ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on June 22, 2007
ICES Journal of Marine Science: Journal du Conseil 2007 64(6):1136-1144; doi:10.1093/icesjms/fsm080
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Larval otolith growth histories show evidence of stock structure in Northeast Atlantic blue whiting (Micromesistius poutassou)
Commercial Fisheries Research Group, Department of Life Sciences, Galway Mayo Institute of Technology, Dublin Road, Galway, Ireland
Correspondence to D. Brophy: tel: +353 91 742484; fax: +353 91 758412; e-mail: deirdre.brophy{at}gmit.ie
Brophy, D., and King, P. A. 2007. Larval otolith growth histories show evidence of stock structure in Northeast Atlantic blue whiting (Micromesistius poutassou). – ICES Journal of Marine Science, 64: 1136–1144.Oceanographic modelling studies suggest that blue whiting (Micromesistius poutassou) larvae released on the Northeast Atlantic spawning grounds split into two branches, one following a northerly drift trajectory and the second drifting towards the south. This mechanism is proposed to restrict gene flow between northern and southern stock components. This study examined larval growth histories recorded in otoliths of adult blue whiting from three regions of the main spawning area and three feeding areas for evidence of divergent dispersal pathways. Increment measurements show that fish from the south of the spawning area on average grew significantly faster as larvae than those from the north of the spawning area, confirming that blue whiting spawning west of Ireland and Scotland do not form a randomly mixing unit, and that larval dispersal influences the subsequent distribution of spawning adults. Larval otolith growth rates in feeding blue whiting from the Bay of Biscay were significantly faster than those of fish from the Norwegian Sea feeding grounds, showing that mixing of fish from these areas is limited. Fish from the Bay of Biscay grew faster as larvae than fish from all regions of the main spawning area. The results support the proposed split in the blue whiting stock and signal caution for managing the fishery.
Keywords: blue whiting, larval dispersal, Micromesistius poutassou, otolith microstructure, population structure, stock identification
Received 22 September 2006; accepted 10 May 2007; advance access publication 22 June 2007.
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Introduction |
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 Top Introduction Materials and methodsResultsDiscussionReferences |
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In fish stock assessment, management units are assumed to represent closed populations, although the designation of these divisions may not be based on knowledge of the structure of the stock (Begg et al., 1999). Management of a fishery as a single stock when it is actually composed of more than one non-randomly mixing unit can lead to bias in stock projections (Daan, 1991; Begg et al., 1999). For this reason, stock identification is an essential component of sustainable fisheries management.
The concept of a stock is not rigidly defined, and it may vary depending on the application (Waldman, 2004). A genotypic stock is reproductively isolated and genetically discrete from other stocks of the same species (Booke, 1981; Kutkuhn, 1981). However, although even small levels of gene flow can produce genetic homogeneity, a low degree of reproductive exchange may not be enough to replenish an overexploited fishery or a component within a fishery. Despite considerable advances in genetic techniques, phenotypic markers remain important for identifying groups of fish that for management purposes should be treated as distinct stocks (Hare, 2004). Phenotypic information stored in the otolith provides a particularly powerful tool for discriminating between stocks because of its chronological nature. Otolith microstructure or composition can be used to identify groups that were spatially or temporally discrete at a particular point in their life history. When measurable differences arise in the early larval portion of the otolith, it indicates that the groups were spatially or temporally distinct soon after hatching, and may intimate distinct spawning origin.
In the pelagic environment, where there are few obvious physical barriers to movement, ocean circulation patterns have a crucial influence on the distribution of larvae and the structure of fish populations. Topographic features such as seamounts and banks produce circulation features that may influence the distribution of planktonic organisms (Mohn and Beckmann, 2002). Oceanographic mechanisms in combination with fish spawning behaviour can ensure that offspring from different spawning aggregations remain distinct. Eggs and larvae of fish spawning at different times or locations may be either retained close to their spawning site or carried along divergent drift trajectories (Bailey et al., 1997; Ruzzante et al., 1998; Bruce et al., 2001), thus limiting mixing of larvae from different spawning aggregations.
The early life history information stored in the larval region of fish otoliths can provide insight into the influence of ocean transport on stock structure. The periodic deposition of protein and calcium carbonate produce visible increments in otolith structure which can be revealed via sectioning and polishing of the adult otolith (Stevenson and Campana, 1992). Environmental variables such as temperature (Reichert et al., 2000; Folkvord et al., 2004), prey density (Johannessen et al., 2000; Feet et al., 2002), and photoperiod (Dowd and Houde, 1980) can influence otolith growth rate. Environmental conditions along larval drift trajectories may be reflected in the width of increments at the larval core. A number of field studies have used larval otolith microstructure to reconstruct recent environmental histories (Bailey and Heath, 2001; Baumann et al., 2003) or to infer larval drift trajectories (Kokita and Omori, 1999). When growth histories of larvae from different areas or spawning seasons are sufficiently distinct, otolith microstructure patterns at the larval core can be used to assess the integrity of adult populations (Quinn et al., 1999; Husebo et al., 2005; Brophy et al., 2006).
In this study, measurements of increments at the larval core of adult otoliths are used to investigate the influence of ocean circulation and adult spawning behaviour on blue whiting (Micromesistius poutassou) stock structure. For most species studied, the rate of increment deposition has been shown to be daily and generally proportional to somatic growth. Exceptions to this can occur in extremely poor growth conditions when non-daily increment formation and a decoupling of otolith and somatic growth have been observed (Geffen, 1982; Barber and Jenkins, 2001; Baumann et al., 2005). However, regardless of the timing of increment formation and its relationship with somatic growth, variability in increment width patterns at the larval core indicates variability in the growth conditions experienced during the larval phase. Here, larval increment width patterns are used as a marker of larval growth history. Interpretation of the results does not rely on assumptions of daily increment formation or exact proportionality between otolith and body growth.
Blue whiting in the Northeast Atlantic support an important international commercial fishery that is concentrated on the main spawning aggregations from March to May in the region encompassing the Porcupine Bank and the waters west of Ireland and Scotland (Bailey, 1982). There is strong evidence that fish from feeding areas in the Norwegian Sea make annual migrations to the main spawning grounds in February, with spent fish returning north from May to June (Bailey, 1982). It has been suggested that blue whiting from nursery areas in the Bay of Biscay and from a residual resident population to the west and southwest of Ireland also contribute to the spawning aggregations, with some smaller fish migrating south after spawning (Bailey, 1982; Carrera et al., 2001).
The level of mixing between these suggested subgroups in the main spawning aggregation is uncertain. Results from morphometric and meristic studies support the existence of two stock components within the main spawning aggregation; a northern component that spawns north of Porcupine Bank and a southern component that spawns to the south of the bank and along the continental slope (Isaev and Seliverstov, 1991). Genetic studies have also revealed some genetic heterogeneity in the main spawning aggregations (Ryan et al., 2005).
An ocean circulation model has been proposed as a mechanism for maintaining structure within the stock (Skogen et al., 1999). It is suggested that fish from the northern component will tend to spawn north of the Porcupine Bank, where oceanographic conditions will produce a predominantly northward flow of their eggs and larvae, whereas the southern component will spawn to the south of the bank and their eggs and larvae will drift south, thus maintaining at least some degree of separation between the stocks. The potential for stock mixing exists on the Porcupine Bank (53–55°N), where the direction of flow shows interannual variability (Bartsch and Coombs, 1997; Skogen et al., 1999; Kloppmann et al., 2001). After the first week of life, blue whiting larvae rise to the upper 100–50 m of the water column (Coombs et al., 1981), and their growth is influenced by the temperatures within this layer. Larvae that drift north will move into cooler waters than those that follow a southerly drift trajectory. It is likely that this will be reflected in the otolith microstructure at the larval core. Indeed, over smaller spatial scales, such a relationship between north/south temperature variation and otolith growth rate has been observed (Bailey and Heath, 2001). If this split in the larval population is maintained in aggregations of spawning adults, and if the divergent drift pathways expose blue whiting to different conditions for growth, fish from the north and the south of the spawning grounds will show variation in otolith microstructure at the larval core. However, if fish on the spawning grounds form a single, randomly mixing population, spatial variability in larval growth history will not be preserved in aggregations of spawning adults.
This study tests the hypothesis that fish from the north and the south of the Porcupine Bank have distinct growth patterns in the larval portion of the otolith, with fish that grew faster as larvae (suggesting a southward drift trajectory) occurring in the south, and those that grew more slowly as larvae (suggesting a northerly drift trajectory) being found in the north. If present, this spatial variability in otolith growth histories would support the split in larval drift trajectories proposed by Skogen et al. (1999) and confirm that the fish spawning west of Ireland and Scotland do not form a randomly mixing unit. Spatial variability in larval growth history is investigated in 3 year classes collected over 2 years. Larval otolith growth rates in fish collected from feeding grounds in the Norwegian Sea and the Bay of Biscay are also analysed. It is proposed that fish from the Norwegian Sea will display lower larval otolith growth rates than those in the Bay of Biscay because of their distinct larval histories. Spatial variability in larval otolith growth patterns is assessed in the context of the current hypothesis that fish spawning to the north of the spawning grounds feed in the Norwegian Sea, whereas those spawning to the south of the spawning grounds feed in the Bay of Biscay.
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Materials and methods |
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TopIntroductionMaterials and methodsResultsDiscussionReferences |
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Blue whiting were collected from the main spawning aggregation west of Scotland and Ireland during the Norwegian Blue Whiting Survey on board the RV "Johan Hjort" in March/April 2003, and during the International Blue Whiting Survey on board the RV "Johan Hjort", the RV "Celtic Explorer", and the RV "Tridens" in March/April 2004. Additional samples were collected from commercial fishing vessels operating in the spawning area during the same period. Blue whiting were also collected from non-spawning aggregations in the Norwegian Sea, West of Ireland, and the Bay of Biscay. These samples were obtained during a survey of the feeding grounds in the Norwegian Sea on board the RV "G. O. Sars" in July/August 2003, from the Irish groundfish survey on board the RV "Celtic Explorer" in October 2003, and from a survey in the Bay of Biscay on board the RV "B. O. Cornide de Saavedra" in September 2003 (Figure 1). All fish were collected with a pelagic trawl.
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Total lengths of each fish were measured to the nearest 0.5 cm, and fish were weighed to the nearest 1 g. Sex and maturity stage were assigned by visual inspection of the gonads, and otoliths were removed. Otoliths were viewed in water using a stereomicroscope, and the opaque (summer) and translucent (winter) bands were enumerated to derive estimates of age.
After age determination, subsamples of the fish were selected for microstructure analysis. The sampling area was divided into six regions: North spawning (NS), Mid-spawning (MS), South spawning (SS), Norwegian Sea feeding (NF), West of Ireland feeding (WF), and Bay of Biscay feeding (BF) (Figure 1). Each sampling region contained two sampling sites selected randomly from the available sampling stations. Two-, three- and four-year-old blue whiting from the 2000, 2001, and 2002 year classes. The term whiting should not be used in place of blue whiting or fish as this refers to a different species were selected by stratified random sampling from each of the six regions for inclusion in the otolith analysis.
Otoliths were cleaned of adhering tissue, mounted in epoxy resin, and polished on the distal surface on a lapping wheel with a series of graded silicon carbide papers; 300 grit, 600 grit, and 2400 grit. Polishing was continued until the increments in the larval portion of the otolith were just visible beneath the polished surface. Otoliths were then remounted in epoxy resin and polished on the proximal side in the same way until the larval core and daily increments were fully exposed. After polishing, otoliths were etched in a proteinase solution, as described in Shiao et al. (1999), to enhance the clarity of the daily increments.
Etched otoliths were examined under a light microscope at a magnification of x1000. Otolith microstructure measurements were made using a digital CCD camera and image-analysis software (Olympus DP–Soft). The widths of the first 20 increments were measured along the longest growth axis (Figure 2). Otoliths of 425 blue whiting were included in the microstructure analysis. In a subsample of 30 otoliths, increment measurements were repeated three times, and the CV of the three measurements was calculated to evaluate measurement precision.
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The mean width of increments 1–20 was used as a measure of early larval otolith growth. Data were screened for normality and homogeneity of variance, and transformed where appropriate. Spatial variability in larval otolith growth histories was examined in fish collected from the spawning grounds, using ANOVA. Year classes were analysed separately to avoid the potentially confounding effect of interannual variation in larval otolith growth rate. Spatial variability in larval otolith growth rate among adults collected from the spawning grounds was examined in fish from the 2000 year class, collected as 3-year-olds in 2003 and as 4-year-olds in 2004. This analysis was repeated using fish from the 2001 year class, collected as 2-year-olds in 2003 and as 3-year-olds in 2004. For the 2002 year class, there were insufficient fish from the MS region, so the analysis was carried out with fish from two regions – NS and SS, collected as 1-year-olds in 2003 and as 2-year-olds in 2004. In each analysis, region and sampling year were included as orthogonal fixed factors, and site as a random factor nested within region and sampling year. Equal numbers of otoliths from each region and sampling year were included in the analysis to ensure that the data were balanced. When the interaction or nested terms were not significant at p > 0.25, they were pooled with the error term to increase the power of the test for the main effects (Winer et al., 1991). Where significant effects were detected, pairwise comparisons were carried out using Tukey's post hoc test.
A separate analysis was carried out to include fish collected from the three feeding areas in 2003, and fish collected from the three areas on the spawning grounds in 2003 and 2004. The 2000, 2001, and 2002 year classes were analysed separately using univariate ANOVA, with region as the fixed factor. Where significant effects were detected, pairwise comparisons were carried out using Tukey's post hoc test.
The mean width of increments 1–20 was used in a univariate discriminant function analysis to assess the extent of group separation based on larval growth. For this analysis, groups that showed similar increment width patterns were pooled (group 1, BF; group 2, WF, SS; group 3, MS, NS, NF).
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Results |
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Otolith larval growth rates were highly variable, the mean width of increments 1–20 ranging from 0.78 to 6.6 µm (Table 1). The mean CV from repeated readings was 9.3%. The range of increment width measurements showed considerable overlap between areas (Figures 3 and 4). However, there was spatial heterogeneity in larval otolith growth rate. Fish that displayed very fast otolith growth rates as larvae, with mean widths at increments 1–20 exceeding 3.9 µm, were in the SS, MS, BF and WF regions, but were absent from the NS and NF regions. Similarly, fish that displayed slow otolith growth rates as larvae (<2.2 µm) were absent from the BF region, and very slow growth as larvae (<1.3 µm) was only observed in fish from the NS, MS and NF regions.
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ANOVA confirmed that spatial variability in larval otolith increment widths is preserved in aggregations of spawning adults. In each analysis (2000, 2001, and 2002 year classes), widths of increments 1–20 showed no significant variability between sampling sites within regions (p > 0.25), so sites within each region were pooled. In the analysis of fish from the 2000 year class, there was no significant interaction between orthogonal factors year and region, and no significant variability in increment width between years (p > 0.05). Increment widths were significantly different between regions (p < 0.001, Table 2). Tukey post hoc comparisons confirmed that increment widths were significantly greater in fish from the SS region than from the MS and NS regions (p < 0.001). For the 2001 year class, there was a significant interaction between year and region, so post hoc multiple comparisons were carried out within each year and within each location separately (p = 0.003, Table 3). Tukey pairwise comparisons confirmed that there was no significant difference in increment width between regions for fish from the 2001 year class collected from the spawning grounds in 2003 as 2-year-olds. For the same year class collected in 2004 as 3-year-olds, mean increment width was significantly greater in fish from the SS region than from the MS (p < 0.05) and NS regions (p < 0.001). Multiple comparisons within each region revealed that, in the NS region otolith growth rates were significantly higher in fish collected in 2003 than in 2004 (p = 0.009). In the SS region otolith growth rates were significantly slower in fish collected in 2003 than in 2004 (p = 0.02), whereas in the MS region, there was no significant difference between years (p > 0.05).
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For the 2002 year class, there was no significant interaction between orthogonal factors year and region, or in increment width between years (p > 0.05). Larval otolith growth rates were significantly different between regions with faster growth rates observed in fish from the SS than from the NS region (p < 0.001, Table 2).
The final set of ANOVAs included fish collected from the three feeding regions and the three spawning regions with the 2000, 2001, and 2002 year classes analysed separately. Increment widths were significantly different between regions for fish from the 2000 year class (r2 = 0.31, F = 17.1, p < 0.002), the 2001 year class (r2 = 0.37, F = 16.4, p < 0.001), and the 2002 year class (r2 = 0.42, F = 21.1, p < 0.001). For the 2000 year class, Tukey post hoc tests (Table 4) showed that increment widths were significantly greater in fish collected from the BF region than in fish from the three spawning regions and from the NF region (p < 0.001). Fish from the WF region showed significantly faster larval otolith growth than fish from the NF or NS regions (p < 0.05), but fish from the SS region showed significantly faster larval otolith growth than fish from the NS and the NF regions (p < 0.05). Similar patterns were observed for the 2001 year class, although there was less geographical heterogeneity in larval otolith growth rate, mainly because of faster larval otolith growth rates in fish feeding in the Norwegian Sea. No difference in larval otolith growth rate was detected when fish from the NF region were compared with fish from the SS and the WF regions (p > 0.05). For the 2002 year class, fish from the BF region again showed a faster larval otolith growth rate than fish from all other areas for which otoliths were available (NS, SS, and WF), whereas fish from the WF region grew faster as larvae than fish from the NS region.
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A discriminant function based on mean width of increments 1–20 (Wilk's Lambda = 0.638, p < 0.001) separated the three pooled groups with an overall jackknifed classification success of 60% (Table 5). Predictions of group membership were highest for group 1 (BF fish; 83%). The misclassified fish from this group were identified as belonging to group 2 (WF, SS), but never group 3 (MS, N, NF). Group membership predictions were most inaccurate for group 2 fish (SS, MS), most of these fish being misclassified (61%). In all, 35% and 25% of fish belonging to group 2 were misclassified as belonging to groups 3 and 1, respectively, and 25% and 6% of fish from group 3 were misclassified as belonging to groups 2 and 1, respectively.
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Discussion |
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Spatial variability in increment width at the larval core is evident in aggregations of adult blue whiting from spawning and feeding grounds throughout their distribution. It is unlikely that the spatial variability in otolith growth was greatly influenced by measurement error along a restricted increment sequence. In otoliths that were difficult to read, increments laid down after day 20 may have been mistakenly included in the 1–20 count and otolith growth would be overestimated as a result. If fish from one region contained a disproportionate number of otoliths that were difficult to read, there could be a systematic bias in the results. However, the otoliths that were more difficult to read, and that were more likely to produce errors, were the slow-growing otoliths with tightly packed increments. Any systematic overestimation of growth rate for those fish would reduce rather than enhance spatial variability in growth.
Although fish from different areas show considerable overlap in increment width and no group is entirely distinct, the occurrence of significant spatial variability confirms that blue whiting spawning west of Ireland and Scotland do not form a randomly mixing unit and that subunits within the spawning aggregations have, on average, experienced different conditions during the larval phase. The preservation of spatial variability in larval growth in the adult stock shows that distribution during the larval phase influences the subsequent distribution of spawning adults. The overlap in growth rate may indicate mixing of fish with different larval growth histories, or may simply arise because the larval environments are not sufficiently different to produce entirely distinct otolith growth patterns.
The factors responsible for the variability we observed in otolith growth have not been tested, and they do not affect the overall conclusions of the study. It is likely that differences in larval otolith growth rate reflect variation in temperature and food supply along larval drift trajectories, and they may also be influenced by the timing of hatching and by selective mortality during the larval phase. The effect of temperature and food supply on larval otolith growth is well documented (Campana and Hurley, 1989; Folkvord et al., 1997; Reichert et al., 2000; Feet et al., 2002; Otterlei et al., 2002). In field-sampled larvae, otolith growth is often correlated with temperature and feeding conditions in the associated water masses (Oozeki and Zenitani, 1996; Bailey and Heath, 2001; Jenkins and King, 2006). Blue whiting eggs and larvae are exposed to a wide range of temperature across their spawning grounds and larval drift pathways. Larvae released within the northern and southern sections of the spawning area are separated by distances of 640–1300 km. This corresponds to a mean monthly temperature difference of 1–3°C in the top 50 m of the water column during April and May (Levitus, 1998). Using the mean larval displacement distances estimated by Skogen et al. (1999) for 137 days after spawning (3.4–4.6 cm s–1), northerly and southerly drift from these areas during the first 25 days of egg development and larval growth could increase the geographic separation of fish spawned there by 150–200 km. This corresponds to a monthly mean temperature difference in the upper 50 m of 1.4–4°C between fish from the northern and southern extremes of the distribution during the same period (Levitus, 1998). Bailey and Heath (2001) observed significant variability in otolith growth profiles across latitudinal temperature gradients of 
1°C, so temperature differences between the northern and southern extremes of larval blue whiting distribution are sufficient to generate the variation in otolith increment widths observed here.
Larvae of blue whiting feed mainly on copepod nauplii. The larval period coincides with low prey abundance, and prey densities can fluctuate markedly from year to year (Hillgruber et al., 1997). Blue whiting appear to have adapted to food-limited environments, and are efficient at feeding in low prey concentrations (Hillgruber et al., 1997; Hillgruber and Kloppmann, 1999). Therefore, geographical variation in food abundance may have less of an influence on otolith increment width patterns than the north–south temperature gradient.
Assuming that temperature has a marked influence on otolith growth pattern in blue whiting larvae, the spatial variability in otolith growth pattern that we observed is consistent with the hypothesis of Skogen et al. (1999); fish spawned in the south of the spawning area and growing faster as larvae are found in the south as adults, and those spawned in the north and growing more slowly as larvae occur in the north as adults. The results also indicate that fish spawning on the Porcupine Bank (MS region) have, on average, encountered different environmental conditions and grown more slowly as larvae than fish spawning south of the bank. The topography of the Porcupine Bank leads to the development of Taylor column circulation patterns, which isolate the water in the area from adjacent water masses (White et al., 1998; Mohn and Beckmann, 2002). Evidence is that anticyclonic recirculation in the water over the Porcupine Bank may provide a mechanism for retaining larvae within the area under certain meteorological conditions (Kloppmann et al., 2001). The current results provides the first piece of field-based evidence that ocean circulation patterns produce a split in the larval population, and that this segregation is maintained in fish returning to the spawning grounds as adults.
The influence of larval distributions on the subsequent location of spawning in the adult population will impact on the structure of the stock. If adults tend to return to the same general area that they inhabited as larvae, and if ocean circulation patterns ensure that their offspring follow similar larval drift trajectories, then this will limit reproductive mixing of the northern and southern components. Interannual variability in circulation patterns (Bartsch and Coombs, 1997; Skogen et al., 1999) could result in larvae following a different trajectory from their parents, mixing with another stock component at juvenile nursery grounds and adult feeding areas, and subsequently spawning in a different location. Under this scenario, there would be limited gene flow under certain oceanographic conditions, and the components may not be genetically distinct. However, this level of segregation could be significant from a management perspective.
Larval growth histories also show heterogeneity between the feeding areas and the main spawning grounds. The fastest otolith growth rates were observed in fish from the Bay of Biscay feeding grounds. Those fish had significantly faster mean otolith growth rates than fish from each region on the spawning grounds. The results do not exclude the possibility that fish feeding in the Bay of Biscay contribute to spawning assemblages west of Scotland and Ireland. However, the differences confirm that none of the suggested subunits on the spawning grounds consist entirely of those fish. In addition, fish from the Bay of Biscay on average experienced different growth conditions during the larval phase from those feeding in the Norwegian Sea, confirming that mixing between the two groups is limited. Fish from the Norwegian Sea feeding grounds displayed slower mean larval otolith growth rates than fish from the south of the spawning grounds, with no detectable growth differences between the Norwegian Sea and the northern and mid-spawning grounds. This shows that blue whiting migrating from the Norwegian Sea makes a lesser contribution to spawning assemblages to the south of the spawning area than it does to assemblages in the more northerly parts.
As discussed above, similarity in otolith growth patterns does not confirm that groups of fish are of the same larval origin, because geographically segregated groups of larvae may experience similar environmental conditions and show no variation in otolith growth pattern. However, larval otolith growth patterns can be used to identify potential feeding areas for the northern and southern subunits on the main spawning grounds. Given the complete overlap in their otolith growth pattern, it is likely that fish from the West of Ireland feeding grounds contribute considerably to spawning assemblages in the south of the spawning area. Similarly, the lack of any significant variation in mean larval otolith growth rates between fish from feeding areas in the Norwegian Sea and the north of the spawning area provides support for the proposed migration of fish between these two areas and is consistent with genetic evidence (Giaever and Stien, 1998) and the observed growth patterns in adult fish (Monstad, 1996). No significant differences in larval otolith growth were detected between fish spawning in the mid-spawning grounds and fish feeding in the Norwegian Sea and west of Ireland. It is therefore plausible that fish from both feeding areas are contributing to the spawning assemblages in that area.
The observed inconsistencies between year classes and sampling years are difficult to interpret. The source of the discrepancy was the 2001 year class collected in 2003. Those fish showed no spatial heterogeneity in otolith growth pattern across the spawning grounds and the Norwegian Sea and west of Ireland feeding grounds. However, for the same year class collected in 2004, differences in growth rate were apparent, with faster larval otolith growth rates observed in the southern spawning grounds than in the north and mid-spawning grounds and the Norwegian Sea feeding grounds. The more homogenous growth patterns observed in 2003 are attributed to the presence of fish with faster larval otolith growth in the northern spawning grounds and fish with slower larval otolith growth in the southern spawning grounds. This may reflect interannual variability in the distribution of different stock components, leading to increased mixing of fish with different larval growth histories. However, increased mixing in 2003 is not evident in the 2000 or 2002 year classes, which showed spatial variation in otolith growth patterns in both sampling years. Alternatively, the lack of any spatial variation in otolith growth patterns in fish from the 2001 year class collected in 2003 may be linked to the timing of sampling relative to the migration of fish to and from the spawning grounds. As discussed above, it is likely that the variation in otolith growth histories observed across the spawning grounds is the consequence of subunits with different larval growth histories migrating to the spawning grounds and mixing with the resident population. The timing of spawning migrations is related to age in many fish species including blue whiting, older fish reportedly arriving at the spawning grounds first (Bailey, 1982). Therefore, a particular year class may show no spatial variability in otolith growth pattern because the migrating component of that year class is not present on the spawning grounds in sufficient numbers at the time of sampling. Temporal variation has also been observed in the genetic structure of blue whiting in the main spawning area (Ryan et al., 2005; Was et al., 2006) and in the Norwegian and Barents Seas (Giaever and Stien, 1998). Although such temporal genetic variability is difficult to explain, it has been cautiously linked to movements of fish from different population subunits in and out of the sampling area. The potential affect of sampling time on the interpretation of stock structure should be investigated further, using repeated sampling of spawning assemblages throughout the spawning period.
Analysis of larval otolith growth patterns has been used here to identify groups of blue whiting that have on average experienced different environmental conditions. Although fish from the Bay of Biscay could be identified with moderately high classification success (83%) based on larval increment widths, the prediction of group membership for fish from the west of Ireland feeding grounds and the southern spawning grounds was not much better than would be achieved by chance alone. Because of the extensive overlap in the growth patterns observed, it was not possible to identify larval origin in individual fish with great accuracy, or to measure the exact contribution of fish from each feeding area to the main spawning assemblage. This could be achieved by combining otolith increment width measurements with other environmental and genetic markers to obtain a unique signature for fish within each spawning and feeding area, which could then be used to track migration pathways between them. The use of multiple markers has proved to be a powerful approach in the elucidation of migration pathways and the separation of components in mixed assemblages for species such as Atlantic herring (Clupea harengus) (Ruzzante et al., 2006).
Blue whiting in the Northeast Atlantic are currently assessed as a single stock. However, there is mounting evidence from the current study and other research that blue whiting in the main spawning area do not form a randomly mixing unit (Skogen et al., 1999; Ryan et al., 2005; Was et al., 2006). Failure to account for structure in the stock could introduce bias into its assessment, leading to underestimates of fishing effort, inaccurate estimates of the trends in both fishing mortality and spawning-stock biomass, and the possible extinction of a subpopulation (Ovenden, 1990; Daan, 1991; Pawson and Jennings, 1996; Frank and Brickman, 2001).
In conclusion, growth histories recorded in the larval core of adult otoliths have shown that blue whiting spawning aggregations west of Ireland and Scotland do not form a randomly mixing unit, and that fish from feeding areas throughout the distribution do not contribute equally to spawning assemblages in the north and south of the spawning grounds. The results coincide with evidence from oceanographic modelling and signal caution for management of the stock.
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Acknowledgements |
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The study was funded through funding from the Department of Education, Ireland, to PAK under the Technological Sector Research: Strand III Core Research Strengths Enhancement Programme. Thanks are due to Mikko Heino, Manuel Meixide, Ronald Bol, Gavin Power, Ole Gullaksen, and all scientists and crew on board the RV "Johan Hjort", the RV "G. O. Sars", the RV "Celtic Explorer", the RV "B. O. Cornide de Saavedra", and the RV "Tridens" for their help with the sample collections. We also thank Peter Wright and two anonymous referees for their constructive comments which helped to improve an early version of the manuscript.
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References |
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  A. Was, E. Gosling, K. McCrann, and J. Mork Evidence for population structuring of blue whiting (Micromesistius poutassou) in the Northeast Atlantic ICES J. Mar. Sci., March 1, 2008; 65(2): 216 - 225. [Abstract] [Full Text] [PDF]
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