The shortspine or greeneye spurdog (Squalus mitsukurii Jordan and Snyder 1903) is a bathyal and benthopelagic elasmobranch species (Musick et al., 2004). It is found in cold-temperate to tropical seas of the continental and insular shelves, upper slopes, submarine ridges and seamounts. It is observed primarily between 100 and 700 m, though it has been recorded as deep as 954 m and as shallow as 4 m depth (Carpenter, 2003; Compagno et al., 2005; Cavanagh et al., 2007). The geographic distribution is extensive and patchy and includes the northwest, southwest and central Pacific Ocean and the south Atlantic Ocean (Compagno, 1984, 2005). However, the distributional status of S. mitsukurii may change when thorough systematic studies are carried out on a regional or global basis, as there are actually taxonomic problems related to S. mitsukurii in the Indo-Pacific and Atlantic populations. However, the review of these taxonomical issues for S. mitsukurii is taking place in the present (Stevens, 2004; Kyne and Simpfendorfer, 2007).
S. mitsukurii exhibit yolk-sac viviparity, with four to nine pups per litter, most births occurring in the autumn3 off the east coast of South Africa. The gestation period could take up to two years and sexual segregation of females would also occur in this species (Compagno, 1984). Within our study area, Lucifora et al. (1999) provided maturity estimations for around the Rio de la Plata River mouth (36° 05' S to 36° 39' S and 53° 23' W to 53° 48' W), of 51–55 cm and 52–60 cm total length for males and females, respectively. The species feeds mainly on bony fishes but also on cephalopods and crustaceans (Wilson and Seki, 1994; Compagno et al., 2005).
In the southwest Atlantic, S. mitsukurii occurs off the Rio de la Plata and its oceanic front (Meneses and Paesch, 2003), moving to the southern Brazilian shelf in winter, where it is an important component of the local commercial fisheries (Vooren, 1997). Off Uruguay, the species is incidentally caught by the commercial offshore bottom trawl fishery (Paesch and Domingo, 2003), landed by vessels targeting the Argentine hake (Merluccius hubbsi) and piked dogfish (Squalus acanthias). However, the quantification of these landings is very difficult because they are not reported in the fishing statistics (Paesch, pers. obs.).
The lack of information on landings for this species in Uruguay is a matter of concern. For the period 1995–1998, the RV Aldebarán (from the Dirección Nacional de Recursos Acuáticos, Uruguay) carried out several research cruises in the Argentinean-Uruguayan Common Fishing Zone and collected specimens of S. mitsukurii, but the data gathered had not been analysed. Although almost one decade has passed since collection of the samples, we believe that the analysis of this information would make a valuable contribution to the understanding the population of this species. Dramatic declines of the catches of S. mitsukurii have been reported in other areas, suggesting extreme vulnerability (Wilson and Seki, 1994; Graham et al., 2001). However, in spite of the fact that Kyne and Simpfendorfer (2007) consider that S. mitsukurii is one of the Squalus species with more considerable biological data available, the conservation status of the species is considered as “data deficient” by the IUCN Red List of Threatened Species (Cavanagh et al., 2007). This fact reinforces the need to analyse and present available data. The management of shark species requires a good knowledge of spatial distribution, population structure and reproductive parameters, to support management measures (Mollet et al., 2000). In this way, the aim of this work is to analyze the spatial size structure, preliminary information on the reproductive parameters and abundance of S. mitsukurii, during summer, autumn and spring along the Uruguayan continental shelf of the south-western Atlantic Ocean for the period 1995–1998.
Materials and Methods
Samples of S. mitsukurii were obtained during five bottom trawl research cruises carried out in early autumn 1995, late autumn 1995, spring 1995, and early autumn 1996 and 1998 on board of the RV Aldebarán. These surveys were designed for the assessment of demersal fisheries targeting the Argentine hake (Merluccius hubbsi) resources in the Argentinean-Uruguayan Common Fishing Zone (ZCPAU, 34º 30'–37º 00' S, between 50 and 250 m) (Fig. 1, Table 1).
At each sampling location, a 30 min tow was conducted at a towing speed of approximately 3 knots during daylight. A high-opening “Engel” type net with an 80 mm (stretched mesh) codend was used. Trawl stations were selected using a stratified random sampling design, which was defined by depth and latitude (Ehrhardt et al., 1977).
Distribution and abundance analysis
Fresh specimens of S. mitsukurii were sampled on board immediately after each trawling station. The specimens were sexed and measured to total length (TL) to the nearest cm sensu Compagno (1984), and the relative frequency of TL (pooled samples) by sex was calculated. For detecting differences in the length distributions by sex and season a Kolmogorov-Smirnov test was performed. For comparing total length distributions by sex among seasons, a Kruskal-Wallis H-test (given by “Hc”) was used. Post-hoc Mann-Whitney U-test Bonferroni corrected was performed when differences among seasons were detected (Sokal and Rohlf, 1998). The non-parametric correlation Spearman coefficient was used to analyse the relationships between size and depth (Sokal and Rohlf, 1998).
For plotting the spatial distribution and abundance (density, expressed as individuals per squared nautical miles) of females/males and immature/mature sharks by sex, density was calculated as C/A where, C = number of individuals captured per haul, and A = swept area (= velocity×time×horizontal opening/1852, km2). Horizontal opening was estimated trough net sounders. Analysis of Variance (ANOVA) (Sokal and Rohlf, 1998) was used to compare the density of immature males and females and mature males and females among seasons respectively. In these cases, data were transformed using ln (x+1). Normality and homogeneity were tested with Shapiro-Wilk test and Levene’s test. Multiple comparison Tukey test was performed when means differed significantly among seasons. In all cases a significant level of P<0.05 was used.
Reproductive parameters analysis
The proportion of males:females (sex ratio) and immature:mature sharks by trawl station was analysed using a chi-square χ2-test (Sokal and Rohlf, 1998). A random sub-sample of males and females from all seasons was collected for analysis of sexual development and reproduction. For males, clasper length (to the nearest cm below the actual clasper length) was measured from the point of insertion to the distal end, sensu Compagno (1984). As no data on rigidity of the clasper to assess calcification were available, then TL50 (size at which 50% of the specimens were mature) in males was inferred by analyzing the clasper size and development, by plotting clasper length against total length. The logistic model (presented below for the females) was fitted to the TL clasper length data. The inflection point of the logistic curve was calculated by the ratio of the equation parameters -a/b. Females were considered mature when large, yellow oocytes were present in the ovary and/or embryos were present in oviducts, following the methodology by Peres and Vooren (1991) for lecitotrophic viviparous elasmobranchs. Presence of yolk in the oviduct was recorded and assumed as an ovulation sign. Length at 50% maturity (TL50) was calculated by a logistic model fitted to the maturity data as follows:
Y = 1/(1+e-(a+bX))
where Y is the proportion of mature individuals, X is the TL (by 2.0 cm classes), and TL at 50% maturity is given by -a/b (Mollet et al., 2000). Similarly, for females, TL at 50% maternity (MTL50) was inferred by calculating the proportion of females in maternal condition (gravid) by TL class and fitting the logistic model (Restrepo and Watson, 1991).
Data collected on litters included number of pups per female in each oviduct, sex and TL (cm) of the embryos. The sex ratio of embryos was calculated for spring 1995 and early autumn 1998, as embryo sex was only recorded in that cruises. Differences from the expected 1:1 were analysed using χ2-test (Sokal and Rohlf, 1998). However, data on the embryos sex was only recorded in spring 1995 and autumn 1998. Ovarian (number of vitellogenic follicles in the ovaries, OF) and uterine fecundity (number of macroscopically visible embryos, UF) were assessed and compared among cruises by Kruskal-Wallis H-test. The relationship between both variables and maternal total length (MTL) was also assessed by linear regression. The time of parturition was inferred by analyzing the TL frequency distribution of the embryos, and an ANOVA test was used to compare the mean embryo TL among season (Sokal and Rohlf, 1998).
Population structure and seasonal distribution
Total lengths ranged from 24–82 cm for females (n = 1 124) and from 25–79 cm for males (n = 1 893) (Fig. 2). Significant differences in the length-frequency distributions between sexes were found (p<0.05) (Table 1). For males and females, the length composition varied significantly among seasons (Hc = 92.40 for males and Hc = 84.17 for females). Post-hoc pair-wise comparison for males were not significant (p>0.05) between early autumn, and spring 1995; between late autumn 1995 and early autumn 1996 and 1998 and between early autumn 1996–1998 (Table 2). Post-hoc pair-wise comparison for females were not significant (p>0.05) between late autumn 1995-early autumn 1998 and spring 1995-early autumn 1996 (Table 2). A positive and significant relationship (p<0.05) were found between depth and TL, except for autumn 1998 (Table 1).
Mature males predominated in all seasons throughout the study area (Fig. 3b, d, f, h, j), whereas the highest densities of immature males were found in spring 1995 were recorded in two hauls at depths of 136 and 70 m. Immature females predominated in all seasons (Fig. 3a, c, e, g, i), except for late autumn 1995 when mature females were dominant (Fig. 3c).
Density distributions for all the seasons were not normal (P<0.05) while homogeneity was found for all cruises. Significant differences in density among seasons were recorded for immature and mature females and mature males. Non significant differences (P>0.05) between seasons were found for immature males (Table 3). Significant differences with regard to density were detected between immature females and mature males (p<0.05) for late autumn 1995 and early autumn 1996 respectively being the density of mature males lower than the density of immature females. The opposite pattern was observed in early autumn 1996. Density of mature females significantly varied (p<0.05) for the pair early autumn 1995 and late autumn 1995–early autumn 1996 and for the pair late autumn 1995 and early autumn 1998, with the highest density values recorded in the latter (Tables 3 and 4).
Males. Males collected for reproductive analysis ranged from 25.0 to 75.0 cm TL (n = 1 181, Table 1). The clasper length was highly variable throughout the size range, but clasper growth became faster as the sharks approached maturity, which corresponded to the range 40.0–55.0 cm TL. Total length at 50% maturity was inferred from the clasper length-TL relationship by calculating the point of inflection of the logistic curve, which was located at 43.1 cm of TL (r = 0.913, n = 1 181, Fig. 4a). From ~60.0 cm TL onwards, claspers grew slower in relation to TL, varying from 5.0 to 8.0 cm of length. This TL range consisted of adult males with fully developed claspers.
Females. Females collected for reproductive analysis ranged from 24.0 to 82.0 cm TL (n = 862, Table 5). The smallest mature female was 48.0 cm TL. The largest immature female was 51.0 cm TL, presenting no sign of sexual activity or development. The smallest gravid female was 49.0 cm of TL and bore two embryos. The estimated TL50 was 51.9 cm (r = 0.94, n = 32, Fig. 4b). Size at 50% maternity was estimated at 55.9 cm (r = 0.97, n = 32, Fig. 4b) and the percentage of gravid females varied from 21.4% in spring 1995 to 49.8% in late autumn 1995.
Fecundity and observations on the reproductive seasonality
The Ovarian Fecundity (OF) was positively correlated with the MTL and so was the Uterine Fecundity (UF) (r2 = 0.37, P<0.05 and r2 = 0.38; P<0.05, respectively, sample sizes in Table 5). The predictive regressions for these relationships are: OF = -3.89+0.13MTL and UF = -3.35+0.12MTL (Fig. 5a, b). Ovarian fecundity varied significantly among seasons (Hc = 15.84, P<0.05) from one (early autumn 1995) to 15 (late autumn 1995). Uterine fecundity varied from one (early autumn 1995) to 10 (late autumn 1995) being significantly different among seasons (Hc = 15.47, P<0.05).
In the spring of 1995, a total of 36 mature females were observed, with two females possessing four and five recently ovulated and fertilized ova in the oviduct. In the early autumn 1995, recently ovulated and fertilized ova were also observed in three females from a total of 65 mature females, in numbers of three, three and four per female (Table 5).
Embryo TL varied from 0.5 cm (late autumn 1995) to 22.0 cm (early autumn 1995 and early autumn 1996, Table 5). Embryo TL varied significantly among seasons (F4,358 = 22.88, P<0.05) attaining the highest values in early autumn 1996 and 1998 (Fig. 5c). The highest relative frequency of 22.0 cm TL was recorded in early autumn 1996. Embryo TL frequency distributions by seasons are showed in Fig. 6. Sex ratio showed no significant difference from the expected 1:1 (χ2 = 2.8, d.f = 1, P>0.05; Table 5).
Vooren (1997) considered Squalus mitsukurii as a winter migrant, reproducing in Uruguayan and Argentine waters in the summer, and migrating in the winter back to the continental shelf of southern Brazil. As our samples were obtained in autumn and spring, predominance of adults was expected. Our observations in fact showed that male S. mitsukurii adults dominated during most sampling periods, while for females, juveniles were more common. However, there was no relationship between fish size and depth for both sexes. Segregation by size and sex is commonly observed among Squalus species, though the population structure may vary by species and location. Litvinov (1990) observed that S. mitsukurii on the Nazca and Sala y Gomez seamounts was in the form of two schools consisting of individuals of similar size and sex. The same author noted habitat segregation by sex for this species. Comparison of different seamounts in the southeastern Pacific Ocean revealed significant differences in the size distribution for both sexes. Other Squalus species, such as S. megalops show complex population structures, with segregation by sex and size (with small females and males segregated from large females). Female S. megalops exhibited segregation by breeding condition, as large females in the first year of pregnancy were separated from those in the second year (Braccini et al., 2006a). The same may occur with S. mitsukurii, the reason why mostly immature females were recorded in our samples. Sion et al. (2003) noted significant differences between length-frequency distributions for males and females S. blainvillei with the sex ratio being 1:1 in both analyzed periods (September–October 1999 and April 2000). Graham (2005) recorded heavily dissimilar sex ratios for S. megalops. For S. mitsukurii Fischer et al. (2006) noted significant deviation towards females and Litvinov (1990) also found a sex ratio different from 1:1. However, Sion et al. (2003) recorded sex ratios of 1:1 for S. blainvillei.
Wilson and Seki (1994) noted that for January 1985–November 1988, S. mitsukurii was the most abundant fish species captured as by-catch in the Southeast Hancock Seamount (Pacific Ocean). However, the dramatic decline in the catch of S. mitsukurii during that period could indicate the sensitivity of the species to overfishing. The same authors argued that the limited habitat area could be another risk of overexploitation for the seamount populations of S. mitsukurii. Fischer et al. (2006) raised the question of the selectivity of some gears, as traps and longlines used in their survey, which are also typical of other Brazilian fisheries, as responsible of the depletion of juvenile S. mitsukurii, recommending gear restrictions to avoid young fishing mortality. Graham (2005) noted that in spite of the fact that stocks of some Squalus species inhabit large areas seemingly subject to light exploitation, they were already greatly depleted on the main trawling ground. The assessment of elasmobranch populations is often limited by the lack of biological information (Cortés, 1998). This fact is especially valid for non-targeted species (Braccini et al., 2006b, c) such as S. mitsukurii. Therefore, it is expected that the reproductive parameters calculated in this study may aid in the adequate management of the species, namely with special regard to the presence of a large number of juveniles in the samples, which reflects the vulnerability of these specimens to the fishing gear.
Female S. mitsukurii attain a larger total length than males, also observed for the same species by Wilson and Seki (1994) and Fischer et al. (2006) and commonly reported in sharks (Cortés, 2000) and batoids (Capapé et al., 2000; Capapé et al., 2008; Mnasri et al., 2009). However, in S. mitsukurii, Litvinov (1990) observed maximum sizes virtually equal in both sexes. The maximum total length recorded in the present study for S. mitsukurii in both sexes is within the range reported by other authors in other areas (Table 6). For males, this value varied from the range 48.0–51.9 cm (Central North Pacific) to 110.0 cm (SE Atlantic) whereas the females from 68.0–71.9 cm (Central North Pacific) to 110.0 cm (SE Atlantic). Size at maturity along with size at 50% maturity (when available) reported for S. mitsukurii in this study and elsewhere are presented in Table 6. This parameter varied from 40.0–45.0 cm TL (this study) to 65.0 cm TL (SE Atlantic) in the males and 49.0–51.0 TL (this study) cm to 89.0 cm TL (Central North Pacific). Taniuchi et al. (1993) already reported the variability in reproductive parameters of S. mitsukurii by examining specimens from four NW Pacific localities, demonstrating later that age at maturity also varied between areas (Taniuchi et al., 1999). Litvinov (1990) raised the possibility for the existence of reproductively isolated subpopulations. Lucifora et al. (1999) argued on the plasticity of the size at maturity for this species. For Fischer et al. (2006) the considerable differences in sizes at maturity between populations from the northern Pacific and Atlantic (as those shown in Table 6) could mask the presence of two species: S. mitsukurii for the Pacific and S. blainvillei for the Atlantic. For the NW Pacific Ocean, Taniuchi et al. (1993) observed that both sexes matured at smaller sizes and that the fecundity and size ranges of pregnant females were lower at latitudes closer to the equator. Fischer et al. (2006) however reported the opposite pattern for the southwestern Atlantic, the result of several abiotic and biotic factors including the effect of fisheries. Populations of S. mitsukurii have been intensively fished in the southwestern Atlantic for the past 30 years (see Vooren et al. (1990) for the South Brazilian area). However, stocks from off northeastern Brazil would have not been exploited yet, according to Fischer et al. (2006). However, more research is needed to assume so. Similarly to Wilson and Seki (1994), the currently study observed a positive correlation between ovarian fecundity and maternal size. This relationship was expected and has been observed in several other Squalus species (Avsar, 2001). We noted that ovarian fecundity varied from 1 to 15 vitellogenic follicles and uterine fecundity varied from 1 to 10 embryos in S. mitsukurii. Both values are within the range recorded by other authors elsewhere (Table 6). Large ovarian and uterine fecundity ranges for S. mitsukurii were recorded by Fischer et al. (2006) (3–27 and 3–11, respectively) and by Taniuchi et al. (1993) (4–15 and 4–15, respectively), comparing with authors form other areas (Table 5). Fischer et al. (2006) observed that the fecundity-female size positive correlation in S. mitsukurii would be the reason why southern Brazilian S. mitsukurii females have a lower number of vitellogenic follicles and embryos, when compared with specimens from other areas that attain larger sizes. Our results are consistent with those of Calderón (MS 1994), for southern Brazil, who recorded similar female maximum and maturity sizes as well as similar fecundity values (Table 6). Capapé et al. (2002) and Conrath (2004) argued that the difference between ovarian and uterine fecundity indicates that a certain number of oocytes undergo atresy. However, some authors recorded the same maximum number of ovarian follicles and embryos in S. mitsukurii (Table 6). For other squaloid sharks, mean biennial fecundity was calculated in eight pups by female in S. acanthias, with positive relationships between size and fecundity (Avsar, 2001). In the roughskin spurdog Cirrhigaleus asper uterine fecundity was found to be 12–19 (Fischer et al., 2006).
In the present study, the analysis of the relative frequency of embryos TL demonstrated that the largest embryos (full term litters) occurred in early autumn 1996. Also high embryos TL classes were observed in late autumn 1995. Parturition could therefore occur in autumn-winter off Uruguay. The presence of ovulating females and candled uterine embryos in early spring 1995 would indicate that ovulation may occur immediately after birth. However, we are aware that with the present data are not sufficient to assess the length and timing of the events compounding the reproductive cycle (i.e., ovulation, mating, gestation, birth) and the possible synchronicity to the population level. Graham (2005) observed that in three Squalus species reproduction was continuous, with no evidence of seasonality. Bass et al. (1976); Wilson and Seki (1994) and Fischer et al. (2006) assumed (despite the fragmentary data) a biennial cycle for S. mitsukurii, consistent with those described for S. acanthias, where females undergo a 22-month long cycle (Wourms, 1977; Compagno, 1984). However, complex asynchronous cycles have been reported for squalid sharks (Yano and Tanaka, 1988; Yano, 1995; Watson and Smale, 1998). The hypothesis of parturition occurring in the period July–August off Uruguay, is reinforced by the fact that in early autumn 1995 the lowest percentage of gravid females was recorded, which could indicate that to the population level, most females had already given birth. So a reproductive cycle for S. mitsukurii off Uruguay on a biennial basis is rather speculative, as a longer cycle for the species would be also possible. Wilson and Seki (1994) reported evidences of a not well defined parturition period in S. mitsukurii. However, they observed the presence of the smallest uterine embryos in fall and winter, that at the same time, were absent in spring and summer, indicating a well-defined seasonal production cycle for young. Concomitant development of vitellogenesis and gestation had already been noted for S. mitsukurii by Litvinov (1990) and Fischer et al. (2006). As specimens of 24 cm TL recorded in our samples were free-swimming and the maximum size of an intrauterine embryo was 22 cm TL we inferred that size at birth may be situated in the TL range of 22–24 (Table 5).
In the present study, maternity and maturity ogives were presented, with MTL50 exceeding TL50 by 4.0 cm. Braccini et al. (2006b) argued that for species with complex reproductive cycles longer than one year, maternity ogives must be considered, apart from maturity ogives, otherwise population models would overestimate recruitment rates and bias assessment. Further age and growth studies are necessary and recommended in order to understand these processes temporally altogether with the reproductive parameters determined in this study.
We are grateful to the crew of RV Aldebarán, to the colleagues of DINARA’s Department of Fisheries Biology who collaborated with the sampling on board, to Dr. John Stevens for kindly providing taxonomical comments on the Australian S. mitsukurii-like specimens, to Dr. Leonardo Castillo-Geniz and Dr. Felipe Galván Magaña for kindly providing missing references and to four anonymous referees who made valuable comments on the submitted draft.
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3The following seasons occur in the southern hemisphere: summer (Jan–Mar), autumn (Apr–Jun), winter (Jul–Sep) and spring (Oct–Dec)