Effects of juvenile nursery on geographic spawning distribution in Norwegian spring-spawning herring (Clupea harengus L.)

ICES Journal of Marine Science, 55: 987 996. 1998 Article No. jm980371 Effects of juvenile nursery on geographic spawning distribution in Norwegian spring-spawning herring (Clupea harengus L.) J. C. Holst and A. Slotte Holst, J. C., and Slotte, A. 1998. Effects of juvenile nursery on geographic spawning distribution in Norwegian spring-spawning herring (Clupea harengus L.). ICES Journal of Marine Science, 55: 987 996. The Norwegian spring-spawning herring is characterized by a heterogeneous growth pattern originating from nurseries situated along the Norwegian coast and in the Barents Sea. Using a classification algorithm based on measurements of the three first scale annuli, the geographic, temporal, and age dependent recruitment patterns of the coastal and Barents Sea components of most year classes from 1930 to 1989 were studied. The relative importance of each component in the year classes varied with the fluctuating stock size observed during the period studied. In periods with a low spawning stock almost no recruitment appeared from the Barents Sea juvenile areas, while at high stock levels the Barents Sea component totally dominated the spawning stock. The asynchronous maturation of the two components caused a recruitment pattern characterized by a high proportion of the coastal component at younger ages and an increasing proportion of the Barents Sea component at older ages. Both components recruited along the entire spawning range studied, and once fully recruited, no latitudinal gradient in the spawning stock component composition was observed. 1998 International Council for the Exploration of the Sea Key words: Norwegian spring-spawning herring, recruitment, migration, growth, spawning, stock component. Received 23 November 1995; accepted 26 April 1998. J. C. Holst and A. Slotte: Institute of Marine Research, PO Box 1870, 5024 Bergen, Norway. Correspondence to J. C. Holst: tel: +47 5523 8411; fax: +47 5523 8687; email: jensh@imr.no Introduction The Norwegian spring-spawning herring is a highly migratory stock and through its lifespan individual fish may cover large parts of the north-eastern Atlantic (Devold, 1963; Dragesund et al., 1980; Hamre, 1990). During the last 60 years the herring stock has been characterized by extreme variations in stock abundance and migration pattern. During this period the migration pattern changed from oceanic to coastal and back to oceanic (Hamre, 1990; Anon., 1994), and the spawning stock fell from an estimated 10 million tonnes in the 1940s to near extinction in the early 1970s (Dragesund et al., 1980). Since then the spawning stock has recovered slowly and may have reached 9 million tonnes by 1997 (Anon., 1997). The spawning takes place in February to March along the Norwegian west coast, and at large stock sizes spawning may occur from about 58 N to69 N (Fig. 1). The larvae drift north-eastward and enter the fjords along the Norwegian coast and the Barents Sea. The 0-group of large year classes is found from about 59 N to75 N in August to September and is distributed in both the temperate and arctic zone. It has been observed that the juveniles of abundant year classes are associated both with the Barents Sea and the Norwegian west coast, while the young of smaller year classes are mainly distributed in the coastal area (Dragesund et al., 1980). The large range of temperature and ecological regimes experienced by the juveniles is reflected in differences in growth patterns throughout their geographic range. As a rule, the growth rate decreases northwards, and consequently the herring originating from the coastal nurseries grow quicker and mature at a lower age than the herring originating from the Barents Sea. This was realised by Lea (1929a,b) who discriminated between herring of northern and southern origin using the growth checks deposited in the herring scale. While Lea s method was based on a visual evaluation of the growth pattern in the scales, a recent study by Barros and Holst (1995) presented a statistical 1054 3139/98/060987+10 $30/0 1998 International Council for the Exploration of the Sea

988 J. C. Holst and A. Slotte Figure 1. Areas defined for latitudinal separation of the spawning grounds (,,, A4). Arrows indicate drift of larvae and hatched areas indicate juvenile distribution in autumn. Dashed line separates the nursery area of the coastal component and the Barents Sea component as defined by Barros and Holst (1995). technique using the measurements of the yearly growth zones in the herring scale to discriminate between herring of Norwegian west coast and Barents Sea origin. It should be noted that as when Lea (1929a,b) described a northern and southern growth type, the nomenclature of Barros and Holst (1995) is used; the Barents Sea component and the coastal component. In the present study three hypotheses are explored regarding the effect of juvenile nursery on geographic spawning distribution, covering the year classes 1930 1989. First, that the changes in stock size systematically affect the recruitment pattern of the two defined components in the Norwegian spring-spawning herring stock. Second, that the asynchronous maturity schedule of the two components results in different recruiting patterns of the components. Third, that the juvenile area is a factor determining the geographic spawning distribution of fully recruited components. Finally, the results are discussed with respect to the understanding of the population dynamics of this stock and the significance of the results to fishery management. Materials and methods This study is based on samples of Norwegian springspawning herring collected by the Institute of Marine Research (IMR), Bergen, Norway, from 1935 to 1994. Samples of up to 200 herring were collected from drift-net, beach-seine, purse-seine, and trawl catches, caught by commercial and research vessels. Individual fish were weighed, total length measured and parameters such as sex, maturity stage, relative contents of intestinal fat etc. recorded. Biological measurements of 54 858 herring were included in the analysis. Up to four scales per specimen were collected from the skin posterior to opercullum and mounted on glass plates with a gelatine coat. Using a stereomicroscope fitted with an ocular

Geographic spawning distribution in Clupea harengus 989 micrometer, the age was determined and each annuli and total scale diameter measured. The nursery area of origin (Coastal or Barents Sea) of the individual fish was estimated using the procedure described by Barros and Holst (1995). Based on measurements of the first three annuli the procedure discriminates between individuals originating from the Barents Sea nurseries and the coastal nurseries. The probability of an individual fish originating from the Barents Sea is estimated and a p-value (Probability of Barents Sea origin) is estimated for each individual. Fish of estimated coastal origin will be assigned p-values <, while fish of Barents Sea origin will be assigned values >. The closer the estimated p-value is either to 0 or 1 the more certain is the estimated origin, and fishes characterized by p-values close to have the most uncertain origin. This uncertainty could be reduced by excluding all individuals characterized by p> and p<. However, running the analysis with such exclusion resulted in a lower mean number of fish per group and the removal of some groups due to the minimum number of individuals (n>10) set for including a group in the analysis. Often such removal of groups affected the youngest ages due to their low representation in the spawning stock. On the other hand, no significant changes in the overall classification results were observed. Consequently, it was decided to include all fish in the analysis as this gave a significantly better description of the recruiting pattern of the young and, in this context, important fish. To ascertain that the catch positions corresponded to the spawning area of the fish, only fish in the maturity stages close to spawning (4, 5) or spawning (6) were used in the analysis. The herring spawning area from approximately 58 N to67 N was sectioned in four subareas;,,, A4 (Fig. 1). The latitudinal range covered by the four areas was approximately 1200 km and the majority of known spawning grounds were included. The component composition of the individual year class when recruited was estimated as the mean proportion of the Barents Sea component at age 6 10 over all sampled areas: where N=number in samples, =6 10 and Area= A4. The smoothed long-term trend of the proportion of the Barents Sea component in the spawning stock was plotted using the SAS spline smoothing function (INTERPOL=SM), with the KnnL parameter set at 35 (Reinsch, 1967; SAS, 1990). To study effects of the asynchronous recruitment of the two components to the spawning stock component composition by age and area, and effects of the juvenile nursery on geographic spawning distribution, the studied year classes were pooled in six blocks: 1930 1939, 1940 1949, 1950 1959, 1960 1969, 1970 1979, and finally 1980 1989 (excluding 1983). The 1983 year class was treated separately due to its large size and characteristic recruitment pattern in that block. The proportion of Barents Sea component by block, age, and area was estimated as the proportion of the sampled individuals classified as belonging to the Barents Sea component, equivalent to the equation in the last section. The proportion of the Barents Sea component in the spawning stock is given in graphs by age for the blocks of year classes, and by age and area for each block of year classes separately. Results The component composition of the individual year class varied during the studied period (Fig. 2). All year classes hatched prior to the 1970 year class were dominated by the Barents Sea component, while there was a major shift with the 1971 year class as the proportion of the Barents Sea component dropped drastically from a level at about to about. This trend continued further into the 1970s and the year classes 1974 1976 all had a Barents Sea proportion at or below. The drop in the relative importance of the Barents Sea component coincided with an extremely low spawning stock level (Fig. 2). The importance of the Barents Sea component was low in most year classes hatched during the 1970s, but its importance increased in the last year classes of that decade. The proportion of the Barents Sea component increased further into the 1980s and the 1983 year class was the first year class hatched after the stock collapse which was totally dominated by the Barents Sea component. Later, year classes did not exhibit such Barents Sea component dominance and the proportion of the Barents Sea component appears to have stabilized at some intermediate level in the year classes hatched during the late 1980s. The mean proportion of the Barents Sea component in the spawning stock increased with age during the recruitment period (age 3 6) in all decades studied (Fig. 3). The component composition then stabilized at some level varying between the decades. The highest level of Barents Sea component was observed in the year classes hatched during the 1930s, while the lowest level occurred in the year classes hatched during the 1970s. The 1980s year classes (excluding 1983) showed an intermediate trend, while the 1940s, 1950s, and 1969s year classes exhibited a relatively high level. By including the 1983 year class in the 1980s block, the 1980 block appears very much like the 1983 year class due to the dominating size of that year class. During the period of recruitment (age 3 6), the component composition varied over the geographic

990 J. C. Holst and A. Slotte 15 Proportion 14 13 12 11 10 9 8 Spawning stock 7 6 5 4 3 2 1 30 42 90 32 34 36 40 44 46 48 50 0 38 52 54 56 58 60 62 64 66 68 70 72 74 76 78 80 82 84 86 88 Year class/year Figure 2. Left axis and dots: estimated mean proportion Barents Sea component in the investigated year classes (missing value indicates to few observations to estimate composition). Thick line: smoothed proportion. Right axis and thin line: estimated spawning stock biomass by year (from Anon. 1997). Spawning stock biomass (tonnes 10 6 ) 1930 1950 1940 1960 1970 1980 Figure 3. Estimated mean proportion of the Barents Sea component by age and blocks of year classes. spawning range. The proportion of the Barents Sea component at age 4 was higher in the northernmost area () than in the more southern areas (,, A4) during the 1930s, the 1960s, and the 1980s including the 1983 year class (Figs 4 10). During the 1970s, however, the Barents Sea component proportion was somewhat larger in than in at age 4. The same trend was also observed at age 5, while at age 6 and higher ages no specific geographic trend in the geographic component composition was observed. At this age, when most individuals had recruited, the component composition appears to be stabilized at about the same level in all areas, but varying between the decades. Discussion The heterogeneous growth structure of the Norwegian spring-spawning herring stock was subject to investigation

Geographic spawning distribution in Clupea harengus 991 A4 1930 1939 Figure 4. Estimated mean proportion of the Barents Sea component by age and area in the year classes 1930 1939. A4 1940 1949 Figure 5. Estimated mean proportion of the Barents Sea component by age and area in the year classes 1940 1949. early in this century (Lea, 1929a,b; Ottestad, 1934; Runnstrøm, 1936) and the existence of two separate subunits or races was discussed. Later it was concluded that the Norwegian spring-spawning herring stock is a single stock unit and the two distinctive growth patterns originate from northern and southern nurseries (Østvedt, 1958; Anon., 1963; Dragesund et al., 1980). In the present study the authors have explored three hypotheses regarding the effect of juvenile nursery on geographic spawning distribution, covering the year classes 1930 1989. The authors have followed the definition of components in the Norwegian spring-spawning herring as defined by Barros and Holst (1995), i.e. two different growth patterns are discernible in the herring stock and these are related to juvenile areas situated within two major ecological systems; the Norwegian coast (59 N 70 N) and the Barents Sea including the Norwegian coast north of 70 N (Fig. 1). Barros and Holst (1995) used the growth pattern of several year classes to estimate their discrimination rule, which in strict terms means that the rule is made for some year class representing some mean growth pattern. It should therefore be noticed that for year classes of extraordinary high growth, the discrimination rule may

992 J. C. Holst and A. Slotte A4 1950 1959 Figure 6. Estimated mean proportion of the Barents Sea component by age and area in the year classes 1950 1959. 1960 1969 Figure 7. Estimated mean proportion of the Barents Sea component by age and area in the year classes 1960 1969. overestimate the coastal component, while the opposite will happen to year classes characterized by low growth. This effect could be compensated for by excluding the fish of most uncertain geographic origin (for instance fish characterized by p> and p<). However, as pointed out in the method section such exclusion hardly changed the results of the analysis, but left out important parts of the data, in particular affecting the younger ages. The first hypothesis, suggesting that the changes in stock size affect the recruiting pattern of the two components, was supported by the data. The switch from the dominance of the Barents Sea component to dominance of the coastal component in the spawning stock around 1970 coincided with the collapse in the spawning stock in the same period. After the stock collapse in the late 1960s the spawning stock remained at a relatively low level during the 1970s and the early 1980s (Hamre, 1990; Anon., 1994). From 1973 to 1983 the 0-group abundance index in the Barents Sea was 0 in 50% of the years and very low the others with a log index below (Anon., 1994). During the same period 0-group herring was observed in the coastal areas in all years (Anon., 1994). It appears that below a certain spawning stock

Geographic spawning distribution in Clupea harengus 993 1970 1979 Figure 8. Estimated mean proportion of the Barents Sea component by age and area in the year classes 1970 1979. A4 1980 1989 (excluding 1983) 3 4 5 6 7 8 9 Figure 9. Estimated mean proportion of the Barents Sea component by age and area in the year classes 1980 1989. Excluding the 1983 year class. 10 size the recruitment potential from the Barents Sea nurseries decrease strongly as compared to the coastal nurseries. The causal mechanisms underlying the establishment of the relative strength between the coastal and the Barents Sea component in the individual year class must be regarded a complex process involving factors such as spawning stock size, geographic spawning distribution, oceanographic conditions, growth, and both natural and fishing mortality. These mechanisms are so far not very well understood and should be addressed in future studies. The component switch around 1970 may also have been affected by the closing of the young herring fishery in the same period. This fishery exploited both the nurseries of the Barents Sea and coastal component (Dragesund, 1970; Dragesund et al., 1980), but from the figures given by Dragesund (1970) it appears that the fishery exploited the young herring in the nurseries of the coastal component relatively harder than those in the Barents Sea component nurseries (figures given for the 1959 1964 year classes). The closing of the young herring fishery following the stock collapse may

994 J. C. Holst and A. Slotte A4 1983 Year class Figure 10. Estimated mean proportion of the Barents Sea component in the spawning stock by age and area in the 1983 year class. consequently have resulted in increased survival in the coastal nurseries as compared to the Barents Sea nurseries, which again may have increased the proportion of the coastal component in the spawning stock. Conditional on the young herring fishery not being reopened in the future, the authors hypothesize that the coastal component will constitute a larger mean proportion of the spawning stock in the future as compared to the pre-collapse period, in particular in small year classes. The second hypothesis, suggesting that the asynchronous maturity schedule of the two components results in different recruiting patterns, was also supported by the data. Herring originating from the southern nurseries exhibit a faster growth than those from the northern nurseries (Dragesund et al., 1980; Toresen, 1990; Holst, 1996) and thus mature at a lower age (Toresen, 1990). The observed increase in the proportion of the Barents Sea component in the spawning stock during the age of recruitment in most periods studied is ascribed to this asynchronous maturation schedule of the two components. The effect of the asynchronous maturity schedule on the recruitment pattern was particularly pronounced in the 1983 year class. At age 3, only the coastal component had started recruiting to the spawning stock and a small portion spawned at Møre (area ) (Røttingen, 1990; Seliverstova, 1990). At age 4, a minor portion of the Barents Sea component matured and dominated at the northernmost spawning grounds studied (), whereas it comprised only about 65% of the spawners at Møre (). At age 5 the Barents Sea component had fully recruited to the spawning stock and dominated at all spawning grounds with a mean composition of about 99%. The mode of recruitment of the 1983 year class resembles several year classes between 1930 and 1960 and is suggested as typical for large year classes characterized by a large proportion of the Barents Sea component. Whilst the component composition appeared to stabilize within each spawning area after the age of full recruitment in most decades, this appeared not to be the case during the 1980s. For instance, in area the proportion of the Barents Sea component continued to grow up to age 10, about 5 years after full recruitment. The only possible explanation to this phenomena is that the mortality was different in the two components during this period. The fishing pressure was rather high during a period in the latter half of the 1980s (Anon., 1997) and it is proposed that the Fs (fishing mortality) exerted on the coastal component was larger than that exerted on the Barents Sea component. Such a differential mortality is consistent with the fishing practices of the purse-seine fleet, which will try to optimize its profit by catching the larger and better priced herring (Slotte and Johannessen, 1997a). The increase in the proportion of the Barents Sea component levelled off and stabilized at age 5 or 6 during most periods studied. However, it levelled off at 4 5 years during the 1970s. The earlier stabilizing during this period is consistent with a lower mean age at maturity of these year classes (Toresen, 1990). The third hypothesis, suggesting that the juvenile area is a factor determining the geographic spawning distribution of fully recruited components, was not supported by the data. The only pronounced latitudinal gradient in the component composition over the studied spawning grounds was observed during the recruitment period

Geographic spawning distribution in Clupea harengus 995 (age 3 6) between the northernmost area () and the more southern areas (,, A4). The authors are not able to interpret these results in terms of absolute abundance of recruiting herring of either component within the studied areas, but most likely the recruitment of the Barents Sea component is strongest into the northern spawning areas at the younger ages, while at older ages the recruitment increases into the more southern areas. In a recent study on the spawning behaviour of the Norwegian spring-spawning herring (Slotte and Johannessen, 1997b) it was shown that recruit spawners which wintered in the Ofotfjord/Tysfjord/Vestfjord area during the early 1990s and consisted mainly of the Barents Sea component, had a somewhat delayed maturation schedule as compared to the older spawners. The southerly spawning migration of these first time spawners are relatively short, and consequently they had a relatively northerly spawning distribution. As second year spawners the maturity schedule appeared better coordinated with the older spawners, and the southerly spawning migration distance increased. These observations are consistent with the observed age dependent latitudinal recruitment gradient of the Barents Sea component and is suggestive of a causal mechanism related to the energetics of migration and maturity schedule of the Barents Sea component first time spawners. The age dependent weakening of the latitudinal gradient in component composition may also be affected by exchange of non-first-time spawners between spawning grounds, a phenomenon described in this and other herring stocks (Wheeler and Winters, 1984; Holst, 1991). The authors expect that dynamic processes connected to the recruitment of juveniles originating from different juvenile areas occur both in other herring stocks and other fish species. Due to the long time series available and the wide geographic range of the spawning grounds of the Norwegian spring-spawned herring, the present system may serve as an example of some of the fascinating processes occurring in connection with the recruitment in herring. It is believed that in many cases these structures are difficult or even impossible to observe and describe due to the small scale on which they occur or simply due to the lack of appropriate data sets. The present study has demonstrated the importance of the Barents Sea component to high catch levels in the fisheries. It has also demonstrated the importance of the coastal component as a buffer at low stock levels and a contributor to new recruitment in such periods. Consequently, it is of importance for the management of this stock to secure recruitment both into the Barents Sea nursery and all the potential nurseries along the coast. The authors are of the opinion that this goal can best be achieved by the following general measures. First, secure a spawning stock which is sufficiently large to produce year classes that enter the Barents Sea. Second, allow for a maximum geographic extent of the spawning area. This second goal will in some cases imply the closing or reduced fishing effort in marginal spawning grounds. The present management regime includes such regulations (Ingolf Røttingen, IMR, pers. comm.). Acknowledgements The work of Jens Christian Holst and Aril Slotte was supported by the Norwegian Research Council. The authors wish to thank Sigmund Myklevoll for drawing the map. References Anon. 1963. ICES herring Committee, Doc. No. 70, Appendix 1. Anon. 1994. Report of the Atlanto-Scandian herring and Capelin working group. 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