ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on June 27, 2007
ICES Journal of Marine Science: Journal du Conseil 2007 64(6):1161-1172; doi:10.1093/icesjms/fsm081
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Growth of juvenile Norwegian spring-spawning herring in relation to latitudinal and interannual differences in temperature and fish density in their coastal and fjord nursery areas
Institute of Marine Research, PO Box 1870 Nordnes, 5817 Bergen, Norway
Correspondence to Å. Husebø: tel: +47 55 238500; fax: +47 55 238687; e-mail: aase.huseboe{at}imr.no
Husebø, Å., Slotte, A., and Stenevik, E. K. 2007. Growth of juvenile Norwegian spring-spawning herring in relation to latitudinal and interannual differences in temperature and fish density in their coastal and fjord nursery areas. – ICES Journal of Marine Science, 64: 1161–1172.Norwegian spring-spawning herring (Clupea harengus) spawn in February and March along the Norwegian coast from 58°N to 69°N. The larvae are transported north with the coastal current, and in autumn, the main part of the 0-group is found in the Barents Sea, and a smaller and variable fraction ends up in coastal and fjord nursery areas that experience a wide range of environmental conditions and fish densities. Based on data from herring 0–2 years old collected from 1970 to 2004, there is a positive relationship between temperature and the growth of this coastal component, in terms of length, weight, condition factor, and annual otolith increment width, and a negative relationship between acoustic abundance and the same growth indices. In general, juvenile growth decreased northwards along the coast concurrently with decreasing summer and autumn temperatures and increasing acoustic abundance. It seems, therefore, that there may be interference in the relationship between juvenile herring growth and temperature, attributable to variable recruitment, currents, larval drift, and advection into the fjords, causing latitudinal and interannual differences in fish density, and hence variable competition for food.
Keywords: acoustic abundance, growth, herring, latitude, nursery area, temperature
Received 18 December 2006; accepted 13 May 2007; advance access publication 27 June 2007.
 |
Introduction |
|---|
 Top Introduction Material and methodsResultsDiscussionReferences |
|---|
We focus on two factors that potentially influence the growth of juvenile herring: ambient temperature and population density. Temperature is generally considered to be one of the most influential environmental factors in determining the growth of marine fish larvae (Houde, 1989; Morse, 1989). Therefore, models of growth and ingestion processes have demonstrated the positive effect of temperature on growth of herring (Clupea harengus) larvae (Fiksen and Folkvord, 1999), and this relationship has been verified in laboratory experiments with equal and adequate food regimes (Folkvord et al., 2004). Hence, growth is likely to follow interannual variations in temperature. However, differences in growth can also be explained by the counter-gradient hypothesis, wherein the potential for growth varies inversely with latitude in terms of decreasing temperatures (Conover and Present, 1990). Many marine fish species exhibit a latitudinal gradient, populations in higher latitudes exhibiting slower growth, later age at maturity, increased longevity, and likely lower population productivity (Beverton and Holt, 1959; Beverton, 1992). In contrast, the density-dependent growth hypothesis assumes that fish growth declines through increased competition for food when density increases, as demonstrated for herring on both sides of the Atlantic (Iles, 1968; Lett and Kohler, 1976; Sinclair et al., 1982; Anthony and Fogarty, 1985; Winters et al., 1986; Cardinale and Arrhenius, 2000; Axenrot and Hansson, 2003; Casini et al., 2006; Melvin and Stephenson, 2007), and in Pacific herring (Clupea pallasi) (Haist and Stocker, 1985; Tanasichuk, 1997).
Norwegian spring-spawning herring (NSS herring) have shown substantial fluctuations in recruitment and abundance over time (Hjort, 1914; Devold, 1963; Toresen and Østvedt, 2000), but at present it is the largest herring stock in the world, with a spawning-stock biomass (SSB) of more than 12 million tonnes (ICES, 2005). NSS herring clearly differ from other herring stocks, dispersing their larvae over a very large area and a broad latitudinal range. Spawning takes place on hard bottom substrata (stones, gravel, and shell sand) at depths down to 250 m, and the spawning grounds are located along the central Norwegian continental shelf between 58°N and 69°N (Sætre et al., 2002b). Regardless of spawning ground, most larvae drift north and eventually end up in the Barents Sea nursery area, whereas a comparably smaller portion ends up in coastal and fjord nursery areas along the coast from 58°N to 71°N (Dragesund, 1970a; Holst and Slotte, 1998), and although the strong year classes originate from the Barents Sea, the coastal and fjord nursery areas crucially act as buffers in years of poor recruitment (Holst and Slotte, 1998).
It has already been demonstrated that the growth of 0-group herring in the Barents Sea is influenced by temperature and population density (Ottersen and Loeng, 2000). Moreover, it has been demonstrated that interannual differences in the pre-recruit and adult growth of the coastal and Barents Sea components combined follows interannual fluctuations in temperature (Holst, 1996), and are significantly influenced by population density (Toresen, 1990; Engelhard and Heino, 2004a, b). However, studies focusing on latitudinal variation in growth of juvenile NSS herring in coastal and fjord nursery areas in relation to temperature and population density are scarce in the published literature, although data on biological parameters of juvenile herring, acoustic abundance, and ambient environmental conditions have been recorded synoptically in nursery areas at various latitudes along the coast since the 1970s. The dataset is unique for studies of temperature- and density-dependent growth, because they add a spatial aspect instead of simply focusing on interannual variations, as in most other studies on the subject. Hence, the main objective of this study was to test whether there were latitudinal and interannual differences in growth of juvenile NSS herring in coastal and fjord nursery areas that may be related to differences in temperature and population density.
|
Material and methods |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
Study area and biology
The study area was limited to the Norwegian coastal areas and fjords from 62°N to 72°N. As mentioned above, spawning and nursery areas of juvenile NSS herring are also found as far south as 58°N, but herring only use them sporadically, so data collected in those areas were excluded from the analyses. Further, for statistical comparisons, the coastal and fjord nurseries were split into five subareas in accordance with the areas used by the Norwegian Directorate for Fisheries for catch statistics (Figure 1).
|
Biological data were collected during autumn surveys carried out by the Institute of Marine Research (IMR) in the months September–December of 1970–2004. Juvenile herring were sampled with a pelagic trawl close to or at the surface. In all, 47 666 herring 0–2 years old were analysed from trawls distributed throughout the study area (Figure 1). Older juveniles were also occasionally present in some samples, but those were excluded from the analyses. In trawls in all five subareas, 0-group herring were more numerous than herring 1 and 2 years old (Table 1). In general, 30 fish were measured at each station, but in areas where the 0-group was mixed with older juveniles, more fish were included in the biological samples. The variables measured and included in the present analysis were body length (5-mm groups), weight (g), age, and the width of the annual growth zones in the otoliths. The condition factor (weight x length–3) was used as a parameter to describe the condition of the juveniles.
|
First year otolith growth of 0-group herring was defined as the total distance from the nucleus to the edge of the otolith, and the first and second year otolith growth of the 1-year-olds were defined as the distance from nucleus to the first winter ring, and the distance from the first winter ring to the otolith edge, respectively. Herring 2 years old were excluded from analyses of otolith growth, because most of them were aged by scales.
Abundance estimates
Acoustic estimates of abundance of 0-group herring in coastal and fjord nursery areas have been made annually since 1975 during the period September–December. The acoustic data have been reported to and used in assessment by the International Council for the Exploration of the Sea (ICES, 2005). The estimates, in millions of fish, have been split into four areas: south of 62°N, 62–65°N, 65–68°N, and north of 68°30'N. For this study, the estimates between 62°N and 68°N have been aggregated to analyse the effect of population density on juvenile herring growth, and this abundance index was assumed to be representative for statistical areas 1–2. Similarly, the abundance index north of 68°30'N was assumed to be representative for areas 3–5 (Figure 1). After 2002, a new survey design was introduced, which resulted in changed areas and a wider and denser coverage of the fjords in the north. Therefore, the estimates in areas 3–5 from 2003 on are likely to be higher and not directly comparable with the earlier estimates, which with few and minor exceptions are based on the same coverage. Consequently, the estimates for areas 3–5 during the years 2003 and 2004 were excluded from the analyses here.
Because of variable larval drift and advection into the coastal and fjord nursery areas, fish density in those areas is not necessarily related to total recruitment for the stock. Hence, the official assessment estimates of total recruitment at age 0 (R0) (ICES, 2005) were included for comparison.
Temperature data
Regular measurements of temperature with a CTD concurrently with acoustic observations of juvenile herring in the fjords and coastal waters started in 1986. Here, we included temperatures recorded 20 m deep (the approximate average school depth) from a total of 4118 stations taken within the defined study area during the years 1986–2004. These temperature data were assumed to be representative of ambient temperatures experienced by juvenile herring during autumn. Temperatures at 10, 30, and 50 m were different, but showed the same fluctuations. Note that temperature was not measured in 1987 in areas 2 and 5, and in 1989 in areas 1–3.
Additionally, 20 m deep temperatures recorded 1–4 times each month during the years 1970–2004 at IMR's coastal monitoring stations along the Norwegian coast were assumed to be representative of interannual and seasonal temperature fluctuations in the surrounding juvenile nursery areas during the summer feeding season (May–September). Hence, 2546 recordings were included from stations Bud (62°56'N 06°47'E), Eggum (68°22'N 13°38'E), and Ingøy (71°08'N 24°01'E), and in statistical analyses, these stations were assumed to be representative of temperature fluctuations in the respective areas 1–2, 3, and 4–5 (Figure 1). Note that the summer temperatures were not measured at Bud in 1994 or 1995, at Eggum in 1972, and at Ingøy in 1977.
To present interannual differences in temperature graphically, the data were smoothed using 3-year running means, but for statistical tests, the actual annual means were used.
Statistical analyses
SAS (SAS Institute, 2005) was used to extract the data from the IMR's database, and STATISTICA 7.0 (StatSoft Inc., 2006) was used for all statistical analyses and graphics.
One aim of the work was to test whether the measured growth variables and recorded temperatures differed significantly by sampling area on a latitudinal range, or interannually within areas. For these analyses, data were pooled over periods of several years and months. Hence, when testing for the effects of sampling area on growth variables and temperature, linear regression models were run with year and day number as covariates, to adjust for this temporal effect. Correspondingly, when testing for interannual differences in growth variables and temperature, linear regression models were run area by area, with day number as covariates. The adjusted mean values ±95% confidence intervals (CI) of temperature and growth variables resulting from these analyses are presented graphically to demonstrate latitudinal and interannual differences.
Another aim was to test whether latitudinal and interannual differences in the measured growth variables were related to differences in recorded temperatures and population density. Therefore, the annual adjusted mean values of temperature and growth variables from each area were used in simple and multiple regression analyses together with indices of acoustic abundance, to study the individual and combined effects of temperature and population density on growth.
Note that in some areas and years, there were very few or no data on growth, especially of 2-year-olds. Hence, all age groups, areas, and years with n < 10 data points were excluded from graphics and further statistical analyses. Note also that the growth parameters of 1-year-olds were related to the average temperature and acoustic abundance in the year of collection and the year before collection. These average values were assumed to be representative for the temperature and population density experienced over the two seasons of growth. Similarly, the length of 2-year-olds was related to the average temperature and acoustic abundance in the year of collection and the two years before collection.
Residuals from the statistical analyses all followed the normal distribution. Hence, the assumptions underlying these types of parametric tests were not followed. Note that the acoustic abundance index was log-transformed before testing in order not to violate this assumption.
|
Results |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
Latitudinal and interannual fluctuations in growth
The growth of juvenile herring in coastal and fjord nursery areas was inversely related to the latitude of collection. All growth variables (length, weight, condition factor) of juveniles 0–2 years old that were analysed, decreased significantly northwards from areas 1–5 (linear regression models, p < 0.001) (Figure 2). The same negative latitudinal effect was found for first year otolith growth of the 0-group, as well as for the first and second year otolith growth of 1-year-olds (linear regression models, p < 0.001) (Figure 3).
|
|
Interannual differences in body length of 0–2-year-old herring were observed in all areas studied (linear regression models, p < 0.001) (Figure 4). In the north (areas 3–5), growth peaked around 1970, 1980, 1990, and at the end of the study period around 2004, whereas in the south (areas 1–2), the decline in growth in the mid-1990s and the subsequent peak around 2004 was not as evident as in the north. Similar periodic fluctuations were also found for the other growth variables analysed, although they are not presented here.
|
Latitudinal and interannual variations in temperature and abundance
Summer and autumn temperatures experienced by juvenile NSS herring along the coast were clearly lower in the north. Temperatures recorded at IMR's coastal monitoring stations along the Norwegian coast in the years 1970–2004 were significantly influenced by area and month of collection (linear regression models, p < 0.001), decreasing northwards in all months and peaking in September (Figure 5a). Similar latitudinal differences were found during the autumn survey (September–December of 1986–2004) (linear regression models, p < 0.001); the adjusted mean temperature decreased northwards from 10.2°C in area 1 to 6.8°C in area 5 (Figure 5b).
|
A closer look at the interannual differences in temperature revealed periodic changes similar to those found in juvenile herring growth. There were four temperature peaks in summer data from the coastal monitoring stations (Figure 6a); around 1973, 1983, 1990, and 2002. Similarly, the autumn survey temperatures tended to peak around 1990 and 2000 (Figure 6b). Note that at the most southern monitoring station, Bud, there was an additional peak around 1998.
|
Pooled acoustic estimates of 0-group herring from the fjords in the two southern areas (Figure 7a) were small and fluctuated in a different manner from estimates made farther north (Figure 7b). According to official ICES assessments, the recruitment of NSS herring peaked in 1983, 1992, 1998, and 2002 (Figure 7c). The high recruitment in 1983 and 2002 was apparent also in the coastal nursery areas, in both the south and the north. However, the strong 1992 recruitment was apparent in the southern fjords only, and the 1998 peak was apparent in the northern fjords only.
|
Effects of temperature and acoustic abundance on growth
In general, the body length of 0–2-year-olds increased with ambient summer and autumn temperatures, and decreased with acoustic abundance (Figure 8). The single effect of temperature and acoustic abundance was revealed in simple regression analyses (Table 2), and the combined effect was demonstrated in multiple regression analyses (Table 3). The relationships were significant for most age groups, seasons, and periods tested. An exception was that body length of 2-year-olds was not significantly related to acoustic abundance regardless of period tested. Using data from 1986 on, the effects of autumn and summer temperatures on body length of 0-group herring were less significant (lower ß-values) than the effect of acoustic abundance (Table 3), but the opposite applied to 1-year-olds. However, using data going back to 1975, including a longer period with low recruitment, the effects of summer temperature and acoustic abundance were the same.
|
|
|
Note that, although they are not presented here, all other growth variables were tested in the same manner as body length, with similar results. In addition, the same respective positive and negative effects of temperature and acoustic abundance were found when tested within areas. In general, more variance was explained (higher r2) and relationships were stronger (higher ß-values) in the northern (areas 3–5) than in the southern areas (areas 1–2).
|
Discussion |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
Our study has demonstrated that latitudinal and interannual differences in growth of juvenile NSS herring in nursery areas along the Norwegian coast can be related to differences in temperature and acoustic abundance. In general, juvenile growth decreased northwards along the coast concurrently with decreasing summer and autumn temperatures and increasing acoustic abundance, but the respective positive and negative effects of interannual variations in temperature and population density were also observed within areas.
The inverse relationship found between latitude and juvenile NSS herring growth is a follow-up from previous studies which demonstrated that herring from coastal and fjord nurseries grow faster and recruit to the spawning stock 1–2 years earlier than fish growing farther north in the Barents Sea (Lea, 1929a, b; Ottestad, 1934; Runnström, 1936; Holst, 1996). Already at the larval stage, there appears a latitudinal gradient in individual somatic growth of this stock (Fossum and Moksness, 1995; Stenevik et al., 1996), a statement further supported by model predictions that clearly indicate that larvae drift through warmer waters the farther south they hatch (Slotte and Fiksen, 2000). According to our results, the latitudinal effect on 0-group growth also carries on through ages 1 and 2. This finding agrees with that from a study on Irish herring by Brophy and Danilowicz (2003), confirming that growth during the first year of life influences subsequent growth and age at first spawning. Counter-gradient growth is also found in other species, such as silversides (Menidia menidia) (Conover and Present, 1990), little skate (Leucoraja erinacea) (Frisk and Miller, 2006), and in larval stages of blue whiting (Micromesistius poutassou) (Bailey and Heath, 2001). In general, larvae of marine fish species exhibit a latitudinal gradient, populations at higher latitudes growing more slowly (Houde, 1989), a trend that seems to proceed through the juvenile and the adult stages of life, resulting in later age at maturity and increased longevity (Beverton and Holt, 1959; Beverton, 1992). This may explain why it is often found that marine fish including herring may respond to climate change with shifts in distribution (Bainbridge and Forsyth, 1972; Corten, 2001; Rose, 2005; Stenevik and Sundby, 2007).
Similar interannual fluctuations in growth to those observed for juvenile NSS herring in the coastal and fjord nursery areas have also been documented for other areas and stocks, and they might be explained by large-scale climate change. Clearly, temperature fluctuations observed at the monitoring stations along the Norwegian coast were similar to those observed during the autumn surveys in the fjords. The time trend and the peaks of the two temperature datasets also overlap with changes in temperature observed in IMR's environmental sections along the coast and in the Barents Sea (Ottersen and Loeng, 2000; Toresen and Østvedt, 2000; Sætre et al., 2002a), which are related to changes in the North Atlantic oscillation (NAO) index (Hurrell, 1995; Stenseth et al., 2003; Hurrell et al., 2004). Hence, the large-scale changes in Northeast Atlantic waters clearly also influence the environment along the Norwegian coast and fjords as well as in the Barents Sea, influencing growth and recruitment of many species in the area (Stenevik and Sundby, 2007). Correspondingly, periodic peaks in juvenile herring growth along the Norwegian coast were simultaneous with peak growth of juvenile NSS herring (Ottersen and Loeng, 2000) and capelin (Mallotus villosus) in the Barents Sea (Gjøsæter, 1998; Gjøsæter et al., 1998, 2002; Hamre, 2003; Orlova et al., 2005), and they also overlap with peak growth of pre-recruit and adult NSS herring in the Barents Sea and coastal components combined (Holst, 1996; ICES, 2005). Similar and simultaneous fluctuations were also observed in studies on Northeast Atlantic mackerel (Agnalt, 1989; Slotte, 2003; Villamore et al., 2004) and blue whiting (Bailey, 1982) feeding in the Norwegian Sea (Mongstad, 2004). Specifically, it seems that the decline in growth during the 1970s and the peak in the early 1990s followed by another decline is visible in many of the species influenced by Atlantic water masses.
Although temperature appears to have been of major significance for juvenile NSS herring growth along the Norwegian coast, it is clear that population density interfered with this relationship. When combining the effects of temperature and acoustic abundance in the same model, more of the observed variation in juvenile growth was explained, indicating that both factors are important. Hence, the results of the present study agree with the density-dependence hypothesis, that herring growth declines when herring density increases. Support for this is found in numerous other studies, including studies on the growth of 0-group NSS herring in the Barents Sea (Ottersen and Loeng, 2000), studies on the growth and age at maturity of the coastal and Barents Sea components of NSS herring combined (Toresen, 1990; Engelhard and Heino, 2004a, b), and in general, in a wide range of studies on the growth of herring on both sides of the Atlantic (Iles, 1968; Anthony, 1971; Lett and Kohler, 1976; Hubold, 1978; Sinclair et al., 1982; Anthony and Fogarty, 1985; Winters et al., 1986; Winters and Wheeler, 1994; Heath et al., 1997; Shin and Rochet, 1998; Cardinale and Arrhenius, 2000; Cardinale et al., 2002; Axenrot and Hansson, 2003; Casini et al., 2006; Melvin and Stephenson, 2007) and in Pacific herring (Haist and Stocker, 1985; Tanasichuk, 1997). Further, the same is found for species such as capelin (Gjøsæter, 1998), sprat (Sprattus sprattus) (Möllmann et al., 2005), Japanese mackerel (Scomber japonicus) (Watanabe and Yatsu, 2004), and Arctic cod (Gadus morhua) (Ottersen and Loeng, 2000). Few studies have contradicted the density-dependent hypothesis, but there is one example for the Baltic Sea where no significant correlation between weight-at-age and herring abundance was found (Rönkkönen et al., 2004). The possible effect of population density on herring growth in the Baltic Sea has also previously been discussed (e.g. Arrhenius and Hansson, 1993), but the latest results from that area still suggest that growth of both sprat and herring is density-dependent (Cardinale and Arrhenius, 2000; Cardinale et al., 2002; Möllmann et al., 2005; Casini et al., 2006).
Several studies have demonstrated that recruitment of Atlantic herring (Winters et al., 1986; Winters and Wheeler, 1987; Toresen and Østvedt, 2000; Corten, 2001) and Pacific herring (Clupea harengus pallasi) (Anthony and Fogarty, 1985; Stocker et al., 1985) is positively related to temperature. The relationship documented suggests that in years with high temperature there may also be density-dependent growth among juvenile herring, and therefore increased variance in the temperature–growth relationship. However, for juvenile herring along the Norwegian coast, it is a little more complicated. This study has shown that acoustic abundance of juvenile herring in the fjords did not fluctuate in accord with recruitment of the whole stock. Density in the coastal and fjord areas appears to be better related to interannual differences in larval retention and advection into the fjords, in which the location of banks (Sætre, 1999; Sætre et al., 2002b), and wind speed and direction (Sætre et al., 1988; Johannessen et al., 1995; Asplin et al., 1999) play an important role. Hence, there will be years with high advection into the fjords, when year classes may appear very good, whereas they are weak in terms of the total stock, and vice versa. For instance, the 1992 year class, which was one of the largest ever in the total stock, was almost absent from the northern fjords (areas 3–5), whereas the opposite was the case for the 1996 year class.
Another point regarding larval drift of NSS herring, and variable population density along the coast, is that the probability of larvae drifting into coastal areas and fjords in general increases northwards, for three main reasons. First, there are two main routes of drift along the shelf: the main inner route on the coastal side of the banks and a secondary outer route, which follows the shelf break. North of 67°N these two drift routes merge, and the larvae drift close to the coast and fjords. Second, the northern fjords are broader than the southern fjords, which suggest a higher probability of advection into the northern fjords during periods of southerly wind (Asplin et al., 1999). Third, tidal currents increase towards the north, resulting in more exchange of water between fjords and coastal areas (Aure et al., 2007). This may explain why juvenile abundance in the northern fjords can be higher than that in the southern fjords. High temperatures and low population densities in southern fjords appear to be favourable conditions for juvenile herring growth, which may explain why the interannual variations in temperature and abundance in these areas appeared to have less influence on the various growth variables than in the colder areas with greater abundance farther north.
The results of the present study also indicated that the influence of temperature and population density on growth may vary with age of the juveniles. The relative contribution of acoustic abundance on growth was clearly highest among 1-year-olds, indicating that feeding in the second year is more sensitive to the influence of population density than first-year feeding. This seems plausible given that the amount of energy needed for metabolism and growth increases exponentially with size, although the metabolic rate may decrease (Winberg, 1957; Slotte, 1999). However, the effect of acoustic abundance on growth was not so clear among the 2-year-olds. Interannual differences in growth among 2-year-olds must be regarded as uncertain, though, given the fact that at that age, a large fraction of the year class may already have left the fjords to feed outside the fjord systems, where prey is more abundant per individual herring; i.e. the migration is a response to stock density in the fjords and less favourable growth conditions as the fish grows. In fact, looking at how few 1- and 2-year-olds there were in the samples in comparison with the 0-group, it is clear that there might be such a migration out of the fjords. Studies by Devold (1963), Dragesund (1970b), and Røttingen (1990) suggest that 0-group herring mainly utilize the fjords as an overwintering area in the first year of life, and that by the next summer they need to migrate out of the fjord to find sufficient food for growth. However, they stay close to the coast, and the migration may be highly dynamic, and some of them may even migrate back into the fjords after summer feeding for a second and even a third overwintering, before becoming oceanic and mixing with the adults. In general, both the coastal and the Barents Sea components leave the nursery areas and enter the Norwegian Sea 1–2 years before first spawning, at ages 2–8, dependent on growth rate and on average 1–2 years earlier for the coastal component (Lea, 1929a, b; Ottestad, 1934; Runnström, 1936; Holst, 1996).
Given that the feeding of herring usually stops in September (Blaxter and Holliday, 1963; Hay et al., 1988; Slotte, 1999), it is clearly an advantage for 0-group herring to have large energy reserves available before their first winter. Correspondingly, it has been demonstrated that the condition of the 0-group is a major factor that influences first-winter survival (Paul et al., 1998). Here, we demonstrated also that the condition factor of juveniles is inversely related to latitude. This suggests that relatively more will survive to age 1 in the southern areas of the Norwegian coast than in the north. However, it is difficult to track first-winter mortality based on the abundance of the year class the following autumn, because of the dynamic and uncertain migration of 1-year-olds.
What distinguishes the present study from other studies that focus on the effects of temperature and population density on fish growth is the inclusion of the spatial aspect in addition to the temporal one. The synoptic collection of biological parameters of juvenile herring, acoustic abundance, and environmental conditions in nursery areas at various latitudes along the Norwegian coast over a period of 30 years must be regarded as somewhat unique. The results clearly signify that one may experience interference in the relationship between juvenile herring growth and temperature, attributable to variable recruitment, currents, larval drift, and advection into the fjords, causing latitudinal and interannual differences in fish density, and hence in variable competition for food. Similar interferences with temperature-dependent growth should be expected in other fish stocks that distribute their progeny over large areas on a latitudinal range, and where variable currents and advection play an important role in determining the population density within different nursery areas.
|
Acknowledgements |
|---|
This work received financial support from the Research Council of Norway. We thank Georg Engelhard and an anonymous referee for extremely thorough reviews of the manuscript, and for providing really constructive comments on how to improve the final product.
|
References |
|---|
|
TopIntroductionMaterial and methodsResultsDiscussionReferences |
|---|
-
Agnalt A. L. Long-term changes in growth and age at maturity of mackerel, Scomber scomber L, from the North Sea. Journal of Fish Biology (1989) 35:305–311.[ISI]
Anthony V. C. The density-dependence of growth of the Atlantic herring in Maine. Rapports et Procès-Verbaux des Réunions du Conseil International pour l'Exploration de la Mer (1971) 160:196–205.
Anthony V. C., Fogarty M. J. Environmental effects on recruitment, growth, and vulnerability of Atlantic herring (Clupea harengus harengus) in the Gulf of Marine region. Canadian Journal of Fisheries and Aquatic Sciences (1985) 42:158–173.
Arrhenius F., Hansson S. Food consumption of larval, young and adult herring and sprat in the Baltic Sea. Marine Ecology Progress Series (1993) 96:125–137.[ISI]
Asplin L., Salvanes A. G. V., Kristoffersen J. B. Non-local wind driven fjord-coast advection and its potential effect on plankton and fish recruitment. Fisheries Oceanography (1999) 8:255–263.[CrossRef][ISI]
Aure J., Asplin L., Sætre R. Coast/fjord water exchange. In: The Norwegian Coastal Current—Sætre R., ed. (2007) Trondheim, Norway: Tapir Academic Press. 115–125.
Axenrot T., Hansson S. Predicting herring recruitment from young-of-the-year densities, spawning stock biomass, and climate. Limnology and Oceanography (2003) 48:1716–1720.[ISI]
Bailey R. The population biology of blue whiting. Advances in Marine Biology (1982) 19:257–355.[ISI]
Bailey M. C., Heath M. R. Spatial variability in the growth rate of blue whiting (Micromesistius poutassou) larvae at the shelf edge west of the UK. Fisheries Research (2001) 50:73–87.[CrossRef][ISI]
Bainbridge V., Forsyth D. C. T. An ecological survey of a Scottish herring fishery. 5. The plankton of the northwestern North Sea in relation to the physical environment and the distribution of herring. Bulletin of Marine Ecology (1972) 8:21–52.
Beverton R. J. H. Patterns of reproductive strategy parameters in some marine teleost fishes. Journal of Fish Biology (1992) 41((Suppl. B)):137–160.[CrossRef][ISI]
Beverton R. J. H., Holt S. J. A review of the lifespan and mortality rates of fish in nature and their relation to growth and other physiological characteristics. CIBA Foundation Colloquium on Ageing (1959) 5:142–180.
Blaxter J. H. S., Holliday F. G. T. The behaviour and physiology of the herring and other clupeids. Advances in Marine Biology (1963) 1:261–393.
Brophy D., Danilowicz B. S. The influence of pre-recruitment growth on subsequent growth and age at first spawning in Atlantic herring (Clupea harengus L.). ICES Journal of Marine Science (2003) 60:1103–1113.
Cardinale M., Arrhenius F. Decreasing weight-at-age of Atlantic herring (Clupea harengus) from the Baltic Sea between 1986 and 1996: a statistical analysis. ICES Journal of Marine Science (2000) 57:882–893.
Cardinale M., Casini M., Arrhenius F. The influence of biotic and abiotic factors on the growth of sprat (Sprattus sprattus) in the Baltic Sea. Aquatic Living Resources (2002) 15:273–281.[CrossRef][ISI]
Casini M., Cardinale M., Hjelm J. Inter-annual variation in herring, Clupea harengus, and sprat, Sprattus sprattus, condition in the central Baltic Sea: what gives the tune? Oikos (2006) 112:638–650.[CrossRef][ISI]
Conover D. O., Present T. M. C. Counter gradient variation in growth-rate—compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia (1990) 83:316–324.[ISI]
Corten A. Northern distribution of North Sea herring as a response to high water temperatures and/or low food abundance. Fisheries Research (2001) 50:189–204.[CrossRef][ISI]
Devold F. The life history of the Atlanto-Scandian herring. Rapports et Procès-Verbaux des Réunions du Conseil Permanent International pour l'Exploration de la Mer (1963) 154:98–108.
Dragesund O. Factors influencing year-class strength of Norwegian spring spawning herring (Clupea harengus L.). Fiskeridirektoratets Skrifter Serie Havundersøkelser (1970a) 15:381–450.
Dragesund O. Distribution, abundance and mortality of young and adolescent Norwegian spring spawning herring (Clupea harengus L.) in relation to subsequent year-class strength. Fiskeridirektoratets Skrifter Serie Havundersøkelser (1970b) 15:451–556.
Engelhard G. H., Heino M. Maturity changes in Norwegian spring-spawning herring Clupea harengus: compensatory or evolutionary responses? Marine Ecology Progress Series (2004a) 272:245–256.[CrossRef][ISI]
Engelhard G. H., Heino M. Maturity changes in Norwegian spring-spawning herring before, during, and after a major population collapse. Fisheries Research (2004b) 66:299–310.[CrossRef][ISI]
Fiksen Ø., Folkvord A. Modelling growth and ingestion processes in herring Clupea harengus larvae. Marine Ecology Progress Series (1999) 184:273–289.[ISI]
Folkvord A., Johannessen A., Moksness E. Temperature-dependent otolith growth in Norwegian spring-spawning herring (Clupea harengus L.) larvae. Sarsia (2004) 89:297–310.[CrossRef][ISI]
Fossum P., Moksness E. Recruitment processes of the 1991 year-class of Norwegian spring-spawning herring (Clupea harengus L.) determined from otolith microstructure examination. In: Recent Developments in Fish Otolith Research—Secor D. H., Dean J. M., Campana S. E., The Belle W., eds. (1995) University of South Carolina Press. 467–479. 19 Baruch Library in Marine Science.
Frisk M. G., Miller T. J. Age, growth, and latitudinal patterns of two Rajidae species in the north-western Atlantic: little skate (Leucoraja erinacea) and winter skate (Leucoraja ocellata). Canadian Journal of Fisheries and Aquatic Sciences (2006) 63:1078–1091.
Gjøsæter H. The population biology and exploitation of capelin (Mallotus villosus) in the Barents Sea. Sarsia (1998) 83:453–513.[ISI]
Gjøsæter H., Dalpadado P., Hassel A. Growth of Barents Sea capelin (Mallotus villosus) in relation to zooplankton abundance. ICES Journal of Marine Science (2002) 59:959–967.
Gjøsæter H., Dommasnes A., Røttingen B. The Barents Sea capelin stock 1972–1997. A synthesis of results from acoustic surveys. Sarsia (1998) 83:497–510.[ISI]
Haist V., Stocker M. Growth and maturation of pacific herring (Clupea harengus pallasi) in the Strait of Georgia. Canadian Journal of Fisheries and Aquatic Sciences (1985) 42:138–146.
Hamre J. Capelin and herring as key species for the yield of north-east Arctic cod. Results from multispecies model runs. Scientia Marina (2003) 67:315–323.[ISI]
Hay D. E., Brett J. R., Bilinski E., Smith D. T., Donaldson E. M., Hunter G. A., Solmie A. V. Experimental impoundments of prespawning pacific herring (Clupea pallasi)—effects of feeding and density on maturation, growth and proximate analysis. Canadian Journal of Fisheries and Aquatic Sciences (1988) 45:388–398.
Heath M., Scott B., Bryant A. D. Modelling the growth of herring from four different stocks in the North Sea. Journal of Sea Research (1997) 38:413–436.[CrossRef]
Hjort J. Fluctuations in the great fisheries of Northern Europe. Rapports et Procès-Verbaux des Réunions du Conseil Permanent International pour l'Exploration de la Mer (1914) 20:228.
Holst J. C. Long term trends in the growth and recruitment pattern of the Norwegian spring-spawning herring (Clupea harengus Linnaeus 1758). (1996) Norway: University of Bergen.
Holst J. C., Slotte A. Effects of juvenile nursery on geographic spawning distribution in Norwegian spring spawning herring (Clupea harengus L.). ICES Journal of Marine Science (1998) 55:987–996.
Houde E. D. Comparative growth, mortality and energetics of marine fish larvae: temperature and implied latitudinal effects. Fishery Bulletin US (1989) 87:471–495.
Hubold G. Variations in growth rate and maturity of herring in the northern North Sea in the years 1955–1973. Rapports et Procès-Verbaux des Réunions du Conseil International pour l'Exploration de la Mer (1978) 172:154–163.
Hurrell J. W. Decadal trends n the North Atlantic oscillation—regional temperatures and precipitation. Science (1995) 269:676–679.
Hurrell J. W., Hoerling M. P., Phillips A. S., Xu T. Twentieth century north Atlantic climate change. 1. Assessing determinism. Climate Dynamics (2004) 23:371–389.
ICES. (2005) 290. Report of the Northern Pelagic and Blue Whiting Fisheries Working Group. ICES Document CM/ACFM: 05.
Iles T. D. Growth studies on North Sea herring. 2. 0-group growth of East Anglian herring. Journal du Conseil Permanent International pour l'Exploration de la Mer (1968) 32:98.
Johannessen A., Slotte A., Bergstad O. A., Dragesund O., Røttingen I. Reappearance of Norwegian spring spawning herring (Clupea harengus L.) at spawning grounds off southwestern Norway. In. In: Ecology of Fjords and Coastal Waters. Proceedings of the Mare Nor Symposium on the Ecology of Fjords and Coastal Waters—Skjoldal H. R., Hopkins C., Erikstad K. E., Leinaas H. P., eds. (1995) Amsterdam: Elsevier. 347–364.
Lea E. The herring scale as a certificate of origin, its applicability to race investigations. Rapports et Procès-Verbaux des Réunions du Conseil Permanent International pour l'Exploration de la Mer (1929a) 54:21–36.
Lea E. The oceanic stage in the life history of Norwegian herring. Journal du Conseil Permanent International pour l'Exploration de la Mer (1929b) 4:3–42.
Lett P. F., Kohler A. C. Recruitment: a problem of multispecies interaction and environmental factors, spawning stock size and recruitment for Georges Bank area. Journal of the Fisheries Research Board of Canada (1976) 33:1353–1371.[ISI]
Möllmann C., Kornilovs G., Fetter M., Koster F. W. Climate, zooplankton, and pelagic fish growth in the central Baltic Sea. ICES Journal of Marine Science (2005) 62:1270–1280.
Melvin G. D., Stephenson R. L. The dynamics of a recovering fish stock: Georges Bank herring. ICES Journal of Marine Science (2007) 64:69–82.
Mongstad T. Blue whiting. In: The Norwegian Sea Ecosystem—Skjoldal H. R., Sætre R., Fernö A., Misund O. A., Røttingen I., eds. (2004) Trondheim, Norway: Tapir Academic Press. 263–288.
Morse W. W. Catchability, growth and mortality of larval fishes. Fishery Bulletin US (1989) 87:417–446.
Orlova E. L., Boitsov V. D., Dolgov A. V., Rudneva G. B., Nesterova V. N. The relationship between plankton, capelin, and cod under different temperature conditions. ICES Journal of Marine Science (2005) 62:1281–1292.
Ottestad P. Statistical analyses of the Norwegian herring population. Rapports et Procès-Verbaux des Réunions du Conseil Permanent International pour l'Exploration de la Mer (1934) 88:1–45.
Ottersen G., Loeng H. Covariability in early growth and year-class strength of Barents Sea cod, haddock, and herring: the environmental link. ICES Journal of Marine Science (2000) 57:339–348.
Paul A. J., Paul J. M., Brown E. D. Fall and spring somatic energy content for Alaskan Pacific herring (Clupea pallasi Valenciennes 1847) relative to age, size and sex. Journal of Experimental Marine Biology and Ecology (1998) 223:133–142.[CrossRef][ISI]
Rose G. A. On distributional responses of North Atlantic fish to climate change. ICES Journal of Marine Science (2005) 62:1360–1374.
Runnström S. A study on the life history and migrations of the Norwegian spring herring based on analysis of the winter rings and summer zones of the scale. Fiskeridirektoratet Skrifter Serie Havundersøkelser (1936) 5:1–110.
Rönkkönen S., Ojaveer E., Raid T., Viitasalo M. Long-term changes in Baltic herring (Clupea harengus membras) growth in the Gulf of Finland. Canadian Journal of Fisheries and Aquatic Sciences (2004) 61:219–229.
Røttingen I. The 1983 year class of Norwegian spring spawning herring as juveniles and recruit spawners. Mongstad T., ed. (1990) 6. Proceedings of the 4th Soviet–Norwegian Symposium, 12–16. Bergen, Norway: Institute of Marine Research. 165–203. 1989.
Sætre R. Features of the central Norwegian shelf circulation. Continental Shelf Research (1999) 19:1809–1831.[CrossRef][ISI]
Sætre R., Aure J., Ljoeen R. Wind effects on the lateral extension of the Norwegian costal water. Continental Shelf Research (1988) 8:239–253.[CrossRef][ISI]
Sætre R., Toresen R., Anker-Nilssen T. Factors affecting the recruitment variability of the Norwegian spring-spawning herring (Clupea harengus L.). ICES Journal of Marine Science (2002a) 59:725–736.
Sætre R., Toresen R., Søiland H., Fossum P. The Norwegian spring spawning herring—spawning, larval drift and larval retention. Sarsia (2002b) 87:167–178.[CrossRef][ISI]
SAS Institute. SAS User's Guide: Statistics, version 9.1. (2005) Cary, NC: SAS Institute.
Shin Y. J., Rochet M-J. A model for the phenotypic plasticity of North Sea herring growth in relation to trophic conditions. Aquatic Living Resources (1998) 11:315–324.[CrossRef][ISI]
Sinclair M., Sinclair A., Iles T. D. Growth and maturation of southwest Nova Scotia Atlantic herring (Clupea harengus harengus). Canadian Journal of Fisheries and Aquatic Sciences (1982) 39:288–295.
Slotte A. Effects of fish length and condition on spawning migration in Norwegian spring spawning herring (Clupea harengus L.). Sarsia (1999) 84:111–127.[ISI]
Slotte A. Historic changes in the condition of NEA mackerel—possible effects on fecundity. (2003) 16. Working document prepared for the ICES Working Group on Mackerel, Horse Mackerel, Sardine and Anchovy.
Slotte A., Fiksen Ø. State-dependent spawning migration in Norwegian spring spawning herring (Clupea harengus L.). Journal of Fish Biology (2000) 56:138–162.[CrossRef][ISI]
StatSoft Inc. Electronic Statistics Textbook. (2006) Tulsa, OK: StatSoft. http://www.statsoft.com/textbook/stathome.html.
Stenevik E. K., Fossum P., Johannessen A., Folkvord A. Identification of larvae of Norwegian spring spawning herring (Clupea harengus L.) from spawning grounds off south-western Norway applying otolith microstructure analysis. Sarsia (1996) 80:285–292.[ISI]
Stenevik E. K., Sundby S. Impacts of climate change on commercial fish stocks in Norwegian waters. Marine Policy (2007) 31:19–31.[CrossRef][ISI]
Stenseth N. C., Ottersen G., Hurrell J. W., Mysterud A., Lima M., Chan K. S., Yoccoz N. G., et al. Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. (2003) 270. Proceedings of the Royal Society of London Series B – Biological Sciences. 2087–2096.
Stocker M., Haist V., Fournier D. Environmental variation and recruitment of Pacific herring (Clupea harengus pallasi) in the Strait of Georgia. Canadian Journal of Fisheries and Aquatic Sciences (1985) 42:174–180.
Tanasichuk R. W. Influence of biomass and ocean climate on the growth of Pacific herring (Clupea pallasi) from the southwest coast of Vancouver Island. Canadian Journal of Fisheries and Aquatic Sciences (1997) 54:2782–2788.
Toresen R. Long-term changes in growth of Norwegian spring-spawning herring. ICES Journal of Marine Science (1990) 47:48–56.
Toresen R., Østvedt O. J. Variation in abundance of Norwegian spring spawing herring (Clupea harengus, Clupeidae) throughout the 20th century and the influence of climatic fluctuations. Fish and Fisheries (2000) 1:231–256.[CrossRef]
Villamor B., Abaunza P., Farina A. C. Growth variability of mackerel (Scomber scombrus) off north and northwest Spain and a comparative review of the growth patterns in the northeast Atlantic. Fisheries Research (2004) 69:107–121.[CrossRef][ISI]
Watanabe C., Yatsu A. Effects of density-dependence and sea surface temperature on interannual variation in length-at-age of chub mackerel (Scomber japonicus) in the Kuroshio–Oyashio area during 1970–1997. Fishery Bulletin US (2004) 102:196–206.
Winberg G. G. Rate of metabolism and food requirements of fishes. Fisheries Research Board of Canada Translation Series (1957) 194.
Winters G. H., Wheeler J. P. Recruitment dynamics of spring-spawning herring in the northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences (1987) 44:882–900.
Winters G. H., Wheeler J. P. Length-specific weight as a measure of growth success of adult Atlantic herring (Clupea harengus). Canadian Journal of Fisheries and Aquatic Sciences (1994) 51:1169–1179.
Winters G. H., Wheeler J. P., Dalley E. L. Survival of a herring stock subjected to a catastrophic event and fluctuating environmental conditions. Journal du Conseil International pour l'Exploration de la Mer (1986) 43:26–42.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||