Differentiation in juvenile growth and bimodality patterns between northern and southern populations of Atlantic salmon (Salmo salar L.)

ALFREDO G. NICIEZA, FELIPE G. REYES-GAVILAN, AND FLORENTINO BRANA Departamento de Biologia de Organismos y Sistemas, Universidad de Oviedo, 33071 Oviedo, Spain

Received November 19, 1993 Accepted June 22, 1994

NICIEZA, A.G., REYES-GAVILAN, F.G., and BRANA, F. 1994. Differentiation in juvenile growth and bimodality patterns between northern and southern populations of Atlantic salmon (Salmo salar L. ) Can. J. Zool. 72: 1603- 1610.

Juvenile Atlantic salmon, Salmo salar, from two contrasting populations that had been reared under identical conditions differed in freshwater growth rates and the development of bimodality in length-frequency distributions. Segregation by size started at least a month earlier in the northern (River Shin, northern Scotland) than in the southern population (River Narcea, northern Spain). Northern fish initially grew faster and entered the upper modal group at a larger size (about 100 mm) than did southern fish (about 90 mm). However, the percentage of fish in the upper modal group was greater for the southern population and they grew fastest over winter and during the spring leading up to smolting, and were larger at the smolt stage. By late winter, the individual growth rates of upper modal fish were inversely correlated with their body length in December. These results suggest the existence of genetic differences between populations in the expression of growth bimodality in juvenile Atlantic salmon. This may indicate that size and growth rate thresholds determining the developmental pathway associated with age at smolt metamorphosis may vary between populations as a function of both smolt size and expected growth opportunity during winter and spring.

NICIEZA, A.G., REYES-GAVILAN, F.G., et BRANA, F. 1994. Differentiation in juvenile growth and bimodality patterns between northern and southern populations of Atlantic salmon (Salmo salar L.) Can. J. Zool. 72 : 1603 - 16 10.

De jeunes Saumons atlantiques (Salmo salar) provenant de deux populations trks diffkrentes ClevCes dans des conditions identiques avaient des taux de croissance diffkrents en eau douce et la bimodalit6 de leur distribution longueur-frCquence ne suivait pas la meme tenda'nce. La sCgrCgation en fonction de la taille est apparue au moins 1 mois plus t6t chez la population du nord (rivikre Shin, nord de 1'Ecosse) que chez celle du sud (rivikre Narcea, nord de 1'Espagne). La croissance des poissons nordiques Ctait plus rapide au dCpart et ces poissons atteignaient le stade du groupe modal supCrieur a une taille plus ClevCe (environ 100 mm) que les poissons plus austraux (environ 90 mm). Cependant, le pourcentage de poissons dans le groupe modal supCrieur Ctait plus important chez la population du sud et ces poissons avaient une croissance plus rapide durant l'hiver et au printemps prCcCdant la transformation en saumoneau; les saumonneaux de cette population Ctaient Cgalement plus gros. A la fin de l'hiver, les taux individuels de croissance des poissons du mode supCrieur Ctaient en corrClation nCgative avec leur longueur totale en dCcembre. Ces rCsultats indiquent l'existence de diffkrences gCnCtiques entre les populations quant B I'expression de la bimodalit6 de croissance chez les jeunes Saumons atlantiques. Ce phknomkne est peut-etre attribuable au fait que les seuils de taille et taux de croissance qui dCterminent le dCveloppement associC a 1'2ge au moment de la mktamorphose en saumonneau varient, d'une population a l'autre, en fonction de la taille des saumonneaux et des probabilitks de croissance en hiver et au printemps.

[Traduit par la RCdaction]

Introduction One of the main goals of life-history theory is to distinguish

between the genetic and environmental sources of geographic variation in life-history traits. Growth rates of poikilotherms in particular are highly sensitive to changes in physical factors such as temperature or food availability, therefore environ- mental variation may influence life-history variation both through phenotypic plasticity and as a source of genotypic selection (Berven and Gill 1983; Sinervo and Adolph 1989; Conover 1990; Conover and Present 1990; Niewiarovski and Roosenburg 1993). The Atlantic salmon (Salmo salar L.) is a widely distributed species with extensive population sub- division that shows considerable variation in life-history traits.

practically cease feeding throughout autumn and winter. This reduction of feeding activity in LMG fish is thought to be a way to reduce the over-winter mortality of the less competi- tive individuals (Metcalfe et al. 1988; Metcalfe and Thorpe 1992).

The smolting process seems to be a set of adaptations that render possible the shift between two habitats with contrasting ecological and physiological requirements. Therefore, as in other poikilotherms that undergo true metamorphosis, the patterns of growth and development determining the timing of smolting in salmonids are likely to have been under strong selection. The ecological significance of size bimodality, how- ever. is not fullv understood. Because both small and late

In some southern rivers, or under relatively favourable labo- migiants have doorer survival to adulthood than larger or ratory conditions, the underyearling salmon exhibit a two-way earlier smelts ( Bilton et al. 982; Feltham 990; Berglund developmental strategy that leads to the formation of bimodal et al. 1992), growth bimodality might result from a mecha- length-frequency distributions at the end of the first growing season. This pattern is linked to the timing of "metamorpho- nism that prevents fish smoltifying below an appropriate size

sis,, and subsequent migration: fish in the upper (or reaching that size after the critical period for migration)

modal group (UMG) often show an increase in their growth or from the trade-off between growth and risk of predation

rates after attaining a threshold size in autumn or early winter when the temperature drops below a given level. In this

(Kristinsson et 1 985; Skilbrei 1988, 199 1 ; whitesel 1993 ) scenario, the autumn threshold length would be a population- and become smolts a year ahead of those in the lower modal specific trait, adapted to local growth conditions and to group (LMG) (Thorpe 1977; Nicieza et al. 1991 ), which different optimal smolt sizes.

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1604 CAN. J. ZOOL. VOL. 72, 1994

Although the development of growth bimodality is mainly under environmental control (Villarreal et al. 1988; Stefansson et al. 1989, 1991; Stewart et al. 1990; Saunders et al. 1989) , several studies have reported genetic effects and genetic constitution X environment interactions (Thorpe 1977; Thorpe and Morgan 1978; Bailey et al. 1980; Hanke et al. 1989; Stefansson et al. 1990). Thresholds in length or growth rate to maintain feeding activity during winter may vary between populations (Thorpe et al. 1980; Skilbrei 1988, 199 1 ), and different thresholds and breaks between modal groups have been reported for different populations (cf. Thorpe et al. 1980; Bailey et al. 1980; Kristinsson et al. 1985; Hanke et al. 1989; Stewart et al. 1990; Heggenes and Metcalfe 1991 ). However, it is unlikely that between-populations comparisons based on the results of separate studies can distinguish between environmental and genetic effects.

The objective of this study was to determine whether inter- population variability in the dynamics of growth bimodality results from genetic differentiation or whether environmental conditions and phenotypic plasticity are the basic factors con- trolling the expression of growth patterns in juvenile Atlantic salmon. We compared growth, survival, proportion of fish entering the UMG, and break points in the length-frequency distributions of juvenile salmon from two populations that were geographically disjunct (River Shin, northern Scotland, 58"N, and River Narcea, nokhern Spain, 43"N) but artificially reared under common environmental conditions. These rivers differ markedly in conditions for growth (e.g., temperature, conductivity, and length of growing season) that could have promoted genetic divergence.

In a previous paper we reported an inverse relationship between the size of individuals during the winter prior to smolt migration and their subsequent spring growth in fresh water (Nicieza and Braiia 1993). This suggests that spring growth may be an important component of smolt size in spe- cies in which migration is restricted to a few weeks (Hansen and Jonsson 1989; Fahy 1990). Specifically, we made two predictions. First, that selection would have favoured higher growth rates in populations subject to more adverse and longer winters. Second, because growth opportunity decreases with increased latitude (Thorpe 1989; Metcalfe and Thorpe 1990), we predicted that if autumn threshold lengths are cou- pled with spring growth opportunity to ensure that fish only begin metamorphosis if they are likely to reach an appropriate size by the time they must enter the sea, the ratio of threshold length to smolt length should be larger in northern than in southern populations.

Methods

Source rivers The River Shin drains Loch Shin, one of the Britain's largest lakes.

River flow downstream of the lake is regulated by a hydroelectric power station. Mean monthly flows range from 3.1 to 8.1 mL ss-I (Julian Hunter, Highland River Purification Board, Dingwall, U.K., personal communication). Water temperature varies between 0°C in winter and 20°C in summer; mean temperature is about 8-10°C. Water flow in the River Narcea is also controlled by a hydroelectric power station; mean flow is 47.3 mL ss-I. In the area accessible to salmon, the water temperature ranges from 6-7°C (winter) to 20- 22°C (summer) (data supplied by Confederacibn Hidrogrifica del Norte de Espafia). Therefore, both the length of the growing season (defined as the number of days per year when the water temperature

is at or above 7°C) and the temperatures during periods of growth and dormancy are markedly different in the two rivers.

Fish and experimental design Between 27 December 1990 and 9 January 1991, a total of

126 200 eggs were obtained from 20 females and 13 males caught in the River Narcea. To the extent that it was possible, each female was mated with one male, but in some instances one male was used to fertilize the eggs of two females. All embryos from this population were pooled and reared at the Rio Aspro hatchery (Asturias, northern Spain). On 16 January 1991, 700 000 fertilized eggs obtained from sea-run adults (approximately 100 females) caught in the River Shin and initially incubated at Kincardine Hatchery were transferred to the Rio Aspro hatchery at the eyed stage. Embryos hatched from 2 to 1 1 March (River Narcea) and from 10 to 13 March (River Shin). After first feeding, lots of 15 000 - 20 000 fish were transferred to 2-m2 quadrangular fiberglass tanks (2000 L ) supplied with fresh water at ambient temperature and under natural photoperiod.

On 16 July, two groups of 1500 randomly selected juveniles were taken from each population and ponded in four separate tanks iden- tical with that mentioned above. Food was delivered in excess (the same amount to each tank) by automatic feeders. We collected random samples of approximately 205 fish on 16 July, 9 November, and 18 December 1991, and 4 February, 28 February, and 9 April 1992. Fish were anaesthetized in 2-phenoxyethanol (3%0) and fork length (FL) was measured to the nearest 1 mm before they were returned to their respective tanks. Specific growth rates (SGR), expressed as percentage of body length per day, were calculated as

(In FL, - In FL,) . 100 SGR =

t2 - tl where FL, and FL, are the mean fork lengths of two consecutive samples of fish taken at times t, and t,. In December 1991, a total of 89 fish (26 from the River Narcea, 63 from the River Shin; length range 108- 144 mm) were tagged with V.I. tags (Northwest Marine Technology, Inc., Washington, U.S.A.) to allow individual growth rates over the period 18 December - 28 February to be calculated. To estimate early mortality in each tank, we collected and conserved in alcohol (70%) all fish that died between 16 and 29 July for further measuring in the laboratory, and recorded the total number of fish in each tank on 28 February and 9 April. Instantaneous mortality rates (m) were calculated as

where No and N , are the initial and final number of individuals and t, - to is the number of days between two successive counts. Indi- viduals in tanks containing the same population were pooled by late May. Smolting status was assessed according to external morphology and coloration criteria (Johnston and Eales 1967; Virtanen 1987). To estimate smolt size, 30 fish with complete silvering of the body and black fin margins were collected at random from each population on 15 June 1992 and measured to the nearest millimetre. We measured a further sample of LMG fish in August 1992 (River Shin, N = 120; River Narcea, N = 128).

Data analysis Length distributions were tested for normality using the

Kolmogorov - Smirnov test. From November onwards deviation from normality was evident in most samples, so we separated two approximately symmetrical distributions by eye and applied the Kolmogorov-Smirnov test to the resulting subsamples to check for normality. The subsequent analyses were the carried out separately for each modal group and sampling date. We used a two-level nested ANOVA (mixed model) to test for population effects (fixed factor) on fork length, with two replicates (tanks) per population. All tests were performed without pooling mean squares. To achieve a balanced design, data were randomly deleted until all the experimental units had the same number of observations within each sample (Sokal and Rohlf 1981; Zar 1984). Because heterogeneity of sample variances

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River Shin River Narcea

60 : 16 July 91 60

4

2

0

Fork length (mm)

FIG. 1. Length-frequency distributions of LMG (solid bars) and UMG (hatched bars) juvenile salmon from rivers Shin and Narcea during their first year of growth in fresh water. The two columns for each population refer to separate replicates. The dotted vertical lines show the 100-mm reference length.

were detected in 4 of the 1 1 samples (Cochran's test: July, P < 0.001, Institute Inc. 1985) and SPSS/PC+TM version 4.0 (Norusis 1992) LMG November, P = 0.01 3; UMG November, P = 0.039; LMG April, programs. P < 0.0005), data were log,,-transformed before carrying out the analyses. Sample variances were still heterogeneous in samples from Results ~ u l ~ - ( P < 0.001), November LMG ( P = 0.038), and April LMG Segregarion of modal ( P < 0.0005 ). Following Underwood ( 198 1 ), we set the significance levels for these three samples at 0.0001, 0.01, and 0.0001, respec- At the start of the experiment (July 16) all distributions

tively. i.e., less than the P value resulting from Cochranls test. We were unimodal and departures from were noted used the log-likelihood ratio ( G test) (Zar 1984) to examine whether (Fig. 1). From November onwards, normality was lost in the ratio of UMG to LMG fish was independent of source population. most of the overall distributions, so each was split into the Statistical analyses were carried out using SAS version 6.02 (SAS two modal groups. All but two of the resulting distributions

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TABLE 1. Ranking of growth among tanks, accumulated mortality, and parameters of length- frequency distributions of juvenile salmon from rivers Narcea and Shin

River Narcea River Shin

Tank 1 Tank 2 Tank 1 Tank 2

Rank of growth 16 July 1991a February 1992'

Accumulated mortality 29 July 1991 28 February 1992 9 April 1992

Distribution parameter (28 February 1992)

Root interval (mm) Modal interval

UMG (mm) LMG (mm)

% fish in UMG

TABLE 2. Two-level nested ANOVA testing the effects of between-populations differences and tanks nested within populations on fork length of salmon

b

Upper modal group Lower modal group

Source of variation MS d f F P MS d f F P

9 November Population Tank (population ) Error

18 December Population Tank (population) Error

4 February Population Tank (population) Error

28 February Population Tank (population) Error

9 April Population Tank (population) Error

NOTE: The F ratio of the population effect was calculated using the mean square of the "tanks nested within population" as the denominator.

(tank A, River Narcea LMG, 4 and 28 February, Kolmogorov- Smirnov test, P = 0.035 and P = 0.038, respectively) were normal. On 18 December, River Shin fish formed clearly bimodal length distributions, while segregation in the River Narcea tanks was somewhat delayed, no clearly bimodal pat- tern being observed until early February.

To test for differences between populations in the fraction of fish entering the UMG, replicates were combined in the samples from 18 December and 4 and 28 February ( G test for heterogeneity Zar 1984, P > 0.05) but not for the April sample ( P < 0.005). Differences could have resulted from an incorrect classification of the River Narcea samples from December but not those from 4 and 28 February, when the

categorization of River Narcea modal groups was reliable. The proportion of UMG fish tended to be greater in the River Narcea tanks until late February ( G test: 18 December, P = 0.043; 4 February, P < 0.001; 28 February, P = 0.153). The number of UMG fish declined further in all four tanks between late February and early May (Fig. 1 ) as a result of mortality, this effect being more pronounced for River Narcea fish (Table 1 ). Within each population, the tank in which the growth rate was greatest from July 1991 to February 1992 had the higher proportion of UMG fish (Table 1 ).

In late February, when the modal groups were clearly sepa- rated, the division between modal groups was at 85-90 and 100- 105 mm for the River Narcea and River Shin tanks,

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FIG. 2. Growth patterns of juvenile salmon from the rivers Narcea and Shin. (A) Evolution of the mean fork length for each population, modal group, and tank (replicates were pooled for May 1992; see Table 2 for significance of differences). ( B ) Mean specific growth rates (replicates were pooled within each population and modal group to simplify). At the end of the experiment, River Narcea UMG fish (smolts) overtook the corresponding group of River Shin fish in length.

respectively (Table 1 and Fig. 1 ). Modal intervals also dif- fered by about 10 mm among populations. The modal length for fish in the LMG, almost constant from November to March, was between 80 and 85 mm for River Narcea fish and between 90 and 95 mm for River Shin fish. UMG fish con- tinued to grow throughout the winter, and by 28 February the modal intervals were 110- 115 (River Narcea) and 125- 130 mm (River Shin).

Differences in size and growth rate Fish in all the four tanks were similar in size on 16 July

1991 (nested ANOVA, among groups F,1,2 = 0.48, P > 0.75). By November, River Shin fish were already larger than River Narcea fish in both modal groups (Fig. 2A), but differences were not statistically significant until December (UMG) or February (LMG), then were maintained until April (Table 2). Growth rates were relatively high between July and Novem- ber; by this time growth was lower for River Narcea than for River Shin fish regardless of modal group. The largest differ- ence in growth rates between modal groups also corresponded to that period (Fig. 2B). Thereafter, growth rates in all groups declined and differences decreased, although they remained somewhat higher for UMG fish until April. From mid-December

onwards, growth rates of River Narcea UMG fish were higher than those of River Shin UMG fish, and by 15 June, River Narcea smolts were larger than River Shin smolts (144.4 + 11.16 mm, N = 30, and 154.8 + 13.3 mm, N = 30; P = 0.020, respectively; Fig. 2A). For both populations, growth rates of LMG fish were close to zero throughout the winter (Fig. 2B). Negative values (River Narcea LMG) probably resulted from sampling error, since we assume that different fish were sam- pled on each occasion.

From a total of 89 UMG fish marked on 18 December, 51 were recaught on 28 February. Growth rates of individu- ally marked fish confirmed that River Narcea fish grew faster than River Shin fish between December and February (0.144 + 0.035 vs. 0.104 + 0.029; ANOVA, P < 0.0002). For the pooled sample there was a strong negative correlation between length and specific growth rate in December ( r = -0.499, P < 0.0001, N = 51). This negative correlation was also detected within the River Shin subsample ( r = -0.472, P = 0.003, N = 38) and a similar trend was noted for River Narcea fish, although in this case the correlation was not statistically significant, perhaps because of the small sample size ( r = -0.526, P = 0.065, N = 13). Fish density did not have an appreciable effect on growth, since there was no correspondence between tank density rank and growth rank by 28 February (Table I ) .

The instantaneous mortality rate decreased from August to February, then increased again in March, more strongly in the River Narcea tanks. Early mortality (16-29 July) affected mainly the smallest fish (length of dying fish (mean ? 1 SD) 29.0 + 5.2 mm, N = 330; length of live fish on 16 July: 35.2 + 5.5 mm, N = 816; tle14, = -17.57, P < 0.0001). Spring mor- tality associated with a sudden thaw affected mainly the smolt-like fish. Since the thaw developed over a period of a few hours (31 March), we were unable to collect samples for measuring.

Discussion This study has documented evidence for genetic differences

in the pattern of growth bimodality between two populations that presumably evolved under contrasting conditions for growth. Previous studies have demonstrated that juvenile salmon from different populations (but reared in different environments) segregate into the two modes at a different size (cf. Thorpe 1977; Bailey et al. 1980; Kristinsson et al. 1985; Skilbrei 1988; Saunders et al. 1989). Our results confirm that these differences persist when fish are reared in the same environment. It should be realized that autumn threshold lengths for entry to the UMG and break points between modal groups can differ between families within a population (e.g., Thorpe et al. 1980; Hanke et al. 1989; Stefansson et al. 1990). For instance, in Skilbrei's (1988) study the antimodes (April) ranged from 85 to 100 mm. In contrast, Stefansson et al.'s ( 1990) results indicate no differences among families with respect to break points or modal composition. For two separate families, Thorpe ( 1977) reported that genetic effects accounted for 59% of variation in the percentage of fish in the UMG. All these studies, however, were concerned only with one population, therefore they do not allow inferences to be made concerning the magnitude of interfamily variation in relation to interpopulation variation. Although we have not considered this source of variation, the River Narcea pool integrated, at least, the variability of 13 independent families,

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or 20 if maternal effects account for most of the variance in growth and development (Thorpe and Morgan 1978). The number of females used to generate the River Shin population was much higher. Therefore, we assumed that family effects had no important influence on the differences between popu- lations.

The antimodes are not themselves size thresholds but are the result of these. However, when population comparisons are carried out under the same rearing conditions they should reflect differences in the true size thresholds or in the growth rates at an earlier time. Specifically, the growth patterns of the two study populations differed in four ways: ( 1 ) the mean sizes within each modal group and the interval of segregation of the modes in midwinter were about 10 mm higher for the fish originating from River Shin ova than for River Narcea fish; ( 2 ) growth rates were greater for River Shin fish between July and November, but in the UMG were greater for River Narcea fish between November and smolting; ( 3 ) the segre- gation process appeared to be delayed in the River Narcea stock; and ( 4 ) direct examination of length distributions in February and differential spring mortality revealed that the proportion of fish entering the UMG was higher in the River Narcea tanks in spite of their slower growth.

Previous studies have shown between-populations differ- ences in growth rates of juveniles under controlled environmental conditions (Nzvdal et al. 1979). Jensen and Johnsen (1986) suggested that fish from cold rivers are gene- tically better adapted to growing at low temperatures. In the Atlantic silverside (Menidia rnenidia), the capacity for growth may vary inversely with the length of the growing season across a latitudinal gradient (Conover 1990; Conover and Present 1990). Our results are in the direction predicted: the population normally subject to the more adverse condi- tions for growth (River Shin) showed the higher growth rates when reared in standardized conditions. However, the study was restricted to two populations and therefore we cannot establish a definitive relationship between potential growth rates and environmental conditions. It should be noted that River Shin salmon appear to exhibit faster growth than salmon from two other Scottish rivers, Helmsdale and North Esk, reared under the same conditions (Laird and Needham 1986). The higher digestive efficiency of juvenile salmon from the River Shin than of those from the River Narcea (Nicieza et al. 1994) could provide the mechanistic basis of the interpopu- lation differences in growth.

There are two major reasons why natural selection could favour higher growth rates in juvenile salmon from more northerly populations. As in many other species of fish, one would be size-selective mortality due to predation or starva- tion during winter (Henderson et al. 1988; Post and Evans 1989; Johnson and Evans 1991 ). The second is the strong negative correlation that has been demonstrated for the Atlan- tic salmon between growth opportunity and age at smolt metamorphosis (Metcalfe and Thorpe 1990). Hence, fresh- water mortality in winter and age at sexual maturity should tend to increase as the freshwater growth conditions become poorer. Therefore, a genetically increased capacity for growth could partially compensate for the negative environmental influence at high latitudes. In some southern populations, these constraints might be relaxed, since environmental condi- tions during winter are favourable enough to allow most fish to attain a suitable size for metamorphosis during the first year.

Several foregoing studies on salmonid species have dem- onstrated that among-populations variation in development rates, morphology, and behaviour has a genetic component, probably resulting from local adaptation (Riddell and Leggett 198 1; Riddell et al. 198 1; Taylor and McPhail 1985a, 1985b; Swain and Holtby 1989; Taylor 1990a, 1990b). For the Atlantic salmon, Thorpe et al. ( 1980) suggested that the thresholds (in size or any physiological factor) required to trigger the smolting process and migration will have evolved in relation to the particular conditions in the freshwater and estuarine environments. Therefore, the ratio of size threshold to smolt size should tend to be larger in northern populations to compensate for the decline in growth opportunity that occurs with increasing latitude. In the River Narcea, the average size of wild smolts aged 1 + is about 15- 17 cm (Nicieza et al. 199 1; Nicieza and Brafia 1993). We do not have equivalent data for the River Shin, but based on other Scottish rivers (about 9- 13 cm; Thorpe et al. 1980), it would not be unreasonable to expect smaller smolt sizes than in the River Narcea population. In this study, River Shin smolts were smaller than River Narcea smolts despite the UMG fish from the River Shin being larger than those from the River Narcea throughout the winter and early spring.

Both the break points between modal groups and the growth rates were higher for River Shin fish. However, December and February samples revealed that differences in the modal structure and timing of segregation were not a consequence of differences in growth rates only, as the proportion of fish in the UMG did not change significantly between the two sampling periods. In this sense, several studies have reported that the photoperiod regime significantly altered the growth rate and the proportion of fish reaching the threshold size to enter the UMG, but not the break point between modes (Hanke et al. 1989; Saunders et al. 1989; Stewart et al. 1990; Stefansson et al. 1990). River Narcea UMG fish grew more slowly than River Shin fish in summer and autumn but faster in winter and spring. If the two populations shared the same environment why should growth rates reverse in UMG fish? The underlying cause may be associated with differences in the length of the growing season. In northern rivers, those individuals able to grow fast in summer-autumn should be favoured over slower growing fish, since water temperatures will nearly preclude growth in winter and spring. This also implies that phases of rapid growth (Kristinsson et al. 1985) must occur before the onset of winter. In contrast, juvenile salmon from southern rivers could attain the same or larger size by growing at a more even rate throughout their first year, because water temperature in winter is usually above the lower limit for growth (5-7°C; Power 1969; Jensen and Johnsen 1986). In our study, the transition from right-skewed to clearly bimodal frequency distributions took place between November and December for the River Shin fish, while most of the River Narcea fish segregated into modes between December and February, which suggests that the phase of rapid growth in the UMG would be delayed by a month in this population.

Our results support previous suggestions that the threshold for smolting (in size or physiological condition) is a population- specific trait (Thorpe 1986; Taylor 1990b). In addition, they provide preliminary evidence that populations from rivers with lower growth opportunity should tend to have larger ratios of threshold size to smolt size than populations having

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better growth opportunities. Smolt size and timing of seaward migration are considered two major factors influencing marine survival of post-smolts (Bilton et al. 1982; Lundqvist et al. 1988; Hansen and Jonsson 1989; Berglund et al. 1992). Therefore, thresholds may be adjusted in each population to reach, under the prevalent environmental conditions, a par- ticular size during the suitable period for seaward migration.

Acknowledgements We thank J. Arrontes, N.B. Metcalfe, E. Prkvost, and three

anonymous reviewers for helpful comments on the manu- script, and Julian Hunter for providing us with information about the River Shin. Permission to work at the Aspro hatch- ery was granted by the Agencia del Medio Ambiente del Principado de Asturias. The research was funded by a project grant from the Fundaci6n para el Fomento en Asturias de la Investigaci6n Cientifica Aplicada y la Tecnologia (FICYT). A.G. Nicieza was supported by FICYT and Ministerio de Educacion y Ciencia postdoctoral fellowships while preparing this manuscript.

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