ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on June 12, 2007
ICES Journal of Marine Science: Journal du Conseil 2007 64(5):1017-1027; doi:10.1093/icesjms/fsm078
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Feeding ecology and abundance of two sympatric skates, the shortfin sand skate Psammobatis normani McEachran, and the smallthorn sand skate P. rudis Günther (Chondrichthyes, Rajidae), in the southwest Atlantic
1 Museo del Mar, Colón 1114, B7600FXR, Mar del Plata, Argentina and Laboratorio de Ictiología, Universidad Nacional de Mar del Plata, Funes 3350, B7602AYL Mar del Plata, Argentina.
2 Laboratorio de Bentos, Instituto Nacional de Investigación y Desarrollo Pesquero, V. Ocampo N° 1, B7602HSA Mar del Plata, Argentina and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
Correspondence to E. Mabragaña: tel: +54 223 4513553; fax: +54 223 4519779; e-mail: acuarios{at}museodelmar.org
Mabragaña, E., and Giberto, D. A. 2007. Feeding ecology and abundance of two sympatric skates, the shortfin sand skate Psammobatis normani McEachran, and the smallthorn sand skate P. rudis Günther (Chondrichthyes, Rajidae), in the southwest Atlantic. – ICES Journal of Marine Science, 64: 1017–1027.The diet, feeding strategy, and abundance of Psammobatis normani and P. rudis in the southwest Atlantic was investigated to determine whether the species are segregated by habitat or dietary preference. The two coexist along the Argentine continental shelf, but there are differences in abundance. The most important prey for P. normani were crustaceans (mainly crabs and isopods) and, to a lesser extent, polychaetes, whereas P. rudis fed almost exclusively on crustaceans (mainly isopods, crabs, and gammarids), and fish and polychaetes contributed less to the diet. This suggests that P. normani and P. rudis are secondary consumers (trophic level <4). The two species fed on similar taxa, but in slightly different proportions according to region. However, an ANOSIM test failed to reveal significant differences in their diets. Circumstantial evidence of food competition is suggested, because the two species attain similar adult size and there are no notable morphological differences between them. Interspecific competition may be reduced by the use of distinct feeding behaviour and by the abundance of prey especially along shelf-break fronts. The use of standard ecological indices of similarity and multivariate techniques to calculate dietary overlap is evaluated.
Keywords: Argentine continental shelf, diet composition, dietary overlap, Psammobatis, skates
Received 22 September 2006; accepted 9 May 2007; advance access publication 12 June 2007.
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Introduction |
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Skates are significant predators in benthic and demersal communities, preying mostly on fish and invertebrates (McEachran and Musick, 1975; Ajayi, 1982; Ebert et al., 1991; Ellis et al., 1996; Orlov, 1998). Skate bycatch in the demersal fisheries of Argentina is considerable (Cedrola et al., 2005); indeed, most skates were discarded until the early 1990s. However, this situation has changed recently, commercial landings increasing from 300 t in 1991 to 14 856 t in 1998 (Cousseau et al., 2000). The generally low fecundity, slow growth, and late maturity typical of most skate species indicates that they are particularly sensitive to fishing pressure and overexploitation (Walker and Hislop, 1998), and fishing pressure could lead to changes in the structure and function of benthic and demersal communities (Stevens et al., 2000).
The skate fauna in Argentine waters comprises at least 23 species (Cousseau et al., 2000; Diaz de Astarloa and Mabragaña, 2004). Despite their local diversity, relatively few studies have been carried out on their feeding habits. The diet and feeding ecology of just three species, the beaked skate Dipturus chilensis, the sand skate Psammobatis extenta, and the Patagonian skate Bathyraja macloviana, were recently investigated (Lucifora et al., 2000; Kohen Alonso et al., 2001; Braccini and Perez, 2005; Mabragaña et al., 2005; Scenna et al., 2006).
The genus Psammobatis is common in South American waters (Menni, 1972; McEachran, 1983; De Carvalho and Figueiredo, 1994; Menni and Stehmann, 2000). It has eight species, seven of which are present in the southwest (SW) Atlantic. Among congeners, P. rudis and P. normani have the widest distributions, occurring in the SW Atlantic and SE Pacific, from 60 m to ca. 200 m (McEachran, 1983; Pequeño and Lamilla, 1993; Mabragaña and Cousseau, 2004). Published biological information for both is limited to their reproductive biology (Sanchez and Mabragaña, 2002; Mabragaña and Cousseau, 2004), length–weight relationships, and length frequencies (Cedrola et al., 2005). A qualitative description of their diet off southern Patagonia was made by Sanchez and Mabragaña (2002).
Both species are common off southern Patagonia, but they are found also over the northern Argentine continental shelf (ACS) (Sanchez and Mabragaña, 2002). These water masses are characterized by the presence of several marine fronts, which enhance primary and secondary production (see references in Acha et al., 2004). The shelf-break front is a permanent feature of the edge of the shelf; their inner boundary lies between the 90 m and the 100 m isobaths. There is also another frontal zone off southern Patagonia, around Islas Malvinas (Acha et al., 2004). The concentration of benthic and pelagic prey along frontal zones is important for several species of teleosts, seabirds, and marine mammals (Acha et al., 2004), but its importance to skates is unknown.
One of many mechanisms facilitating species coexistence is resource partitioning, whereby coexisting consumer species reduce their level of shared prey to avoid deleterious effects of competition (see references in Wilson and Richards, 2000). As P. rudis and P. normani attain similar adult size and inhabit the ACS (Mabragaña and Cousseau, 2004), the main goal of this work was to investigate possible mechanisms of their coexistence, using diet, feeding strategy, and overlap analyses to determine whether they partition either their habitat or type of diet.
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Material and methods |
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Data collection
Skates were collected from nine research cruises carried out by the National Institute for Fisheries Research and Development (INIDEP) in three regions of the SW Atlantic: northern (off Uruguay and the Argentine Province of Buenos Aires, 34–41°S), central (north Patagonia, 41–48°S), and southern (southern Patagonia, 48–55°S) (Figure 1). Each region was divided into shallow (<100 m) and deeper sites (>100 m), allowing for comparisons of sites by oceanographic and biological condition (Acha et al., 2004, and references therein). The research cruises were carried out between 1998 and 2001 and were designed for the assessment of demersal fish stocks, especially Argentine hake (Merluccius hubbsi) and hoki (Macruronus magellanicus). Skates (182 P. normani and 148 P. rudis) were captured using a bottom trawl (200 mm mesh in the wings and 120 mm in the codend, vertical height 4 m, horizontal opening 15 m). Tow duration was 30 min. Additional specimens were obtained from commercial trawlers. Total length (TL) and disc width (DW) of each skate were measured to the nearest millimetre (mm), and weight to the nearest gramme (g), and the sex of each animal was recorded. Stomachs were frozen and analysed ashore.
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Density analysis
Data obtained from two research cruises during 2001 were used to estimate densities of the two species. The total mass of each species caught in each trawl was recorded, and the density of each was calculated as Di = Ci/ai, where Di is the density (by weight), Ci the catch in t, and ai the swept area in square nautical miles (distance of trawling x distance between net wings) in fishing haul i.
Because of significant departures from normality and homogeneity of variances, a non-parametric analysis of variance (ANOVA) (Kruskal–Wallis test), followed by a Dunn's multiple comparisons test (Zar, 1984), was used to determine whether the densities of skate differed significantly among species, sites, or depths.
Diet
Prey items of each skate species were identified to the lowest taxon possible, counted, and weighed (wet) to the nearest 0.01 g. We recorded percentage frequency of occurrence (%F), percentage by weight (%W), and percentage by number (%N) of prey. We assessed prey importance using the alimentary index (IA), calculated for each prey category i as the product of %Fi and %Wi (Lauzanne, 1975 in Rosecchi and Nouaze, 1987), and expressed as a percentage, where
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Prey items were assigned to 12 prey categories to facilitate intra- and interspecific comparison of the diet. For ontogenetic comparisons, individuals of each species were divided into two size classes based on a calculated average size at 50% maturity for males and females, after Mabragaña and Cousseau (2004). To assess sample size sufficiency, randomized prey curves were generated using 100 resamplings; this technique plots the cumulative number of stomachs analysed against the cumulative number of prey taxa (or prey categories) encountered.
Trophic level (TR) was calculated to determine the position of both skates within the foodweb. Trophic level of each skate j (TRj) was calculated after Cortés (1999) as TRj = 1 + (
Pi x TRi), where TRi is the trophic level of each prey item and Pi the proportion of each prey item in the diet of skate j. Trophic level of prey items was obtained from Ebert and Bizarro(in press).
Feeding strategy
To obtain information on feeding strategies in terms of specialization (a narrow dietary niche width) and generalization (a broad dietary niche width), we used the graphic method proposed by Amundsen et al. (1996), which incorporated prey-specific biomass into Costello's (1990) analysis. This parameter is defined as the percentage a prey taxon constitutes of all items in only those predators in which the actual prey occurs, or in mathematical terms:
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Diet overlap
Schoener's diet overlap index (Schoener, 1970) was used to measure the diet overlap between species, sex, size classes, and areas. According to Wallace and Ramsey (1983), overlap values >0.6 should be considered biologically significant. Similarity in the composition of the diet between species and sites was determined by a non-parametric multivariate analysis and an analysis of similarities (ANOSIM) test (Clarke and Warwick, 2001). The %IA of each prey category was calculated for each skate species based on pooled data for each site (trawl). The ANOSIM test was used to search for differences in the diet between areas and species. This permutation test analyses differences between replicates within sites contrasted with differences between sites, computing an R-statistic under the null hypothesis "no differences between sites". R falls between –1 and 1, so R is 
0 if the null hypothesis is true and R = 1 if all replicates within sites are more similar to each other than are replicates from different sites. Classification (CLUSTER, group average sorting of the Bray–Curtis similarity measure based on %IA data), ordination (multidimensional scaling, MDS, on the above similarity matrices), and ANOSIM were performed using the PRIMER software (Clarke and Warwick, 2001).
Morphology of jaws
A sample of jaws (46 P. normani and 34 P. rudis) was dissected to describe the dentition and to assess whether they might be influencing differences in prey type ingested by the skates. A parametric ANOVA (Zar, 1984) was used to compare the number of rows of teeth on upper and lower jaws between species (both are considered to be fixed factors).
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Results |
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Abundance patterns
Psammobatis normani and P. rudis were found at similar depth, from 60 to 200 m, but with some differences in abundance (Figure 2 and Table 1). Densities of P. rudis were greater at southern sites than at northern sites at depths >100 m, whereas densities of P. normani were greater at northern sites <100 m and at southern sites >100 m (Table 1).
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Diet
All sample sizes except that for the central area for P. rudis were adequate for diet comparisons, because the cumulative curves reached an asymptote (Figures 3–5). Schoener's diet overlap index between males and females of both skate species were relatively high (>0.8), indicating a high level of similarity between diets, so diet composition data for both sexes were pooled for subsequent analyses.
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Psammobatis normani (n = 182) ranged from 241 to 580 mm TL. All contained food. Five major zoological groups, comprising 26 prey items, were found (Table 2). The most important prey groups, in terms of %IA, were crustaceans (85.04%) and polychaetes (14.89%). The former includes decapods and isopods (Serolidae) as main items. Other prey items occasionally found in the diet were fish, salps, and cephalopods. Diet composition between the two size classes was similar (Table 3). The Schoener index showed a high degree of dietary overlap between both categories (SI = 0.83). Only the %IA of serolid isopods differed between class I (3.42%) and class II (19.27%) (Table 3). Overall, trophic level of P. normani was 3.65 (northern 3.59, central 3.55, and southern 3.97).
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Psammobatis rudis (n = 148) ranged from 267 to 531 mm TL, and 93.2% contained food. Four major zoological groups, comprising 24 prey items, were found (Table 2). Crustaceans (96.44%) were the most important prey in terms of %IA, and included isopods, crabs, and amphipods as major items. Fish, polychaetes, and molluscs were occasionally included. Diet composition between the two size classes considered was slightly different. The Schoener index showed moderate diet overlap (SI = 0.57). Gammarids, crabs, and polychates were consumed mostly by class I, and isopods (Arcturidae and Cirolanidae) and fish preferably by class II (Table 3). The overall trophic level of P. rudis was 3.95 (northern 3.74 and southern 4.06).
Feeding strategies
The plots of feeding strategy for P. normani indicated a tendency for population specialization towards crustaceans and, to a lesser degree, polychaetes (Figure 6a). Crabs, worms, serolids, and amphipods made a large contribution to the diet and were consumed using a mixed feeding strategy, with varying degrees of specialization and generalization among individual skate (Figure 6b). In contrast, feeding strategy plots for P. rudis indicated a clear tendency to specialize on crustaceans (Figure 7a), preying on gammarids, isopods, crabs, and other crustaceans using a mixed feeding strategy at an individual level (Figure 7b).
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Interspecific comparisons and regional trends
Both skates fed on similar prey, but they appeared in slightly different proportions according to the region analysed (Table 3). This was reflected in the global test of ANOSIM (R = 0.098, p < 0.05), which indicated no significant difference between the diets of the two species. This trend was evident also in the ordination (Figure 8a) and classification (Figure 8b) analysis, in which only a few sampling sites were clustered together. In contrast, the Schoener index revealed no biologically significant overlap between species (SI = 0.39).
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Crabs were important prey of P. normani in northern (Libidoclea granaria and Leucippa pentagona) and central (Peltarium spinosulum and L. granaria) areas (Table 3), whereas in the south, they were replaced by small crustaceans such as serolids and gammarids. Polychaetes were in similar proportions in northern and southern regions. The ANOSIM test reflected these differences between northern and southern areas (R = 0.447, p < 0.001), and between central and southern areas (R = 0.631, p < 0.001). Differences between northern and central areas were not significant (R = –0.021, p > 0.05). These regional trends were reflected in the ordination analysis (Figure 9a). Finally, the Schoener index suggested a relatively limited overlap between northern and southern areas (SI = 0.4), northern and central areas (0.51), and especially central and southern areas (SI = 0.05).
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The diet of P. rudis was relatively consistent over the regions analysed (Table 3). In the northern area, crabs (L. granaria and Peltarium spinosulum) and gammarids were the most important prey, but they were less important in the southern region, where isopods were also one of the major items ingested (Table 3). The MDS plot (Figure 9b) and the ANOSIM test (R = 0.104, p > 0.05) reflected similar diets in northern and southern areas. In contrast, the Schoener index (SI = 0.49) suggested a low degree of overlap between areas. Low sample size in the central area prevented comparisons of that area with the other regions.
Dentition and morphology of jaws
Tooth morphology of both species was similar. Females and juveniles of both species have rounded cusp teeth, whereas mature males have pointed cusps. The ANOVA test (F = 102.45, p < 0.0001) indicated that the median number of teeth differed significantly between species, P. normani having more teeth than P. rudis (40.5 vs. 34; Tukey test, p < 0.05). Moreover, P. normani showed differences in the number of teeth in upper and lower jaws (39.4 vs. 41.5), whereas in P. rudis, both jaws had a similar number of teeth (33.5 vs. 34.5) (Tukey test, p < 0.05).
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Discussion |
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Psammobatis normani and P. rudis were found along the ACS from 60 to 200 m deep at similar relative densities except in the northern area deeper than 100 m, where P. normani was dominant. Although reliable data on the presence and relative densities in the central area were not available for our study, Cedrola et al. (2005) recorded larger catches of P. normani than P. rudis in a Patagonian red shrimp fishery in the San Jorge Gulf (in the central area, Figure 1), and relative densities of the first species were similar to those estimated for other areas in the present study. Therefore, both skates sympatrically inhabit most areas of the ACS, with some differences in abundance.
The most important prey items of P. normani were crustaceans (mainly crabs and isopods) and to a lesser extent polychaetes, whereas P. rudis fed almost exclusively on crustaceans (mainly isopods, crabs, and gammarids), with fish and polychaetes contributing less to the diet. Both skates are mainly benthophagous. The fish found in stomachs were mostly benthic and of low motility, and the occasional presence of planktonic organisms in the stomach contents of P. normani can be explained by the occasional near-bottom aggregations of those organisms (Colombo et al., 2003; Costello and Mianzan, 2003). Regional variation in the groups of crustaceans consumed was observed in both species. In the northern area, crabs were the main group eaten, whereas in the southern area, isopods and amphipods were the most important. Crabs and isopods are widely distributed over the shelf (Boschi et al., 1992), but the lack of quantitative data on their abundance precludes an assessment of prey selectivity or changes in the diet in response to prey availability by these two species of skate.
Generally, partial spatial segregation, differences in feeding behaviour, and good prey availability facilitate the coexistence of sympatric species (McEachran et al., 1976; Platell et al., 1998; Wetherbee and Cortés, 2004). Our results suggest that P. rudis and P. normani do not partition their habitat in the SW Atlantic, because both species coexist over the ACS. In terms of feeding behaviour, P. normani displayed a tendency to prefer crustaceans, and polychaetes to a lesser degree, whereas P. rudis took crustaceans almost exclusively. Both skate species displayed a mixed feeding strategy, with an intermediate situation between high between-phenotype and high within-phenotype contribution to niche width. This was reflected in the prey use over the ACS. For both species, the proportions of different prey differed more at the southern stations than at northern ones. The northern area corresponds to the inner boundary of the Argentine shelf-break front, a zone of high productivity, where high concentrations of prey are exploited by a large number of species (Acha et al., 2004). Therefore, greater availability of benthic prey in the northern area could reduce dietary competition between the two species, whereas in the southern area, coexistence could be achieved by the use of different prey proportions, so reducing competition.
McEachran et al. (1976) found that differences in the shape of the mouth and the number of tooth rows may be related to skate food habits, species with a less arched mouth and a greater number of tooth rows having a preference for infauna. An exhaustive description of P. rudis tooth morphology was given by Herman et al. (1995). They found sexual heterodonty in adults and ontogenetic heterodonty in males, as we found here for P. normani and P. rudis. Mature males and females of both species had similar diets in this study; so sexual heterodonty in these species is probably related to reproductive behaviour, as postulated by McEachran (1977). Moreover, although P. normani has more rows of teeth than P. rudis, both species prey on epibenthic and infaunal organisms, with no particular preference.
One way to understand the ecological role of skates in the ecosystem is to estimate their trophic level (TR). Recently, this parameter was calculated for 60 skate species, including several on the ACS. Values ranged from 3.48 to 4.22, and the values were generally correlated with the TL of predator (Ebert and Bizarro, in press). Earlier studies on the diet of skates over the ACS, based on quantitative analysis, revealed that larger species such as D. chilensis generally preyed on fish and squids (Lucifora et al., 2000; Kohen Alonso et al., 2001), occupying apex positions in the food chains (TR = 4.22). Small species have a mixed diet, based primarily on crustaceans and secondarily on polychaetes such as P. extenta (Braccini and Perez, 2005), with a TR of 3.85, or based mainly on polychaetes such as B. macloviana (Mabragaña et al., 2005; Scenna et al., 2006), with a lower TR (3.66). Values of TR estimated for P. normani and P. rudis were higher than expected considering their small size and their carcinophagous diet. On the other hand, although there were no clear differences in the diet of P. normani and P. rudis, values of TR were different (3.65 vs. 3.95). Differences are mainly attributable to the high TR value for the category "amphipods" (which includes amphipods and isopods), and because these values represent the average TR in the ACS. TR values are similar when calculated by area, and increased from northern to southern areas, possibly reflecting changes in trophic chains from temperate to colder water of Subantarctic origin.
Standard ecological indices of similarity have been used traditionally to calculate dietary overlap among elasmobranch species. More recently, other powerful analyses, including the use of multivariate analysis, have been used to analyse feeding ecology (Platell et al., 1998; Braccini and Perez, 2005; Mabragaña et al., 2005; Lucifora et al., 2006; Rinewalt et al.,in press). Here, we present results from the use of both techniques in the analyses, and there are notable differences in results and interpretation. Do the diets of P. rudis and P. normani overlap? According to the Schoener index, the degree of overlap is less than 0.6, suggesting no biologically significant difference. However, according to the ANOSIM test and ordination techniques, diets are similar. In the same way, geographical differences in diet observed in P. rudis using the Schoener index were not observed using ANOSIM or the ordination approach. Multivariate techniques search for differences between groups of samples, comparing every pair of samples (hence providing more detail), and the results are supported statistically. Therefore, they give a better picture of prey use. On the contrary, traditional indices such as the Schoener index compare just two groups (species, areas, etc.) and show the degree of overlap between the groups considered. Indeed, the "0.6 threshold overlap value" is arbitrary and does not have any statistical support. To improve the accuracy and precision of diet comparisons, the use of statistically supported tools instead of classical methods is recommended.
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Acknowledgements |
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We thank two anonymous referees for valued comments on the submitted version of the manuscript. This is INIDEP contribution 1445.
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References |
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