© 2005 International Council for the Exploration of the Sea
The emerging role of climate in post-smolt growth of Atlantic salmon
a UMass/NOAA CMER Program, Blaisdell House, University of Massachusetts Amherst, MA 01003, USA
b Department of Fisheries and Oceans PO Box 5030, Moncton, NB, E1C 9B6, Canada
c Freshwater Fisheries Laboratory Field Station, 16 River Street, Montrose, Angus DD10 8DL, Scotland, UK
*Correspondence to K. D. Friedland: tel: +401 782 3236. e-mail: Kevin.friedland{at}noaa.gov.
Though it is well established that mortality during the post-smolt year is critical in shaping recruitment patterns in Atlantic salmon (Salmo salar L.), the controlling mechanism for North Atlantic stocks remains elusive. The emerging paradigm is based on relationships between survival and ocean thermal conditions during the early marine phase. The survival of post-smolts from both Europe and North America has been correlated to sea surface temperature conditions during their first month at sea. In addition, data for European fish support the hypothesis that growth mediates survival during that time. Thus, the working model for a salmon recruitment mechanism is analogous to those proposed for other fish species. We present growth data for two stocks, the Girnock Burn, which is a tributary to the River Dee, Scotland, and the Margaree River, Canada. Circuli spacing data for Girnock Burn fish suggest post-smolt growth is negatively correlated with temperature in the migration corridors during the first months at sea, while post-smolt growth of Margaree fish appears to be positively correlated with temperature. Growth is either patterned by a physiological response to an optimal temperature, or is co-varying with some ecosystem effect on growth, and the growth response might affect mortality and maturation of the stocks.
Keywords: Atlantic salmon, climate, growth, post-smolt
Received 8 August 2004; accepted 25 April 2005.
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Introduction |
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The selective advantage of anadromy is attributed to the protection of early life history stages provided by relatively sheltered and stable freshwater rearing habitats where spawning occurs (Gross et al., 1988). Despite lower productivity than marine environments, sheltered freshwater rearing areas tend to produce stable recruitment to intermediate freshwater life stages, a phenomenon illustrated by Atlantic salmon (Salmo salar L.) life history (Chadwick, 1987). Hence, the freshwater portion of the life history is less commonly associated with the mechanisms that produce high or low recruitments. On the other hand, the marine phase is associated with variable survival, which in turn produces the wide swings in recruitment we observe on interannual and inter-decadal time scales (Bley and Moring, 1988; Jonsson et al., 2003). Though the role of mortality during the post-smolt year is critical in shaping recruitment patterns in Atlantic salmon, the nature of recruitment mechanisms for North Atlantic stocks has remained obscure.
A critical period for salmonids appears to be during the transition from freshwater to marine habitats. Salmon smolts are challenged by physiological stressors and exposed to a wider array of potential predators in marine habitats than in freshwater habitats (Magee et al., 2003; Vehanen, 2003). The idea that this time period represents a recruitment bottleneck is supported by observations of Pacific (Fisher and Pearcy, 1988; Holtby et al., 1990) and Baltic populations (Eriksson, 1994; Salminen et al., 1995). Support for similar recruitment control in Atlantic salmon populations (McCormick et al., 1998) comes from two sources, correlative analyses relating spring ocean climate conditions to recruitment and post-smolt growth analyses that relate growth to recruitment patterns.
Ocean conditions, as represented by sea surface temperature (SST) and variations in thermal habitat, show correlation with abundance and survival time-series in both North American and European stocks. Friedland et al. (1998a) analysed the survival time-series for two stocks from central Europe, one from southern Norway, and the other from eastern Scotland, and observed that thermal regimes during the first weeks at sea were correlated with their survival patterns. Climate mediation of survival was suggested by the environmental correlates; however, the nature of the survival mechanism was further elucidated with growth data for one of the two index stocks. In a follow-up study, Friedland et al. (2000) reported that post-smolt growth for the Scottish stock correlated to survival and climate conditions. Analogously similar to mechanisms hypothesized for larval and other juvenile fish, these data support the contention that recruitment patterning survival is simply a function of growth during a critical period, suggesting size-mediated predation control of salmon abundance as noted in other marine fish (Anderson, 1988; Pepin, 1991; Sogard, 1997). Environmental variation during spring has also been related to recruitment in North American fish. Friedland et al. (2003a, b) found that spring thermal conditions in the Gulf of St. Lawrence co-vary with recruitment time-series for North American stocks. European and North American salmon stocks appear to be responding to climate or to factors co-varying with SST. It is interesting, however, that the relationship between SST and survival appears to be negative in North America, opposite to what would be expected if temperature was directly affecting growth.
Post-smolt growth data for North American salmon are of limited utility in evaluating patterns of recruitment because of the origin of samples analysed thus far. A study comparing two hatchery stocks supports the view that survival rates between stocks can be related to post-smolt growth (Friedland et al., 1996); however, no evidence is yet available for a North American stock to show that interannual variation in survival is related to post-smolt growth because of the absence of data for wild fish (Friedland, 1998).
Our goal with this investigation is to examine the early marine growth of two stocks, the Girnock Burn, which is a tributary to the River Dee, Scotland, and the Margaree River, Canada, and to relate their growth patterns to SST conditions along the putative post-smolt migration pathways of the fish.
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Methods |
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The two systems, which are the focus of this study, are relatively pristine river systems supporting self-sustaining stocks of Atlantic salmon. The Girnock Burn is a tributary of the Dee River system in eastern Scotland (Figure 1). The post-smolt growth patterns of smolt cohorts emigrating from the Girnock Burn between 1964 and 1993 were examined on scales taken from homewater adult recaptures of tagged two-sea winter (2SW) fish. Fish scales were mounted between glass slides, and spacings between successive pairs of circuli in the post-smolt zone were measured by means of an image processing system. Measurements were made on a single scale from each specimen at a pixel resolution of 0.004 mm along the 360° axis of the scale (Figure 2). Sample sizes are given in Table 1. The Margaree River is located on Cape Breton Island along the southern shore of the Gulf of St. Lawrence (Figure 1). Scales of returning wild 1SW and 2SW adults were sampled during the migration period 1986–1994. The same data collection procedure was used for both scale samples.
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Growth during the post-smolt period was represented by indices derived from scale circuli spacing. The basis of representing growth with circuli spacing patterns has been demonstrated with salmonids and other fish species (Doyle et al., 1987; Barber and Walker, 1988; Fisher and Pearcy, 1990). For the purposes of this study, we were interested in developing indices that represent growth during the first months at sea. Using an analysis of post-smolt scales from tagged fish and ocean recaptures, Friedland et al. (1993) established that during the spring and summer growth seasons, circuli are laid down in salmon scales approximately every week. This period lengthens to approximately every two weeks by winter. Based on the assumption that four circuli pairs approximate a month of growth during spring and summer, we calculated a "first-4" index or the mean spacing of the first four circuli pairs meant to represent growth during the first month at sea. We similarly calculated a "second-4" index using the next four circuli pairs meant to represent the second month at sea; both first- and second-4 indices were calculated for each stock. We extended the monthly analysis of the Girnock fish by also computing a third and fourth spacing index, using the mean spacing of the next two sets of four circuli pairs, representing the third and fourth months at sea, respectively. In addition, we collected the total distance from the beginning of the marine growth zone to the first winter annulus in the Girnock fish, which represents the post-smolt growth increment or growth during the first year at sea.
We have limited knowledge of the post-smolt migration of Atlantic salmon, but what we do know provides a rationale for defining putative migration corridors for the studied stocks. Atlantic salmon smolts are surface orientated animals and are not always capable of outswimming ocean currents when they first go to sea (Jonsson et al., 1993). Post-smolt salmon are, in part, passively transported during their first months at sea; thus, a combination of swimming potential and current transport vectors will circumscribe an area relevant to a specific stock. After a few months at sea, post-smolts attain sufficient size to outswim currents and will distribute according to other behaviours, such as foraging and open ocean migration. Hypothetically, if smolts achieved highly directed swimming and were constrained to speeds between 0.5 and 1.0 body lengths per second, a band of potential migration distance after one month can be posited (Figure 1). A further observation can help constrain the likely migration routes of North American smolts. Dutil and Coutu (1988) observed that post-smolts could stay resident in the Gulf of St. Lawrence through the summer, suggesting inshore waters may be part of the post-smolt nursery. These data suggest that Margaree fish are likely to be in the Gulf of St. Lawrence during their first month at sea and that they could be resident in the Gulf during their second month at sea as well. How rapidly the fish might leave the Gulf would also depend on the direction of surface currents, which would vary by year. Holm et al. (2000) provide data on the summer distribution of European post-smolts. Their data show that currents and directed swimming result in a migration to the northwest, so Girnock Burn fish would be in the North Sea during their first month at sea and most likely migrating to the southern Norwegian Sea during the following months (Figure 1). Finally, smolt migration to the sea takes place over a multi-week period usually triggered by environmental cues (Whalen et al., 1999). From observations of the subject stocks, enumeration facilities indicate that Margaree fish migrate at the end of May to the beginning of June and Girnock fish migrate at the end of April to the beginning of May.
Post-smolt growth data were compared with SST fields extracted from version 2 of the optimum interpolation (OI) sea surface temperature (SST) analysis by Reynolds et al. (2002). These data are produced weekly on a 1° grid and use in situ and satellite SST plus SST simulated for sea-ice covered areas. Before analysis, satellite data are adjusted for biases using the methods of Reynolds (1988) and Reynolds and Marsico (1993). Pearson product-moment correlations were computed between the scale circuli spacing indices and the mean monthly temperature fields most likely associated with the growth pattern. For the Margaree analysis, we only examined the first two months at sea, assuming that swimming ability and point of origin of the post-smolts would constrain the potential distance they could achieve from their river of origin. The analysis was extended to the first four months at sea for the Girnock fish because of accessory findings on their growth and the nature of the ocean habitats they have to cross to reach their known summer distributions. The analysis was limited to years where both growth data and SST data were available, which begins in 1982. Correlation fields were displayed as contour plots in a geographic context. There is always the concern that time-series data used in correlation analysis might not be independent. For representative bi-variate plots of significant spatial correlation trends, we applied the effective number of degrees of freedom criteria to judge correlation significance (Pyper and Peterman, 1998).
Into the analysis, we introduced an accessory data set from a neighbouring river, the North Esk, for comparative purposes. The Esk is 60 km to the south of the Dee/Girnock system. Post-smolt growth increments collected from returns to the North Esk (Friedland et al., 2000) were compared with the related scale increments from the Girnock fish. The post-smolt growth increments were from scale back-calculation data from North Esk 2SW fish.
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Results |
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Circuli spacing patterns of Atlantic salmon scales from the Girnock Burn and the Margaree River salmon reflect the increased growth that occurs when smolts first go to sea. The annual mean first-4 growth index for Margaree 1SW and 2SW fish ranged from approximately 0.045 mm to 0.055 mm showing a pattern of increasing growth during the study period (Figure 3A). There were significant differences in the growth for 1SW and 2SW fish, in particular, the growth for smolt year 1989. The second-4 index for Margaree fish was significantly higher than for the first-4 index. This index also suggests that growth increased during the study period and that there were significant differences between 1SW and 2SW fish; the largest differences can be seen for the data from smolt years 1990 and 1993.
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Growth indices for Girnock Burn fish were slightly higher than indices for the Margaree fish. Annual means of the first-4 index for Girnock fish ranged from approximately 0.05 mm to 0.07 mm and suggest that early marine growth declined during the study period (Figure 3B). The second-4 index ranged from 0.065 mm to 0.075 mm and followed a similar time-series pattern as the first-4 index. The third- and fourth-4 indices for the Girnock ranged from 0.068 mm to 0.079 mm and 0.064 mm to 0.074 mm, respectively, and suggest that the later indices show similar interannual growth patterns (Figure 3B).
Correlation fields between Margaree scale growth indices and SST revealed environmental correlates with early marine growth that would appear to represent direct and indirect effects on the fish because not all of them were over ecologically relevant temperature ranges. Correlation between the Margaree 1SW first-4 growth index and May and June SST data are shown in Figure 4A and B, respectively. The number of observations for the Margaree data is eight, so a significant correlation coefficient is >0.71 at a 95% confidence level and >0.83 at a 99% confidence level. A significant negative correlation is observed in the May data. Correlation between the second-4 growth index and June and July SST are shown in Figure 4C and D, respectively. None of these correlations were significant. The same analysis was repeated for the growth indices derived from the scales of Margaree 2SW fish. Correlation between the Margaree 2SW first-4 growth index and May and June SST data is shown in Figure 5A and B, respectively. A significant negative correlation was observed in the May data and a significant positive correlation was observed in the June data.
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Representative bi-variate plots of significant correlations eliminated the concern that the scatters were influenced by outlier data and suggest that some correlations are likely to represent indirect effects on the fish. Significant correlation of May SSTs with the first-4 index for 1SW fish is bracketed over a temperature range of 3–4°C, which is outside the temperature range experienced by smolts entering the marine environment and cooler than temperatures post-smolts are believed to utilize during early marine residence (Figure 6A). Likewise, the significant May-first-4 correlation with May SSTs for 2SW fish is over a range of 3–4°C (Figure 6B). Both of the correlations also occur in an area of the Gulf of St. Lawrence that is outside the area where smolts are expected to be found at that time. The significant correlation between June SST and the first-4 index for 2SW fish is over a more ecologically relevant range of temperatures, 9–12°C, with respect to the temperature of first ocean entry and post-smolt distribution (Figure 6C). None of the plots indicate that outliers influenced the relationships. Furthermore, analysis of the effective number of degrees of freedom did not suggest that any change to the significance criteria was needed.
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Correlation fields between Girnock Burn scale growth indices and SST reveal environmental correlates with early marine growth that would appear to represent direct effects on the fish since they are over ecologically relevant ranges. Correlation between the Girnock 2SW first-4 growth index and April and May SST data is shown in Figure 7A and B, respectively. The number of observations for the Girnock data is 12, so a significant correlation coefficient is >0.58 at a 95% confidence level and >0.71 at a 99% confidence level. A significant negative correlation was observed in the April data. The correlation between the Girnock 2SW second-4 growth index and May and June SST data is shown in Figure 7C and D, respectively. A significant negative correlation was observed in the June data. The significant first-4 correlation with April SSTs for 2SW fish was bracketed over a temperature range of 6–8°C, which is close to temperatures associated with first ocean entry and post-smolt distribution (Figure 8A). The significant second-4 correlation with June SSTs for 2SW fish was bracketed over a temperature range of 10–12°C, which is well within the range of temperatures associated with first ocean entry and post-smolt distribution (Figure 8B). Analysis of the effective number of degrees of freedom did not suggest that any change to the significance criteria was needed for these correlations.
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A comparison with accessory data for the salmon stock in the North Esk was made to illustrate the potential importance of late season post-smolt growth in the Girnock stock. In comparing the post-smolt growth increments for North Esk and Girnock 2SW returns, we see evidence of coherence in post-smolt growth pattern between the two stocks (Figure 9). In particular there was a cluster of higher growth years in the early 1970s that is outside the time-series analysed in relation to SST data (limited to 1982 and onwards). Finally, when we compare the first-4 and second-4 growth indices to the post-smolt growth increments in Girnock fish, we see that the early marine growth is a poor predictor of the later season growth that occurred in the 1970s (Figure 10A and B, respectively). However, the third-4 and fourth-4 indices are much better predictors of the post-smolt growth increment, suggesting that late season growth, i.e. growth likely occurring during July and August, may be the growth mainly influencing the recruitment pattern (Figure 10C and D). This observation provides the rationale to extend the analysis of correlation fields between Girnock scale growth indices and SST to July and August growth and to extend the spatial range of the area examined for correlation further to the north, where the nursery is located. The correlation between the Girnock 2SW third-4 growth index and June and July SST data is shown in Figure 11A and B, respectively. A significant negative correlation is observed in both months. Correlation between the Girnock 2SW second-4 growth index and July and August SST data is shown in Figure 11C and D, respectively. Significant negative correlations were observed in both months. The significant third-4 correlation with July SSTs for 2SW fish was bracketed over a temperature range of 8–10.5°C, and the fourth-4 correlation with August SSTs over a range of 9–12°C, both of which are reasonable ranges for post-smolts (Figure 8C and D). Analysis of the effective number of degrees of freedom did not suggest that any change to the significance criteria was needed for these correlations.
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Discussion |
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TopIntroductionMethodsResultsDiscussionReferences |
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Our main finding is that early marine growth of Atlantic salmon is related to ocean conditions in the putative migration corridors related to specific stocks. The nature of this relationship is still poorly understood and may not be the same amongst stocks and stock groups. Our data for the Girnock Burn suggest that growth is negatively affected by higher temperatures that may be exceeding optimal temperatures for fish from the Girnock feeding at natural rations (Handeland et al., 2003). The spatial distribution of these correlations follows a northwest progression that would be consistent with the summer distribution of European post-smolts (Holm et al., 2000). The environmental variable associated with recruitment variability in Europe is thermal habitat, which does not address the issue of whether cool or warm conditions differentially affect post-smolts. Coherence between post-smolt growth patterns of Girnock and Esk salmon further supports the notion that post-smolt growth mediates survival in European fish (Friedland et al., 2000). The questions are whether or not the mechanism is growth inhibition caused by warm conditions, and whether or not the recruitment patterning growth occurs during the first months at sea or later in the post-smolt year.
The response of Margaree fish suggests that an entirely different mechanism may be at work with North American fish. Friedland et al. (2003a) report that a negative correlation exists between the abundance of 2SW fish and thermal conditions in the Gulf of St. Lawrence. Our data show that temperature appears to be positively correlated with growth of 2SW fish but not for 1SW fish. Is this sensible or a conundrum? One possible explanation worth exploring is the role of maturation in shaping interannual abundance. Friedland et al. (2003a) reported that the thermal effect is not equivalent on age groups; the abundance of 1SW fish is not significantly correlated with thermal conditions. The positive thermal effect on post-smolt growth may reflect the contribution of maturation rate on the apparent abundance of age groups owing to the idea that rapid post-smolt growth shifts a higher proportion of the surviving post-smolts to the 1SW abundance tally (Hutchings and Jones, 1998). The immediate question that arises is, why the equivalent growth effect was not seen in the Margaree 1SW fish. Maturation is related to growth, but it also appears that other factors can differentiate the age groups, for example migration trajectory can result in changed maturity schedule (Martin and Mitchell, 1985; Friedland et al., 1998b).
Temperature has primacy over ecological and physiological events affecting post-smolts during their transition to ocean life. Post-smolt metabolic rate changes dramatically with the smoltification process, increasing energy demands and actuating the need for the fish to increase their ration and make the transition to piscivorous prey (Hoar, 1988). Levings (1994) suggested that temperature might be of equal or greater importance than the type and quality of food items in the diet of post-smolts. Beaugrand and Reid (2003) observed correlation between salmon catch and time-series of ocean colour and zooplankton data, suggesting that lower trophic level production is influencing salmon post-smolts via either the abundance or quality of prey items. It is interesting that the well-known gadoid outburst, which has recently been attributed to the production pattern of zooplankton (Beaugrand et al., 2003), approximates the same time period that salmon stocks were in high abundance in Europe. In studies of California Current salmonids, Brodeur et al. (2004) found that size and condition of post-smolts were related to oceanographic conditions in the rearing areas, with temperature being a contributing variable. It is difficult to differentiate the role of competing factors for Atlantic salmon because we have yet to replicate the California Current experiment where growth and condition were measured concurrently with conditions and resources in the rearing areas. Furthermore, growth effects can apparently propagate through the course of the post-smolt year and impact cumulative mortality the first winter season after migration to sea (Beamish et al., 2004), making measurement of the temporal progression of recruitment patterning mortality that much more important.
Our assumptions about the environmental window for post-smolts are critical to dismissing the relationships suggested for relatively cold waters (<4°C) of the eastern Gulf of St. Lawrence. Though we have no data demonstrating lethality of cold conditions in natural waters, Sigholt and Finstad (1990) showed that seawater temperatures of 6–7°C are lethal to salmon smolts in cage rearing settings. We must therefore assume that any correlates relating growth to transitional states of cold-water masses near the time of smolt ocean entry must reflect some co-variation with conditions or factors affecting the fish at some later time and in warmer areas.
Thermal conditions have emerged as one of the most important indices of salmon productivity in both the Pacific and Atlantic (Downton and Miller, 1998; Friedland et al., 2003b). In regard to the North Atlantic, there is accumulating evidence of the importance of the linkage to temperature conditions extant during the early marine stage (Sigholt and Finstad, 1990; Reddin and Friedland, 1996; Friedland et al., 1999). In regard to the Pacific Ocean, Welch et al. (1995, 1998) demonstrated that temperature can act to restrict steelhead trout and Pacific salmon ocean distribution and may ultimately control productivity of these stocks. Other studies of Pacific salmonids suggest that ocean climate, in particular temperature, controls abundance and landings (Beamish and Bouillon, 1993; Downton and Miller, 1998), and that future productivity may be limited by global warming effects (Welch et al., 1998). Understanding the mechanistic linkage between thermal conditions and growth response will undoubtedly contribute to our ability to manage these species under changing climate conditions.
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Acknowledgements |
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We thank M. Manning for image-processing assistance.
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References |
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