Abstract: The dependence of growth rate in postsmolts in seawater on presmolt growth rate was examined in steelhead trout. (Oncorhynchus mykiss) and coho ...
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Does presmolt growth rate in steelhead trout (Oncorhynchus mykiss) and coho salmon (Oncorhynchus kisutch) predict growth rate in seawater? Jörgen I. Johnsson, John Blackburn, W. Craig Clarke, and Ruth E. Withler
Abstract: The dependence of growth rate in postsmolts in seawater on presmolt growth rate was examined in steelhead trout (Oncorhynchus mykiss) and coho salmon (Oncorhynchus kisutch). Presmolt growth rate explained a significant but small proportion, 16% for steelhead and 6% for coho, of the variation in growth rate in seawater. The relationship between presmolt and postsmolt growth rate was positive for steelhead and slightly negative for coho. In steelhead trout, the relationship between freshwater and seawater growth rate was not affected by male parental type (steelhead or domesticated rainbow trout). In coho salmon, however, the slope of regression was affected by differences among family groups. These results demonstrate variable relationships between presmolt and postsmolt growth rate among salmonid species and families, suggesting that fast presmolt growth is not necessarily associated with fast seawater growth in hatchery-reared salmonids. These findings are of interest for rearing procedures in smolt hatcheries and for models predicting optimal time and size for migration in wild smolts. Résumé : La relation de dépendance du taux de croissance après smoltification en mer sur le taux de croissance avant smoltification a été examinée chez la truite arc-en-ciel (Oncorhynchus mykiss) et le saumon coho (Oncorhynchus kisutch) . Le taux de croissance avant smoltification expliquait une partie statistiquement significative, mais tout de même faible (16% chez la truite arc-en-ciel et 6% chez le coho) de la variation du taux de croissance en mer. La relation entre les taux de croissance avant et après smoltification était positive chez la truite arc-en-ciel et légèrement négative chez le coho. Chez la truite arc-en-ciel, la relation entre le taux de croissance en eau douce et en eau salée ne subissait pas l’influence du type parental mâle (truite arc-en-ciel sauvage ou d’élevage). Toutefois, chez le saumon coho, la pente de régression variait en fonction des différences entre les groupes familiaux. Ces résultats mettent en évidence des différences du taux de croissance avant et après smoltification chez les différentes espèces et familles de salmonidés, et indiquent qu’une croissance rapide avant smoltification ne s’accompagne pas nécessairement d’une croissance rapide en mer chez les salmonidés élevés en écloserie. Ces constatations sont intéressantes du point de vue des méthodes d’élevage en écloserie et des modèles destinés à prévoir le moment et la taille optimales pour la migration des smolts sauvages. [Traduit par la Rédaction]
Introduction In anadromous salmonids, the relationship between presmolt growth rate and subsequent growth rate in seawater is of interest for (i) rearing procedures in smolt hatcheries, where it is important to know how selection for fast growth rate in the hatchery will affect adult sizes at return, and (ii) models predicting optimal time and size for migration in wild smolts (Bilton et al. 1982; Irwine and Ward 1989; Bohlin et al. 1993). A model by Bohlin et al. (1993) suggests that the degree of dependence of postsmolt growth on presmolt growth is critical
Received December 6, 1995. Accepted July 16, 1996. J13195 J.I. Johnsson,1 J. Blackburn, W.C. Clarke, and R.E. Withler. Department of Fisheries and Oceans, Biological Sciences Branch, Pacific Biological Station, Nanaimo, BC V9R 5K6, Canada. 1
Present address: Section of Animal Ecology, Department of Zoology, Göteborg University, Medicinaregatan 18, S-413 90 Göteborg, Sweden.
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for the timing of the smolt migration. However, in spite of its importance, information on the relationship between presmolt and postsmolt growth is scarce. The available information on body size and growth for anadromous salmonids indicates a positive relationship between size at migration/release and adult size as well as between presmolt and postsmolt length increase (Elliot 1985; Berg and Berg 1989; Berg and Jonsson 1989; L’Abee-Lund et al. 1989; Hershberger et al. 1990). Nicieza and Braña (1993), however, found an inverse correlation between smolt size and marine length increment in Atlantic salmon (Salmo salar). Further, as pointed out by Bohlin et al. (1993), body sizes and body size increments can be positively correlated even if the corresponding specific growth rates are independent. In two experiments with steelhead trout (Oncorhynchus mykiss) and coho salmon (Oncorhynchus kisutch) (Johnsson et al. 1993; R.E. Withler, unpublished data), which were designed for other purposes, we generated data on presmolt growth rates and growth rates after transfer to seawater. These data are used here to investigate the degree of correspondence between presmolt growth rates and postsmolt growth rates in seawater in these salmonids. © 1997 NRC Canada
Johnsson et al.
431 Table 1. Summary of an ANCOVA on specific growth rate: (a) growth rate in seawater tanks in steelhead trout and steelhead/domesticated rainbow trout hybrids; male type is steelhead trout or rainbow trout; (b) growth rate in seawater net pens in coho salmon. ANCOVA source (a) Steelhead trout Male type Freshwater growth Male type × freshwater growth Replicate (male type) (b) Coho salmon Family Presmolt growth Family × presmolt growth Replicate (family)
Methods Both experiments were conducted at the Pacific Biological Station in Nanaimo, B.C.
Steelhead experiment In the laboratory, we monitored the growth of 18 maternal half-sib families of wild-type steelhead trout and steelhead/domesticated rainbow trout hybrids. The trout were reared under ambient temperature and simulated natural photoperiod conditions from June 1989 (first feeding) to late May 1990. On 28–29 August, all fish were tagged with passive integrated transponder tags (Johnsson et al. 1993). Throughout the experiments, the fish were fed to satiation using commercial salmon diet. On 8 December, 270 fish were distributed into ten 197-L fibreglass tanks. Five tanks contained steelhead trout (27 in each tank) and five contained hybrid trout (27 in each tank). On 23 April, when subsamples from the tanks demonstrated hypoosmoregulatory capacity in a seawater challenge test (Johnsson et al. 1994), all tanks were switched from freshwater to ambient 30 ppt seawater. The salinity change was completed in 30 min. Thereafter, all experimental fish were reared in seawater until the termination of the experiment on 24 May 1990. During the experiments, each individual was weighed at regular intervals. Growth was divided into two periods: growth in freshwater from 5 March to 15 April (mean temperature (T) = 6.9°C) and growth in seawater from 15 April to the termination of the experiment on 24 May (T = 9.4°C). On 5 March, mean masses were 55.4 (61.6 SE) g for steelhead trout and 99.4 (63.1 SE) g for hybrid trout, respectively. Final mean masses were 107.7 (62.9 SE) g for steelhead trout and 178.1 (65.9 SE) g for hybrid trout, respectively. For further details, see Johnsson et al. (1993).
Coho experiment On 20 January, coho fry from a third generation selected Kitimat River stock were ponded into 200-L tanks. Feed was supplied continuously during daylight hours by automatic feeders. The photoperiod was maintained at 10 h from 20 January to 23 March when it was increased to 13.5 h and thereafter adjusted to simulate a seasonally increasing natural daylight plus civil twilight in order to produce underyearling smolts (Clarke 1992). On 30 March, 404 fry were PIT tagged. The fish were gradually acclimated to seawater according to the following schedule: 10 ppt on 21 March, 15 ppt on 7 April, 20 ppt on 2 May, and 29 ppt on 16 May. From 28 January to 18 May, temperature was 14°C. The fish were moved out to two replicate sea-
df
r2 (%)
1 1 1 8
8.0 16.0 0.0 8.7
2.6 55.0 0.6 4.2
0.11 0.0001 0.45 0.0001
6 1 6 7
35.0 6.3 3.9 1.0
5.2 22.4 4.5 1.0
0.0001 0.0001 0.0002 0.45
F
P
water netpens on 20 May. The temperature in the seapens was 14°C on 20 May, rising to 18°C in July and then decreasing to 13.5°C on 4 October; the mean for the entire period was 15.8°C. Wet mass was measured for each individual on 6 April, 10–11 May, and 3–5 October. The mean mass (replicates pooled) was 8.5 (60.1 SE) g on 6 April, 24.5 (60.3 SE) g on 10 May, and 362.1 (64.3 SE) g on 4 October.
Growth calculations and statistical analyses In both experiments, growth data was subjected to GLM analysis of covariance (ANCOVA) (SAS Institute Inc. 1985). Specific growth rates (Ricker 1979) were calculated as G = ln(Mt1/Mt0) 3 100d–1 where Mt0 and Mt1 were the initial and final wet mass for the period and d was the time in days.
Results Steelhead experiment About a third of the total variation in seawater growth of steelhead trout was explained by the ANCOVA model (Table 1a). Seawater growth rate (Gs) was significantly correlated with preceding freshwater growth rate (Gf) (r2 = 16%), and the estimated regression equation was Gs = 0.6(60.1 SE) + 0.4(60.1 SE)Gf. There was no significant effect of male parental type (steelhead or domesticated rainbow trout) or male parent by freshwater growth rate interaction. However, there was a significant variation among replicate tanks within male type. Coho experiment Almost half of the total variation in seawater growth of coho salmon was explained by the model (Table 1b). Seawater growth rate (Gs) was significantly predicted by presmolt growth in brackish water (Gb) (r2 = 6%), but the effect of family explained more of the growth variation (r2 = 35.0%). A significant interaction between family and presmolt growth indicated that the slope between presmolt growth and seawater growth was heterogenous among families. The regression slope was negative in six families and positive in one. The overall regression equation was Gs = 2.4(60.2 SE) – 0.1(60.05 SE)Gb. © 1997 NRC Canada
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Discussion Our results demonstrate that postsmolt seawater growth rate in steelhead trout and coho salmon is significantly predicted by presmolt growth rate in freshwater. However, it is interesting to note the following. (i) The dependence of seawater growth on freshwater growth was not very strong (b ˜ 0.4 for steelhead and b ˜ 20.1 for coho, respectively). (ii) Only a small proportion of the total variation in seawater growth was explained by preceding presmolt growth (16% for steelhead and 6% for coho, respectively). This indicates that although presmolt growth rate is correlated significantly with subsequent growth in seawater, the relationship is weakened by a large amount of random variation, limiting the use of freshwater growth rate as an indicator of future growth performance in the sea. (iii) The relationship between presmolt and postsmolt growth rate differed between experiments, being positive in the steelhead experiment and slightly negative in the coho experiment. There was also considerable variation among family groups in the coho experiment whereas there was no effect of male parental life-history type (steelhead or domesticated rainbow trout) in the steelhead experiment. Overall, our results suggest that fast presmolt growth is not necessarily associated with fast seawater growth. There are several possible explanations for the absence of consistent and strong positive correlations between freshwater and seawater growth rates in the present study. Firstly, growth-promoting characters may be specific to a particular environment. For example, juvenile coho salmon rearing pelagically in lakes are less aggressive than nearby stream-living coho (Swain and Holtby 1989), and chinook salmon (Oncorhynchus tshawytscha) populations with longer stream residence are more aggressive than ocean-type chinook (Taylor 1990). Thus, inherited (nonplastic) behavioural characters may have differential growth-promoting effects in stream and pelagic environments, respectively. Furthermore, the risk of predation in the food-limited stream environment may act to favour slower growth compared with the marine environment with its greater availability of food (Johnsson and Abrahams 1991). Similar limitations on phenotypic plasticity may constrain physiological adaptations, such as osmoregulation (Hasegawa et al. 1987) and digestion, from being equally effective in freshwater and seawater. Secondly, in our experiments, as in most hatcheries, all fish were placed in seawater simultaneously, whereas in natural populations, migration is “voluntary” and individuals of different age and size migrate at different times (Bohlin et al. 1993). It is likely that the possibility of individual choice of migration time might influence the correlation between presmolt and postsmolt growth. Thirdly, higher food abundance in the sea compared with the stream would elevate the intercept of the growth regression equation. In contrast with wild smolts that experience a limited food supply in streams, the fish in our experiments experienced no difference in food abundance between the freshwater and seawater environments. Fourthly, some of the differences may be attributed to the different designs of the two experiments. In the steelhead experiment, seawater growth was measured over a shorter time (39 days) and may not be representative of long-term growth in seawater. The steelhead were also larger than coho when trans-
Can. J. Fish. Aquat. Sci. Vol. 54, 1997
ferred to seawater. Finally, the steelhead were reared in a uniform tank enviroment during the entire experiment whereas coho were transferred from tanks to seawater netpens. It would be interesting to compare our results with other studies on premigratory and postmigratory growth rates of hatchery and wild salmonid populations. Presently, this kind of information is lacking, providing an unexplored and important field of research.
Acknowledgements This study was made possible by a grant (40.0357/93) to J.I.J. from the Swedish Council for Forestry and Agricultural Research. Excellent technical assistance was provided by the staff at the Pacific Biological Station in Nanaimo, B.C. We are grateful to Torgny Bohlin for stimulating discussions during this project.
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