preferring polychaetes, with little regional or seasonal variation in the diet.
The preferred polychaete prey was Travisia sp. (family Opheliidae). Opheliids are errant burrowers, commonly found in sand and mud (Fauchald, 1977; Ruppert and Barnes, 1991), suggesting that B. macloviana may dig into the sediment in search of food.
In the present study, the maximum TL recorded (males 636 mm, females 660 mm) was smaller than reported by Cousseau et al. (2000; males 657 mm, females 675 mm). Of the eight species of Bathyraja found in Argentine waters, the smallest maximum TL was observed for the Patagonian skate (Cousseau et al., 2000; Díaz de Astarloa and Mabragaña, 2004). Our results agree with those of other skate communities from different areas of the world, where smaller skate tend to be benthos-eating (worms, gammarid amphipods, isopods, etc.) and larger skate feed on larger crustaceans, cephalopods, and fish (Ebert et al., 1991; Smale and Cowley, 1992; Orlov, 1998; Lucifora et al., 2000; Brickle et al., 2003).
Ellis et al. (1996) proposed that differences in feeding habits would be controlled, inter alia, by the spatial distribution of each predator species in relation to potential prey items and other predators. The lack of detailed quantitative information on the distribution and availability of potential benthic prey on the northern Argentine shelf prevents an assessment of prey selectivity by B. macloviana in our study. According to other studies of the skate fauna of the southwestern Atlantic shelf, B. albomaculata is a highly specific gammarid amphipod and polychaete feeder (Brickle et al., 2003), whereas other Bathyraja (B. brachyurops, B. griseocauda, B. magellanica, and B. multispinis) and other skate species (Dipturus chilensis, Amblyraja doellojuradoi) prey predominantly on fish, cephalopods, and crustaceans (Garcia de la Rosa, 1998; Lucifora et al., 2000; Koen Alonso et al., 2001; Sánchez and Mabragaña, 2002; Brickle et al., 2003). Some of these species (B. albomaculata, B. brachyurops, and D. chilensis) are sympatric with B. macloviana in northern and southern Argentine waters (Cousseau et al., 2000), so it is possible that B. macloviana's specialization on polychaetes reduces potential interspecific competition pressure if food resources are limiting.
Sexual differences in the food composition of species of Bathyraja from the northern Pacific have been attributed to the existence of sexual size dimorphism (Orlov, 1998). Our results show that mature male and female B. macloviana have a similar diet composition for similar size ranges. In addition, dietary differences relative to maturity status rather than size have been found in some skate species (Orlov, 1998; Skjaeraasen and Bergstad, 2000; Koen Alonso et al., 2001). However, the small number of juveniles collected in our study made it impossible to evaluate this factor.
The small teeth of B. macloviana are suitable for feeding on polychaetes and soft-shelled crustaceans, which constituted the main prey items. We found sexual dental dimorphism in mature Patagonian skate and a different dentition in males, depending on maturity stage. The homodont and heterodont condition of the genus Bathyraja remains uncertain (Sáez and Lamilla, 2004). Our results on dental morphology were based on a qualitative analysis, not on a quantitative analysis as carried out for B. griseocauda in the southeastern Pacific (Sáez and Lamilla, 2004). Sexual heterodonty in mature fish, and change in the dentition of males into sharp conical cusps at sexual maturity is observed in other skate species (McEachran, 1977; Braccini and Chiaramonte, 2002). Sexual dimorphism in the dentition of skate was originally thought to reduce intraspecific competition for food between sexes (Feduccia and Slaughter, 1974). However, McEachran (1977) refuted this hypothesis because males and females take similar prey, and concluded that males used their jaws during copulation. Change in tooth morphology and the development of alar thorns allow the males to grip the females and to provide leverage for clasper insertion (Tricas et al., 1998; Kajiura et al., 2000). In addition to this, sexually dimorphic skin morphology has been observed in batoids such as the Atlantic stingray (Dasyatis sabina), females having a thicker dermis than males of comparable size, presumably providing more protection during copulation (Kajiura et al., 2000). Mature male and mature female Patagonian skate have similar diets, suggesting that sexual dental dimorphism in this species is more important in reproductive behaviour than in differential prey consumption. Besides, if tooth dimorphism is related to niche subdivision, then it should appear earlier than just prior to sexual maturity (McEachran, 1977).
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Acknowledgements |
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We thank the Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP) for permitting us to take part in research cruises in order to collect specimens and for allowing us to sample skate at their facilities. We also thank C. Bremec (INIDEP) and G. Genzano (Universidad Nacional de Mar del Plata) for their help in identifying polychaetes and hydrozoans, respectively. L. Lucifora, A. Baladrón, T. Munroe, and two anonymous reviewers provided helpful comments that greatly improved the manuscript. The work was supported by the Universidad Nacional de Mar del Plata, Argentina (project EXA 252/03).
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  E. Mabragana and D. A. Giberto Feeding ecology and abundance of two sympatric skates, the shortfin sand skate Psammobatis normani McEachran, and the smallthorn sand skate P. rudis Gunther (Chondrichthyes, Rajidae), in the southwest Atlantic ICES J. Mar. Sci., July 1, 2007; 64(5): 1017 - 1027. [Abstract] [Full Text] [PDF]
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