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Genetic correlation for body weight of Atlantic salmon grilse between fish in sea ranching and land-based farming
Aquaculture ELSEVIER
Aquaculture
157 (1997) 205-214
Genetic correlation for body weight of Atlantic salmon grilse between fish in sea ranching and land-based farming J. Jbnasson a,*, T. Gjedrem ’ ’
Stofnfiskur
h AKVAFORSK,
Ltd., Laugac~egi 103, PO Bm 5166, 125 Reykjavik, Iceland Institute ofAquaculture Research Ltd., PO Box 5010, N-1432 A’s, Norway Accepted 22 February
1997
Abstract A research programme in salmon ranching in Iceland was started in 1987. The primary aim was to study the genetic variation in the frequency of return to the site of smelt release. The purpose of this investigation was to estimate the genetic correlation between the body weight of fish returning from sea ranching and the body weight of their full- and half-sibs reared in land-based farms. Fish from two year-classes were used, and progenies of 220 full- and 76 half-sib families were included. Significant effects of sex and age at sexual maturation on body weight were observed. For sea ranching, males were larger than females, and mature males and females were larger than immature fish at the land-based farms. The mean body weight of fish returning from sea ranching was more than two times larger than their sibs reared at the land-based farms. Heritability estimates for the body weight of grilse from salmon ranching for 1989 and 1991 year-classes were 0.20 * 0.10 and 0.23 + 0.12, respectively. The heritability estimates for body weight of grilse at land-based farms for 1989 and 1991 year-classes were 0.31 + 0.17 and 0.27 f 0.10, respectively. The genetic correlation between body weight of fish returning from sea ranching and land-based farming was 0.42 + 0.28 for the 1989 year-class and 0.27 f 0.34 for the 1991 year-class. 0 1997 Elsevier Science B.V.
1. Introduction
Sea ranching of Atlantic salmon has been an important aquaculture method in Iceland since the early 1970s (Isaksson, 1988). In 1993, 450 tonnes of sea-ranched salmon were produced (Stefansson, 1994).
* Corresponding
author. Tel.: +354
5528400.
Fax: +354
5528401.
E-mail: [email protected].
00448486/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SOO44-8486(97)00060-4
206
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The present study is a part of a research programme focusing on the possibilities to increase return rate and body weight in sea ranching by selection. Jonasson et al. (1997) estimated the heritability for return rate from the sire component of variance to 0.12 for grilse, and 0.04 for two-sea winter salmon. The heritability for body weight of grilse was estimated to be 0.36 k 0.11. If increased return rate and body weight are defined as the breeding goal for sea ranching, the best selection method would be a combined individual and family selection because return rate has a low heritability since it is an all-or-none trait. Returning fish from families with the highest mean body weight and return rate should be used as broodstock. Low return rates occur frequently in sea ranching, which means that there are few fish for individual selection within families for body weight. To some extent, although expensive, this might be overcome by increasing the number of released smolts per family. Gjedrem (1986) discussed the design of a breeding programme for sea ranching of Atlantic salmon. Two approaches were suggested to secure effective selection. In the first alternative, all returning fish should be kept alive until the season has ended and broodstock should be selected among returning fish. Gjedrem (1986) concluded that this may be difficult to practise, since the mortality of broodstock may be high before selection is possible. Furthermore, if the return rate is low, very few fish will be available to permit individual selection within families. In the second alternative, Gjedrem (1986) suggested to tag or mark full-sibs of the released smolts and rear them in farms to produce broodstock. This will allow the sea rancher to kill all fish upon return. When all returning fish have been recorded, families may be ranked according to their performance in return rate and body weight in sea ranching. Selection of broodstock could then be practised among the farmed sibs of the returning fish. The objectives of the present study is to estimate the genetic correlation between the body weight of grilse (l-sea-winter salmon) returning from sea ranching, and the body weight of grilse reared in a land-based farm. The estimated genetic correlation will indicate how effective individual selection for increased body weight in sea ranching will be when body weight performance in land-based farming is used as a selection criterion. The estimated genetic correlation can also be a measure of genotype by environment interaction. Falconer (1952) presented a formalised genotype by environment interaction test in terms of genetic correlation, by regarding a trait recorded in two different environments as two separate traits. A genetic correlation between performance in different environments close to unity implies that genotype by environment interaction is negligible. In contrast, a genetic correlation close to or below zero will suggest extensive genotype by environment interaction.
2. Material and methods Fish from two year-classes, 1989 and 1991, were used in the experiment. To produce each year-class, a hierarchical mating system was applied using milt from one male to fertilise eggs of 2-6 females to produce full- and half-sib families. Two salmon strains were used each year. In the 1989 year-class, the Kollafjiiraur ranching strain from the
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Kollafjijraur Experimental Fishfarm and the Isn6 ranching strain from Northern Iceland were used. In the 1991 year-class, the Kollafjiiraur ranching strain and the Laros ranching strain from West Iceland were used. In the 1989 year-class, 120 full-sib families within 44 half-sib groups were produced, and in the 1991 year-class, 100 full-sib families within 32 half-sib families were produced. Broodstock was randomly sampled from each strain, and random mating was applied. Newly fertilised eggs were brought to the hatchery in Kollafjiiraur Experimental Fishfarm and each full-sib family was incubated in a separate tray. Each full-sib group was reared separately in indoor 1-m’ fibreglass tanks during startfeeding and fingerling stage until tagging, 8-10 months after startfeeding. All families released for sea ranching in year-classes 1989 and 1991 were microtagged using Binary coded wire tags. Microtags are small pieces of wire (2 mm long) with a binary code which are injected into the snout of salmon Parr. The tag code can only be read after the fish is killed and the tag is retrieved. As an external indicator of tagging, the adipose fin was cut off. Each family was split into four or five subgroups; for the 1989 year-class three subgroups were released at three different sites, and for the 1991 year-class, sub-groups were released at four different sites. One subgroup for each year-class was reared in one tank in a land-based farm. The smolts of the 1989 year-class which were reared at Grundartangi in West Iceland were tagged with floy tags as an external tag. Coldbranding and fin-clipping (Refstie and Aulsted, 1975) were used to identify the smelts of the 1991 year-class, which were reared at Stofnfiskur in Southwest Iceland. Body size at tagging were 20.5 g and 17.8 g, for 1989 and 199 I year-classes, respectively. After tagging, all families were stocked together in outdoor concrete ponds at Kollafjiiraur Experimental Fishfarm, one pond for each release site,
L
N
a 0
Fig.
50
1OOh
I Location of the release sites in Iceland used in the project.
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Table 1 Number of smolts released at each release site, number of grilse returning Release site
Year-class 1989 Smelts released (N)
Kollafjijraur Silfurlax Vogavik Lgr6s Total
and return rate
1991 Grilse (N)
39 284 19812 17859 _
960 356 271 _
76955
1587
% Return
Smelts released (N)
2.44 1.80 1.52
30539 8082 7164
Grilse (N) 872 169 145
2.86 2.09 1.87
% Return
_ 2.06
5769 52 154
193 1379
3.35 2.64
and one for the farmed group, beginning in November-December, and kept there until transported to the release site and the land-based farm in April-June. By the time the fish were transported to the release sites and to land-based farms, the body size had increased, for 1989 and 199 1 year-classes, to 28.1 g and 24.3 g, respectively. The smelts of the 1989 year-class were released from Kollafjijraur, Vogavik and Silfurlax, and the 1991 year-class smolts were released from Kollafjoraur, Vogavik, Silfurlax and LB& (Fig. I). The number of released smolts and returning grilse to each release site is given in Table 1. For more detailed information about release sites and release methods, see Jonasson (1996). The body weight and sex of the returning grilse were recorded. In the 1989 year-class, all fish in the land-based unit at Grundartangi were slaughtered in August 1991. The sex, stage of maturation and body weight of 740 fish were also recorded. In the 1991 year-class, the body weight of 2359 fish in the land-based unit at Stofnfiskur was recorded in June 1993. The sex and stage of sexual maturation were also recorded. The sex of immature fish was not recorded for the 1991 year-class. The Grundartangi land-based farm had seawater with full salinity (32%0), and the water was pumped from l-4 m under the sea surface all-year-round. The temperature varied from 0°C in winter, to 14-15°C in summer. At Stofnfiskur land-based farm, the sea water was pumped from boreholes with a temperature of 10-l 1°C and the salinity at 28-32%0 for the first 3 months. For the rest of the test period, the temperature was 6-7°C and salinity was 22-25%0 without any seasonal fluctuations in temperature.
3. Statistical
analysis
The body weights of the returning grilse and fish reared in the land-based farms were analysed. The body weights of the returning grilse were readjusted multiplicatively for the effect of sex within salmon strain and release site. All returning fish were mature; males were significantly larger than females and had larger variances compared to females within the same strain. The correction factor used was obtained by multiplying the individual weight and the ratio of the grand mean body weight to the mean body weight of each sex within the strain and release site. A similar correction was applied for
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the body weight of fish reared in the land-based farms for immature fish and mature males and females. The multiplicative adjustment was chosen due to the observed dependency between the mean and the variance (Table 2). The variance components for body weight (upon return from ranching and after rearing in the land-based farms) were separately estimated according to an animal model for each year-class. The animal model allows both the recorded individuals and the unrecorded parents to be included in the analysis, to consider all known additive genetic relationship between the animals. The model also includes both fixed and random effects, such as: y.ik = Yjk
=
P= r= st, = Uijh = .f,,n = e,,!X=
p + r, + St,, + a,jk +frjk + erjk precorrected body weight of the kth fish overall mean fixed effect of the release site (i = 1-3 for 1989 year-class and i = l-4 for 199 1 year-class) fixed effect of salmon strain (j = l-2) random additive genetic effect of the kth fish the random common full-sib effects for the kth fish due to factors other than additive gene effects random error
The additive effects, the common full-sib effects due to factors other than additive gene effects, and the residual effects were assumed to have independent normal distributions with zero means and variances of q,‘, CT+’ and uP2, respectively. The variance components were estimated from a derivative-free restricted maximum likelihood (df-REML) algorithm (Meyer, 1989) using programmes based on the software (DFUNI) written by Meyer (1991). The variance components for body weight in land-based farms were estimated according to the same model, but excluding the fixed effects of the release sites. Technically, a heritability estimate is a strain-specific character, and should be estimated separately for each strain. However, given the limited number of sires and
Table 2 Number of fish, body weight means (kg) and standard deviations Sea ranching
1989 year-class Mature males Mature females Immature males Immature females 199 1 year-class Mature males Mature females Immatures (sex unknown)
Land-based
N
Mean
S.D.
790 797
2.45a 2.08b
0.43 0.28
847 532
(S.D.) for each year-class
2.47a 2.15b
0.40 0.27
N
farming Mean
S.D.
1.09a 1.I3a
263 118 92 267
0.89b 0.90b
0.25 0.19 0.27 0.24
89 9 2261
0.70a 0.76a 0.69a
0.24 0.24 0.25
Within a column and effect, mean values followed by the same letter are not significantly
different (P < 0.05).
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dams in these data, the accuracy of estimates within strains will be very low. Therefore, an average heritability was determined for each trait incorporating strain as a fixed effect in the model. A future selection programme will most likely focus on a single population. For estimation of the phenotypic and genetic correlation between body weight of sea ranched grilse and body weight of their full- and half-sibs reared in land-based farms, a univariate analysis was run as described above. Subsequently, a bivariate analysis was run, in which the body weight of the returning sea ranched grilse and the body weight of fish in land-based farms were regarded as two different traits. The DFMUW programme (Meyer, 1991) sets the error covariance between the traits to zero since they are not measured on the same animal. When estimating genetic correlation, the common full-sib effect was not included. Because of the complexity of the statistical analysis, it was not possible to estimate the standard errors of the estimated variance and covariance components. Therefore, rough approximates of the standard errors of the genetic correlation were derived using the formulae for full-sib analysis for two continuous traits given by Scheinberg ( 1966).
4. Results
4.1. Effect of sex and sexual maturation
The overall return rate from sea ranching was 2.06% for 1989 year-class and 2.64% for 1991 year-class (Table 1). There was a considerable difference in the mean body weight between fish returning from sea ranching and those reared in the land-based farm (Table 2). Significant differences were observed in the body weight between the sexes returning from sea ranching. A significant difference was observed between the body weight of mature and immature fish in the 1989 year-class, but not in the 1991 year-class. In the 1989 year-class, 5 1% of the fish reared in land-based farm matured, but in the 1991 year-class, only 4.1% matured.
Table 3 Number of salmon strains, sires and dams used per year-class
1989 year-class Sea ranching Land-based farming 199 1 year-class Sea ranching Land-based farming
Strains
Sires
Dams
h’ + s.e.
,f’ * s.e.
2 2
44 41
120 102
0.20+0.10 0.31+0.17
0.04 f 0.04 0.02 f 0.07
2 2
32 32
100 96
0.23f0.12 0.27*0.10
0.06 + 0.052 0.00 f 0.04
Estimates of heritabilitiesfstandard errors (h” +s.e.) for body weight caused by factors other than additive genetics (f’ f s.e.1.
and the effect common
to full-sib
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and genetic parameters
The heritability estimates for the body weight of grilse in salmon ranching were estimated as 0.20 f 0.10 and 0.23 f 0.12, for the 1989 and 1991 year-classes, respectively. The heritabilities for the body weight of grilse in land-based farming were estimated as 0.31 k 0.17 and 0.27 f 0.10, for the 1989 and 1991 year-classes, respectively. The common full-sib effects other than additive genetic effects ranged from 0.004 to 0.06 in both year-classes (Table 3). The phenotypic correlation between the body weight of fish returning from sea ranching and that of farmed fish was estimated to be 0.14 for the 1989 year-class and 0.09 for the 199 1 year-class. The genetic correlation between the body weight in the two environments was estimated to be 0.42 f 0.28 for the 1989 year-class and 0.27 * 0.34 for the 1991 year-class.
5. Discussion Grilse that returned from sea ranching were more than twice as large compared to their sibs in land-based farms. Growth performances similar to those achieved in the farmed groups were reported for Atlantic salmon reared in net-pens in Norway (Gjerde et al., 19941, where the mean body weight was 0.6 kg after being reared 12 months in sea cages. This shows that it is not unusual that salmon grew faster in the open sea around Iceland, compared to their sibs stocked in a land-based fish farm. The reason for this difference is uncertain, as the migration pattern of ranched salmon around Iceland during the first year at sea is not known. Using strains for farming in land-based farms, which were previously used in sea ranching for several generations, may result in stressful conditions during the rearing period leading to deleterious effects on growth rate (Pickering et al., 1991). Thus, the sea-ranched strains are not adapted to captivity and the environmental conditions are not optimal for the fishes in a land-based farm. In ordinary cage farming conditions in Norway, using domesticated salmon from the national breeding programme, the fish grow faster than that in sea ranching (Refstie, personal communications). A significant effect on sex was observed after one year in sea ranching. Males were 17.8% larger then females in the 1989 year-class and 14.9% larger in the 199 1 year-class. Grilse returning in sea ranching are all mature, and no information on immature fish is available. There was no significant difference in size between the sexes observed in land-based farming. The effect of sexual maturation was observed in the 1989 year-class in the land-based farm, where mature fish were 22% larger then immature fish. Similar results were reported by Gjerde et al. (1994) for Atlantic salmon reared one year in the sea. Similar effects on sex and sexual maturation have been reported for Atlantic salmon by Navdal (19831, Gjerde (19861, Gjerde and Refstie (1984) and Rye (1992). There was no effect on sex observed in the year-class 1991. There was a significant difference between year-classes in size and frequency of maturation in the land-based farms. This difference could partly be explained by the time of recording, when all fish in 1989 year-class were slaughtered and measured in
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August 1991, while fish in the 1991 year-class were weighed alive in June 1993, two months earlier than that for 1989 year-class. External characteristics on maturing fish might not have been detectable in June on all the maturing fish. For the 1991 year-class, there were no seasonal temperature fluctuations in the land-based farm which could also affect the frequency of maturation after 12 months of rearing in seawater. The estimated he&abilities (Table 3) indicate significant additive genetic variation for the body weight of returning grilse from sea ranching, and for the body weight of salmon reared 12- 14 months in land-based farms. Gjerde et al. (1994) reported a heritability of 0.30 + 0.06 for Atlantic salmon reared for 12 months in sea cages in Norway. These results show that it is possible to increase the body weight at harvesting in sea ranching programme when selection is applied. The estimated effects common to full-sibs caused by factors other than additive genetics (full-sib group effect, f *, Table 3) were low and insignificant, and very low for the fish raised in land-based farms. Gjerde et al. (1994) reported a similar full-sib effect of 0.08. This is, most likely, a transitory common environmental effect introduced when the full-sib families were reared in separate tanks prior to tagging. However, nonadditive genetic effects cannot be ruled out. The genetic correlation between the body weight upon return to sea ranching and the body weight in land-based farms were low to medium and insignificant. These low genetic correlation is, according to Robertson (1959), a measure of the existence of genotype-environment interaction for a trait measured in two different environments. Similar results, although with higher genetic correlation, were found by Sylven et al. (199 1) while recording growth rate for rainbow trout in fresh, brackish and sea water. These results show that these two traits are probably partly controlled by different sets of genes. The body weight characteristic in the present study is an expression of genetic potential within two widely different environments. In salmon ranching, body weight may be affected by genes controlling survival, age at maturation, success in capturing prey, temperature, behaviour, etc. Growth in land-based farms will be affected by stress sensitivity, temperature, behaviour (e.g., aggression), food conversion efficiency, etc. A strong natural selection in salmon ranching may have reduced the genetic correlation between ranching and land-based farming.
6. Conclusion In a selection programme for salmon ranching, where the breeding goal is increased return rate and body weight, the best selection method would be a combined individual and family selection for body weight, and family selection for return rate, using the returning fish as broodstock. The estimation of family breeding values should be based on their performance in return rate and growth rate in the sea. Therefore, enough smelts must be tagged and released per family to get an accurate estimate of family breeding values. However, low return frequencies occur in sea ranching, which means that there are few fish in each family, leading to the low accuracy of family breeding values and low efficiency of individual selection within families for body weight. Therefore, production of salmon under farming conditions from the same families as released to the
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sea will ensure the selection of broodstock from families with high breeding values, although the returns are very low. If a breeding programme will supply the sea ranching industry, the majority of the broodstock must be produced under farming conditions. The breeding station itself should select and use returning fish as broodstock for the next generation as much as possible. Although the genetic correlations are low between sea ranching and land-based farming for body weight, one should also use the largest fish on the land-based farm as broodstock, but the efficiency of selection for increased body weight may be lower compared to using the returning fish from sea ranching as broodstock.
Acknowledgements The project was financed by the government of Iceland, the Nordic Council of Ministers and the Nordic Industrial Foundation. The project was administered, by, a board with representatives from all the Nordic countries. The members are: Ami Isaksson, chairman, Institute of Freshwater Fisheries, Iceland; Dr. Stefan Adalsteinsson, Institute for Agricultural research, Iceland; Dr. Trygve Gjedrem, AKVAFORSK, Norway; Dr. Lars-Ove Eriksson, Agricultural University of Umea, Sweden; Dr. Unto Eskelinen, Lauka research institute, Finland; Dr. Jens-Ole Frier, University of Aalborg, Denmark; Mr. Andrias Reinert and Mr. Ingvard Fjallstein, Research Institute for Marine Fisheries, Faro Islands. Dr. Jonas Jonasson was project leader and secretary for the board. The authors would like to thank them for their help in the project. Many thanks to Dr. Vigftis Johannsson at Kollafjiiraur Experimental Fishfarm at Kollafjoraur, Iceland for helping in running the project. Special thanks to Dr. Hans B. Bentsen and Dr. Bjame Gjerde, AKVAFORSK, Norway for helping in analysing data and fruitful discussions and comments on the manuscript. The author wishes to thank all the staff at Kollafjiiraur Experimental Fishfarm, the staff at Grundartangi and Stofnfiskur land-based farms, as well as the salmon ranching companies Silfurlax, Vogavik and LBr6s for letting us use their release sites for the release of tagged smolts and recapturing returning fish.
References Falconer, D.S., 1952. The problem of environment and selection. Am. Nat. 86, 75-86. Gjedrem, T., 1986. Breeding plan for sea ranching. Aquaculture 57, 77-80. Gjerde, B., Refstie, T., 1984. Complete diallel cross between five strains of Atlantic salmon. Livestock Prod. Sci. I I, 207-226. Gjerde, B., 1986. Growth and reproduction in fish and shellfish. Aquaculture 57, 37-55. Gjerde, B., Simianer, H., Refstie, T., 1994. Estimates of genetic and phenotypic parameters for body weight, growth rate and sexual maturity in Atlantic salmon. Livestock Production Science 38, 133-143. Isaksson, A., 1988. Salmon ranching: a World review. Aquaculture 75, I-33. Jonasson, J., 1996. Selection experiments in Atlantic salmon ranching II Variation among release sites and strains for return rate, body weight and ratio of grilse to total return. Aquaculture 144, 277-294. Jonasson. J., Gjerde, B., Gjedrem, T., 1997. Genetic parameters for return rate and body weight of sea-ranched Atlantic salmon. Aquaculture (same issue).
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Meyer, K., 1989. Restricted maximum likelihood to estimate variance components for animal models with several random effects using a derivative-free algorithm. Genet. Sel. Evol. 21, 317-340. Meyer, K., 1991. DFREML. Programs to estimate variance components by restricted maximum likelihood using a derivative-free algorithm. User’s Notes. Version 2.0, 84 pp. Naevdal. G., 1983. Genetic factors in connection with age at maturation. Aquaculture 33, 97-106. Pickering, A.D., Pottinger, T.G., Sumpter, J.P., Carragher, J.F., LeBail, P.Y., 1991. Effects of acute and chronic stress in the levels of circulating growth hormone in the rainbow trout, Onchrhwchus mykiss. Gen. Comp. Endocrinol. 78, 194-203. Refstie, T., Aulsted, D., 1975. Tagging experiments with salmonids. Aquaculture 5, 367-374. Robertson, A., 1959. The sampling variance of the genetic correlation coefficient. Biometrics 15, 469-485. Rye, M., 1992. Studies on body traits in Atlantic salmon (Salmo S&r). PhD. Thesis, University of Aas Norway. Scheinberg, H., 1966. The sampling variance of the correlation coefficients estimated in genetic experiments. Biometrics 22, 187-191. Stefansson, S.E., 1994. Production in Icelandic Fishfarming in 1993 (in Icelandic). Report from the Institute of Freshwater Fisheries. VMST-R/94003, 19 pp. Sylven, S., Rye, M., Simianer, H., 1991, Interaction of genotype with production system for slaughter weight in rainbow trout (Oncorhynchus mykiss). Livest. Prod. Sci. 28, 253-263.
Aquaculture
157 (1997) 205-214
Genetic correlation for body weight of Atlantic salmon grilse between fish in sea ranching and land-based farming J. Jbnasson a,*, T. Gjedrem ’ ’
Stofnfiskur
h AKVAFORSK,
Ltd., Laugac~egi 103, PO Bm 5166, 125 Reykjavik, Iceland Institute ofAquaculture Research Ltd., PO Box 5010, N-1432 A’s, Norway Accepted 22 February
1997
Abstract A research programme in salmon ranching in Iceland was started in 1987. The primary aim was to study the genetic variation in the frequency of return to the site of smelt release. The purpose of this investigation was to estimate the genetic correlation between the body weight of fish returning from sea ranching and the body weight of their full- and half-sibs reared in land-based farms. Fish from two year-classes were used, and progenies of 220 full- and 76 half-sib families were included. Significant effects of sex and age at sexual maturation on body weight were observed. For sea ranching, males were larger than females, and mature males and females were larger than immature fish at the land-based farms. The mean body weight of fish returning from sea ranching was more than two times larger than their sibs reared at the land-based farms. Heritability estimates for the body weight of grilse from salmon ranching for 1989 and 1991 year-classes were 0.20 * 0.10 and 0.23 + 0.12, respectively. The heritability estimates for body weight of grilse at land-based farms for 1989 and 1991 year-classes were 0.31 + 0.17 and 0.27 f 0.10, respectively. The genetic correlation between body weight of fish returning from sea ranching and land-based farming was 0.42 + 0.28 for the 1989 year-class and 0.27 f 0.34 for the 1991 year-class. 0 1997 Elsevier Science B.V.
1. Introduction
Sea ranching of Atlantic salmon has been an important aquaculture method in Iceland since the early 1970s (Isaksson, 1988). In 1993, 450 tonnes of sea-ranched salmon were produced (Stefansson, 1994).
* Corresponding
author. Tel.: +354
5528400.
Fax: +354
5528401.
E-mail: [email protected].
00448486/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SOO44-8486(97)00060-4
206
J. J6nasson, T. Gjedrem/Aquaculture
157 (19971 205-214
The present study is a part of a research programme focusing on the possibilities to increase return rate and body weight in sea ranching by selection. Jonasson et al. (1997) estimated the heritability for return rate from the sire component of variance to 0.12 for grilse, and 0.04 for two-sea winter salmon. The heritability for body weight of grilse was estimated to be 0.36 k 0.11. If increased return rate and body weight are defined as the breeding goal for sea ranching, the best selection method would be a combined individual and family selection because return rate has a low heritability since it is an all-or-none trait. Returning fish from families with the highest mean body weight and return rate should be used as broodstock. Low return rates occur frequently in sea ranching, which means that there are few fish for individual selection within families for body weight. To some extent, although expensive, this might be overcome by increasing the number of released smolts per family. Gjedrem (1986) discussed the design of a breeding programme for sea ranching of Atlantic salmon. Two approaches were suggested to secure effective selection. In the first alternative, all returning fish should be kept alive until the season has ended and broodstock should be selected among returning fish. Gjedrem (1986) concluded that this may be difficult to practise, since the mortality of broodstock may be high before selection is possible. Furthermore, if the return rate is low, very few fish will be available to permit individual selection within families. In the second alternative, Gjedrem (1986) suggested to tag or mark full-sibs of the released smolts and rear them in farms to produce broodstock. This will allow the sea rancher to kill all fish upon return. When all returning fish have been recorded, families may be ranked according to their performance in return rate and body weight in sea ranching. Selection of broodstock could then be practised among the farmed sibs of the returning fish. The objectives of the present study is to estimate the genetic correlation between the body weight of grilse (l-sea-winter salmon) returning from sea ranching, and the body weight of grilse reared in a land-based farm. The estimated genetic correlation will indicate how effective individual selection for increased body weight in sea ranching will be when body weight performance in land-based farming is used as a selection criterion. The estimated genetic correlation can also be a measure of genotype by environment interaction. Falconer (1952) presented a formalised genotype by environment interaction test in terms of genetic correlation, by regarding a trait recorded in two different environments as two separate traits. A genetic correlation between performance in different environments close to unity implies that genotype by environment interaction is negligible. In contrast, a genetic correlation close to or below zero will suggest extensive genotype by environment interaction.
2. Material and methods Fish from two year-classes, 1989 and 1991, were used in the experiment. To produce each year-class, a hierarchical mating system was applied using milt from one male to fertilise eggs of 2-6 females to produce full- and half-sib families. Two salmon strains were used each year. In the 1989 year-class, the Kollafjiiraur ranching strain from the
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Kollafjijraur Experimental Fishfarm and the Isn6 ranching strain from Northern Iceland were used. In the 1991 year-class, the Kollafjiiraur ranching strain and the Laros ranching strain from West Iceland were used. In the 1989 year-class, 120 full-sib families within 44 half-sib groups were produced, and in the 1991 year-class, 100 full-sib families within 32 half-sib families were produced. Broodstock was randomly sampled from each strain, and random mating was applied. Newly fertilised eggs were brought to the hatchery in Kollafjiiraur Experimental Fishfarm and each full-sib family was incubated in a separate tray. Each full-sib group was reared separately in indoor 1-m’ fibreglass tanks during startfeeding and fingerling stage until tagging, 8-10 months after startfeeding. All families released for sea ranching in year-classes 1989 and 1991 were microtagged using Binary coded wire tags. Microtags are small pieces of wire (2 mm long) with a binary code which are injected into the snout of salmon Parr. The tag code can only be read after the fish is killed and the tag is retrieved. As an external indicator of tagging, the adipose fin was cut off. Each family was split into four or five subgroups; for the 1989 year-class three subgroups were released at three different sites, and for the 1991 year-class, sub-groups were released at four different sites. One subgroup for each year-class was reared in one tank in a land-based farm. The smolts of the 1989 year-class which were reared at Grundartangi in West Iceland were tagged with floy tags as an external tag. Coldbranding and fin-clipping (Refstie and Aulsted, 1975) were used to identify the smelts of the 1991 year-class, which were reared at Stofnfiskur in Southwest Iceland. Body size at tagging were 20.5 g and 17.8 g, for 1989 and 199 I year-classes, respectively. After tagging, all families were stocked together in outdoor concrete ponds at Kollafjiiraur Experimental Fishfarm, one pond for each release site,
L
N
a 0
Fig.
50
1OOh
I Location of the release sites in Iceland used in the project.
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Table 1 Number of smolts released at each release site, number of grilse returning Release site
Year-class 1989 Smelts released (N)
Kollafjijraur Silfurlax Vogavik Lgr6s Total
and return rate
1991 Grilse (N)
39 284 19812 17859 _
960 356 271 _
76955
1587
% Return
Smelts released (N)
2.44 1.80 1.52
30539 8082 7164
Grilse (N) 872 169 145
2.86 2.09 1.87
% Return
_ 2.06
5769 52 154
193 1379
3.35 2.64
and one for the farmed group, beginning in November-December, and kept there until transported to the release site and the land-based farm in April-June. By the time the fish were transported to the release sites and to land-based farms, the body size had increased, for 1989 and 199 1 year-classes, to 28.1 g and 24.3 g, respectively. The smelts of the 1989 year-class were released from Kollafjijraur, Vogavik and Silfurlax, and the 1991 year-class smolts were released from Kollafjoraur, Vogavik, Silfurlax and LB& (Fig. I). The number of released smolts and returning grilse to each release site is given in Table 1. For more detailed information about release sites and release methods, see Jonasson (1996). The body weight and sex of the returning grilse were recorded. In the 1989 year-class, all fish in the land-based unit at Grundartangi were slaughtered in August 1991. The sex, stage of maturation and body weight of 740 fish were also recorded. In the 1991 year-class, the body weight of 2359 fish in the land-based unit at Stofnfiskur was recorded in June 1993. The sex and stage of sexual maturation were also recorded. The sex of immature fish was not recorded for the 1991 year-class. The Grundartangi land-based farm had seawater with full salinity (32%0), and the water was pumped from l-4 m under the sea surface all-year-round. The temperature varied from 0°C in winter, to 14-15°C in summer. At Stofnfiskur land-based farm, the sea water was pumped from boreholes with a temperature of 10-l 1°C and the salinity at 28-32%0 for the first 3 months. For the rest of the test period, the temperature was 6-7°C and salinity was 22-25%0 without any seasonal fluctuations in temperature.
3. Statistical
analysis
The body weights of the returning grilse and fish reared in the land-based farms were analysed. The body weights of the returning grilse were readjusted multiplicatively for the effect of sex within salmon strain and release site. All returning fish were mature; males were significantly larger than females and had larger variances compared to females within the same strain. The correction factor used was obtained by multiplying the individual weight and the ratio of the grand mean body weight to the mean body weight of each sex within the strain and release site. A similar correction was applied for
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the body weight of fish reared in the land-based farms for immature fish and mature males and females. The multiplicative adjustment was chosen due to the observed dependency between the mean and the variance (Table 2). The variance components for body weight (upon return from ranching and after rearing in the land-based farms) were separately estimated according to an animal model for each year-class. The animal model allows both the recorded individuals and the unrecorded parents to be included in the analysis, to consider all known additive genetic relationship between the animals. The model also includes both fixed and random effects, such as: y.ik = Yjk
=
P= r= st, = Uijh = .f,,n = e,,!X=
p + r, + St,, + a,jk +frjk + erjk precorrected body weight of the kth fish overall mean fixed effect of the release site (i = 1-3 for 1989 year-class and i = l-4 for 199 1 year-class) fixed effect of salmon strain (j = l-2) random additive genetic effect of the kth fish the random common full-sib effects for the kth fish due to factors other than additive gene effects random error
The additive effects, the common full-sib effects due to factors other than additive gene effects, and the residual effects were assumed to have independent normal distributions with zero means and variances of q,‘, CT+’ and uP2, respectively. The variance components were estimated from a derivative-free restricted maximum likelihood (df-REML) algorithm (Meyer, 1989) using programmes based on the software (DFUNI) written by Meyer (1991). The variance components for body weight in land-based farms were estimated according to the same model, but excluding the fixed effects of the release sites. Technically, a heritability estimate is a strain-specific character, and should be estimated separately for each strain. However, given the limited number of sires and
Table 2 Number of fish, body weight means (kg) and standard deviations Sea ranching
1989 year-class Mature males Mature females Immature males Immature females 199 1 year-class Mature males Mature females Immatures (sex unknown)
Land-based
N
Mean
S.D.
790 797
2.45a 2.08b
0.43 0.28
847 532
(S.D.) for each year-class
2.47a 2.15b
0.40 0.27
N
farming Mean
S.D.
1.09a 1.I3a
263 118 92 267
0.89b 0.90b
0.25 0.19 0.27 0.24
89 9 2261
0.70a 0.76a 0.69a
0.24 0.24 0.25
Within a column and effect, mean values followed by the same letter are not significantly
different (P < 0.05).
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dams in these data, the accuracy of estimates within strains will be very low. Therefore, an average heritability was determined for each trait incorporating strain as a fixed effect in the model. A future selection programme will most likely focus on a single population. For estimation of the phenotypic and genetic correlation between body weight of sea ranched grilse and body weight of their full- and half-sibs reared in land-based farms, a univariate analysis was run as described above. Subsequently, a bivariate analysis was run, in which the body weight of the returning sea ranched grilse and the body weight of fish in land-based farms were regarded as two different traits. The DFMUW programme (Meyer, 1991) sets the error covariance between the traits to zero since they are not measured on the same animal. When estimating genetic correlation, the common full-sib effect was not included. Because of the complexity of the statistical analysis, it was not possible to estimate the standard errors of the estimated variance and covariance components. Therefore, rough approximates of the standard errors of the genetic correlation were derived using the formulae for full-sib analysis for two continuous traits given by Scheinberg ( 1966).
4. Results
4.1. Effect of sex and sexual maturation
The overall return rate from sea ranching was 2.06% for 1989 year-class and 2.64% for 1991 year-class (Table 1). There was a considerable difference in the mean body weight between fish returning from sea ranching and those reared in the land-based farm (Table 2). Significant differences were observed in the body weight between the sexes returning from sea ranching. A significant difference was observed between the body weight of mature and immature fish in the 1989 year-class, but not in the 1991 year-class. In the 1989 year-class, 5 1% of the fish reared in land-based farm matured, but in the 1991 year-class, only 4.1% matured.
Table 3 Number of salmon strains, sires and dams used per year-class
1989 year-class Sea ranching Land-based farming 199 1 year-class Sea ranching Land-based farming
Strains
Sires
Dams
h’ + s.e.
,f’ * s.e.
2 2
44 41
120 102
0.20+0.10 0.31+0.17
0.04 f 0.04 0.02 f 0.07
2 2
32 32
100 96
0.23f0.12 0.27*0.10
0.06 + 0.052 0.00 f 0.04
Estimates of heritabilitiesfstandard errors (h” +s.e.) for body weight caused by factors other than additive genetics (f’ f s.e.1.
and the effect common
to full-sib
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and genetic parameters
The heritability estimates for the body weight of grilse in salmon ranching were estimated as 0.20 f 0.10 and 0.23 f 0.12, for the 1989 and 1991 year-classes, respectively. The heritabilities for the body weight of grilse in land-based farming were estimated as 0.31 k 0.17 and 0.27 f 0.10, for the 1989 and 1991 year-classes, respectively. The common full-sib effects other than additive genetic effects ranged from 0.004 to 0.06 in both year-classes (Table 3). The phenotypic correlation between the body weight of fish returning from sea ranching and that of farmed fish was estimated to be 0.14 for the 1989 year-class and 0.09 for the 199 1 year-class. The genetic correlation between the body weight in the two environments was estimated to be 0.42 f 0.28 for the 1989 year-class and 0.27 * 0.34 for the 1991 year-class.
5. Discussion Grilse that returned from sea ranching were more than twice as large compared to their sibs in land-based farms. Growth performances similar to those achieved in the farmed groups were reported for Atlantic salmon reared in net-pens in Norway (Gjerde et al., 19941, where the mean body weight was 0.6 kg after being reared 12 months in sea cages. This shows that it is not unusual that salmon grew faster in the open sea around Iceland, compared to their sibs stocked in a land-based fish farm. The reason for this difference is uncertain, as the migration pattern of ranched salmon around Iceland during the first year at sea is not known. Using strains for farming in land-based farms, which were previously used in sea ranching for several generations, may result in stressful conditions during the rearing period leading to deleterious effects on growth rate (Pickering et al., 1991). Thus, the sea-ranched strains are not adapted to captivity and the environmental conditions are not optimal for the fishes in a land-based farm. In ordinary cage farming conditions in Norway, using domesticated salmon from the national breeding programme, the fish grow faster than that in sea ranching (Refstie, personal communications). A significant effect on sex was observed after one year in sea ranching. Males were 17.8% larger then females in the 1989 year-class and 14.9% larger in the 199 1 year-class. Grilse returning in sea ranching are all mature, and no information on immature fish is available. There was no significant difference in size between the sexes observed in land-based farming. The effect of sexual maturation was observed in the 1989 year-class in the land-based farm, where mature fish were 22% larger then immature fish. Similar results were reported by Gjerde et al. (1994) for Atlantic salmon reared one year in the sea. Similar effects on sex and sexual maturation have been reported for Atlantic salmon by Navdal (19831, Gjerde (19861, Gjerde and Refstie (1984) and Rye (1992). There was no effect on sex observed in the year-class 1991. There was a significant difference between year-classes in size and frequency of maturation in the land-based farms. This difference could partly be explained by the time of recording, when all fish in 1989 year-class were slaughtered and measured in
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August 1991, while fish in the 1991 year-class were weighed alive in June 1993, two months earlier than that for 1989 year-class. External characteristics on maturing fish might not have been detectable in June on all the maturing fish. For the 1991 year-class, there were no seasonal temperature fluctuations in the land-based farm which could also affect the frequency of maturation after 12 months of rearing in seawater. The estimated he&abilities (Table 3) indicate significant additive genetic variation for the body weight of returning grilse from sea ranching, and for the body weight of salmon reared 12- 14 months in land-based farms. Gjerde et al. (1994) reported a heritability of 0.30 + 0.06 for Atlantic salmon reared for 12 months in sea cages in Norway. These results show that it is possible to increase the body weight at harvesting in sea ranching programme when selection is applied. The estimated effects common to full-sibs caused by factors other than additive genetics (full-sib group effect, f *, Table 3) were low and insignificant, and very low for the fish raised in land-based farms. Gjerde et al. (1994) reported a similar full-sib effect of 0.08. This is, most likely, a transitory common environmental effect introduced when the full-sib families were reared in separate tanks prior to tagging. However, nonadditive genetic effects cannot be ruled out. The genetic correlation between the body weight upon return to sea ranching and the body weight in land-based farms were low to medium and insignificant. These low genetic correlation is, according to Robertson (1959), a measure of the existence of genotype-environment interaction for a trait measured in two different environments. Similar results, although with higher genetic correlation, were found by Sylven et al. (199 1) while recording growth rate for rainbow trout in fresh, brackish and sea water. These results show that these two traits are probably partly controlled by different sets of genes. The body weight characteristic in the present study is an expression of genetic potential within two widely different environments. In salmon ranching, body weight may be affected by genes controlling survival, age at maturation, success in capturing prey, temperature, behaviour, etc. Growth in land-based farms will be affected by stress sensitivity, temperature, behaviour (e.g., aggression), food conversion efficiency, etc. A strong natural selection in salmon ranching may have reduced the genetic correlation between ranching and land-based farming.
6. Conclusion In a selection programme for salmon ranching, where the breeding goal is increased return rate and body weight, the best selection method would be a combined individual and family selection for body weight, and family selection for return rate, using the returning fish as broodstock. The estimation of family breeding values should be based on their performance in return rate and growth rate in the sea. Therefore, enough smelts must be tagged and released per family to get an accurate estimate of family breeding values. However, low return frequencies occur in sea ranching, which means that there are few fish in each family, leading to the low accuracy of family breeding values and low efficiency of individual selection within families for body weight. Therefore, production of salmon under farming conditions from the same families as released to the
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sea will ensure the selection of broodstock from families with high breeding values, although the returns are very low. If a breeding programme will supply the sea ranching industry, the majority of the broodstock must be produced under farming conditions. The breeding station itself should select and use returning fish as broodstock for the next generation as much as possible. Although the genetic correlations are low between sea ranching and land-based farming for body weight, one should also use the largest fish on the land-based farm as broodstock, but the efficiency of selection for increased body weight may be lower compared to using the returning fish from sea ranching as broodstock.
Acknowledgements The project was financed by the government of Iceland, the Nordic Council of Ministers and the Nordic Industrial Foundation. The project was administered, by, a board with representatives from all the Nordic countries. The members are: Ami Isaksson, chairman, Institute of Freshwater Fisheries, Iceland; Dr. Stefan Adalsteinsson, Institute for Agricultural research, Iceland; Dr. Trygve Gjedrem, AKVAFORSK, Norway; Dr. Lars-Ove Eriksson, Agricultural University of Umea, Sweden; Dr. Unto Eskelinen, Lauka research institute, Finland; Dr. Jens-Ole Frier, University of Aalborg, Denmark; Mr. Andrias Reinert and Mr. Ingvard Fjallstein, Research Institute for Marine Fisheries, Faro Islands. Dr. Jonas Jonasson was project leader and secretary for the board. The authors would like to thank them for their help in the project. Many thanks to Dr. Vigftis Johannsson at Kollafjiiraur Experimental Fishfarm at Kollafjoraur, Iceland for helping in running the project. Special thanks to Dr. Hans B. Bentsen and Dr. Bjame Gjerde, AKVAFORSK, Norway for helping in analysing data and fruitful discussions and comments on the manuscript. The author wishes to thank all the staff at Kollafjiiraur Experimental Fishfarm, the staff at Grundartangi and Stofnfiskur land-based farms, as well as the salmon ranching companies Silfurlax, Vogavik and LBr6s for letting us use their release sites for the release of tagged smolts and recapturing returning fish.
References Falconer, D.S., 1952. The problem of environment and selection. Am. Nat. 86, 75-86. Gjedrem, T., 1986. Breeding plan for sea ranching. Aquaculture 57, 77-80. Gjerde, B., Refstie, T., 1984. Complete diallel cross between five strains of Atlantic salmon. Livestock Prod. Sci. I I, 207-226. Gjerde, B., 1986. Growth and reproduction in fish and shellfish. Aquaculture 57, 37-55. Gjerde, B., Simianer, H., Refstie, T., 1994. Estimates of genetic and phenotypic parameters for body weight, growth rate and sexual maturity in Atlantic salmon. Livestock Production Science 38, 133-143. Isaksson, A., 1988. Salmon ranching: a World review. Aquaculture 75, I-33. Jonasson, J., 1996. Selection experiments in Atlantic salmon ranching II Variation among release sites and strains for return rate, body weight and ratio of grilse to total return. Aquaculture 144, 277-294. Jonasson. J., Gjerde, B., Gjedrem, T., 1997. Genetic parameters for return rate and body weight of sea-ranched Atlantic salmon. Aquaculture (same issue).
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Meyer, K., 1989. Restricted maximum likelihood to estimate variance components for animal models with several random effects using a derivative-free algorithm. Genet. Sel. Evol. 21, 317-340. Meyer, K., 1991. DFREML. Programs to estimate variance components by restricted maximum likelihood using a derivative-free algorithm. User’s Notes. Version 2.0, 84 pp. Naevdal. G., 1983. Genetic factors in connection with age at maturation. Aquaculture 33, 97-106. Pickering, A.D., Pottinger, T.G., Sumpter, J.P., Carragher, J.F., LeBail, P.Y., 1991. Effects of acute and chronic stress in the levels of circulating growth hormone in the rainbow trout, Onchrhwchus mykiss. Gen. Comp. Endocrinol. 78, 194-203. Refstie, T., Aulsted, D., 1975. Tagging experiments with salmonids. Aquaculture 5, 367-374. Robertson, A., 1959. The sampling variance of the genetic correlation coefficient. Biometrics 15, 469-485. Rye, M., 1992. Studies on body traits in Atlantic salmon (Salmo S&r). PhD. Thesis, University of Aas Norway. Scheinberg, H., 1966. The sampling variance of the correlation coefficients estimated in genetic experiments. Biometrics 22, 187-191. Stefansson, S.E., 1994. Production in Icelandic Fishfarming in 1993 (in Icelandic). Report from the Institute of Freshwater Fisheries. VMST-R/94003, 19 pp. Sylven, S., Rye, M., Simianer, H., 1991, Interaction of genotype with production system for slaughter weight in rainbow trout (Oncorhynchus mykiss). Livest. Prod. Sci. 28, 253-263.