Effect of siblings on growth of juvenile coho salmon

Effect of siblings on growth of juvenile coho salmon (Oncorhynchus kisutch) Department of Fisheries and Oceans, Biological Sciences Branch, Pacific Biological Station, Nanaimo, B. C., Canada V9R 5K6

Can. J. Zool. Downloaded from www.nrcresearchpress.com by Fisheries and Oceans on 08/14/15 For personal use only.

Received March 24, 1988 BEACHAM, T. D. 1989. Effect of siblings on growth of juvenile coho salmon (Oncorhynchus kisutch). Can. J. Zool. 67: 601 -605. Five male coho salmon (Oncorhynchus kisutch) were mated to 10 females in a nested mating design, and juveniles from these 10 families were marked and reared for 30 weeks. Juveniles from each family were reared in one of three environments: with full-sibs, with paternal half-sibs, and with all members of the other nine families in a communal tank. Juveniles reared with full-sibs showed the greatest within-family variation in body weight and those reared with nine other .families in the communal environment showed the least, so that the phenotypic expression of body weight was influenced by the degree of kinship of individuals in the environment. Significant genotype - social environment interactions were observed in juvenile body weight, with the average weight of a family member dependent upon the other genotypes present in the rearing environment. BEACHAM, T. D. 1989. Effect of siblings on growth of juvenile coho salmon (Oncorhynchus kisutch). Can. J. Zool. 67 : 601 -605. Cinq Saumons argentks (Oncorhynchus kisutch) miles ont kt6 accouplks h 10 femelles au cours d'une expkrience d'accouplements au nid et les juvkniles issus de ces 10 familles ont kt6 marquks et gardks en klevage pendant 30 semaines. Des juvkniles de chaque famille ont kt6 gardks en trois types de conditions : avec des frkres ou soeurs, avec des demi-frkres ou demi-soeurs paternels et avec des individus des 10 familles h la fois dans un aquarium commun. C'est chez les juvkniles klevks avec leurs propres frkres et soeurs que la masse du corps accuse la plus grande variation intrafamiliale et chez les individus klevks avec les neuf autre familles dans l'aquarium commun qu'elle en accuse le moins, ce qui dkmontre que l'expression phknotypique de la masse du corps est influencke par le degrk de parent6 des individus dans leur milieu. Les interactions gknotype - milieu social se sont av6kes avoir une influence importante sur la masse du corps, car la masse moyenne d'un membre d'une famille dkpend des autres gknotypes prksents dans le milieu d'klevage. [Traduit par la revue]

Introduction In British Columbia, coho salmon (Oncorhynchus kisutch) juveniles may spend 1 or 2 years in freshwater before smolting and migrating to the ocean. While in freshwater, coho salmon juveniles can apparently distinguish between populations (Quinn and Tolson 1986) and between full-sibling groups within populations (Quinn and Busack 1985). However, the effect of sibling recognition on any life history character is uncertain. The timing and size at smolting and migration to the ocean is a major determinant of subsequent survival (Bilton et al. 1982). Size at smolting is a function of growth rate, having both a genetic and environmental component. The environmental component includes such factors as food availability and water temperature, but may also consist of the social environment, given sibling recognition in coho salmon. In hatchery facilities, coho salmon juveniles are reared in high densities compared with the natural environment, and the social component of growth rate may be different than in wild populations. The effect of the social environment on growth rate of coho salmon is currently unknown. The effect of the social environment on growth rate in fish has been examined for some species (Moav and Wohlfarth 1966; Dunham et al. 1982; Wohlfarth and Moav 1985). The social environment that juveniles encounter during rearing may have some influence on their subsequent growth performance. In this study, I investigated the effect of the social environment on growth rates of juvenile coho salmon by rearing full-sib families in isolation, with paternal half-sibs, and in a communal environment. Materials and methods Gametes were collected from 5 male and 10 female wild coho

Printed in Canada 1 Imprimt au Canada

salmon from the Big Qualicum River, located on the east coast of Vancouver Island, on November 20, 1985. The gametes were transported to Rosewall Creek hatchery on Vancouver Island where the experiment was conducted. A nested mating design was used, with each male fertilizing the eggs of two females, producing 10 families. The eggs were fertilized, water-hardened, and then loaded into a vertical stack incubator. Eggs from each family were split into two groups, with each group in an individual container in the incubator. The eggs were reared in well water at approximately 8°C. The salmon remained in these containers until emergence of fry, and thus the embryos and alevins would have been exposed to odours of nonsiblings. Fry emergence occurred on February 24, 1986, when 1000 fry from each family were placed in each of two 1200-L tanks (20 tanks in total used) with a flow rate of 9 - 13.5 Llmin. Full-sibs were reared together for 44 d after ponding. The fish were fed Oregon Moist Pellet daily at a rate of 125% of the manufacturer's recommended amount using automatic feeders and were kept under a simulated natural photoperiod and an average temperature of 8°C during rearing. The experimental design required that families be individually marked. This was accomplished using a hot-branding technique, with up to five brands placed on either the left or right sides of an individual, enough to distinguish the 10 families. The juveniles were judged to be of sufficient size for branding between 2 and 4 g. They were anesthetized and weighed to the nearest 0.01 g on April 9, 1986, and 360 fish from each family were marked. Ten additional 1200-L tanks were allocated to the paternal half-sib rearing (2 families per tank) and two additional 1200-L tanks to communal rearing (10 families per tank); initial loading densities were set at 300 fishltank (Table I). All rearing environments were replicated, so that 600 unmarked fish from each family were reared with full-sibs (300 fish per tank), 300 marked fish from each family were reared with their paternal half-sibs (150 fish per family with two families in each of two tanks), and 60 marked fish from each family were reared in communal tanks (30 fish per family with 10 families in each of two tanks) (Table 1).

CAN. J . ZOOL. VOL. 67, 1989

602

TABLE1. Distribution of families to tanks after initial branding of the juveniles Full-sib


Family Tank

N

Half-sib

Communal

Tank Family N

Tank Family N

TABLE2. Percentage of total phenotypic variation in juvenile weight due to sires, dams, and replicates (tanks) and remainder for 10 families of coho salmon reared for 30 weeks after marking Period (weeks)

Sire

Dam

Replicate

Remainder

Marking Full-sib 6 12 18 24 30 Half-sib 6 12 18 24 30 Communal 6 12 18 24 30 NOTE:All tanks contained 300 fish. In any tank in the full-sib environment, only one family was present, whereas two families were present in the half-sib environment and 10 families were present in the communal environment. N is the number of individuals of each family in each tank.

After the weighing, marking, and distribution to tanks on April 9, 1986, the fish were weighed five times at 6-week intervals through October 28, 1986. At each weighing period, 30 fish per family in each tank were weighed. This meant that at each sampling period, 10% of the individuals in the full-sib tanks were weighed, as were 20% in the half-sib tanks and 100% in the communal tanks. Individuals in the full-sib and half-sib environments were randomly chosen at each sampling period. Different individuals in each family were thus likely weighed at each sampling period in the full-sib and half-sib environments, but the same individuals in each family were always weighed in the communal environment. Variation in juvenile weight for the fish reared with full-sibs was analyzed with the following model:

xjkl

is the observed weight, p is the mean, Mi is the effect of where male (i = 1- 5), Fjjis the effect of female j mated to male i ( j = 1 or 2), Rjjkis the effect of replicate within family (k = 1 or 2), and ejjklis the random error for the lth individual in subgroup ijk. Variation in juvenile weight for the fish reared with their paternal half-sibs was analyzed with the following model:

with the terms defined as previously except for Rik, which is effect of replicate (k = 1 or 2). Variation in juvenile weight for the fish reared in communal tanks was analyzed with the following model:

with the terms defined as previously except for Rk which is the effect of replicate (k = 1 or 2). Variation in relative family weight among the three rearing environments was analyzed with the following model :

where Ek is the effect of rearing environment (k = 1 - 3), MEjkis the interaction between males and rearing environment, and FEU, is the

NOTE:Families were reared with full-sibs, with their paternal halfsibs, or with all families present (communal).

interaction between females within males (individual families) and rearing environment; the other terms are defined as previously. All effects except rearing environment were considered random. Variance components for each effect were determined using method 1 of Henderson (1953) for eqs. 1- 3 and method 3 for eq. 4. Genetic covariances between juvenile weights in each environment were approximated from replicate means using a random effects model incorporating sires and dams. Genetic correlations were determined from the genetic covariances and the genetic variances from single trait analyses. Standard errors of the genetic correlations were determined using the method of Mode and Robinson (1959). Coefficients of variation were compared by sign test analysis (Mendenhall 1971). A comparison was scored plus when the family coefficient of variation (CV) for weight was less in the communal environment when compared with either the half-sib or full-sib environment. Otherwise it was scored minus. When the family CV in the half-sib environment was less than in the full-sib environment, the comparison was scored plus; the alternative was minus.

Results Growth rate The juvenile coho salmon averaged 3.1 g in weight when they were marked. At that time, significant differences in juvenile weight were observed between tanks within families and between offspring of females mated to the same male (both P < 0.05), but not among offspring of different males (P > 0.05). Variance between females accounted for 34% of the total phenotypic variation, and was the largest source of variation observed (Table 2). The juveniles from each family were then combined by tank and distributed to the three environments examined and weighed again after 6 weeks of rearing. Significant differences in mean juvenile weight occurred among the three rearing environments ( F 2 , 8 = 10.22, P < 0.01). The heaviest juveniles were observed in the communal tanks (overall mean weight = 7.86 g) and the lightest in the full-sib tanks (mean weight = 6.78 g). The weights

BEACHAM

TABLE3. Coefficient of variation (%) of weight for 10 families of juvenile coho salmon reared for 30 weeks, where juveniles

were reared with their full-sibs only (FS), with their full-sibs and half-sibs (HS), and with their full-sibs, half-sibs, and unrelated individuals (C)

6 weeks


Family

FS

HS

12 weeks C

FS

HS

18 weeks C

FS

HS

24 weeks C

FS

HS

30 weeks C

FS

HS

C

1 2 3 4 5 6 7 8 9 10 Mean

of juveniles were also more variable in the full-sib tanks than in the communal tanks (Table 3). Maternal effects continued as a significant source of variation in juvenile weight (Table 2). Similar results were observed for the sampling periods 12 and 18 weeks after marking. Twenty-four weeks after marking, no significant difference in weight was observed among the three rearing environments (F2,8 = 0.67, P > 0.10). Coho salmon reared in the communal tanks were still the heaviest (14.70 g) and those reared in the half-sib tanks were the lightest (14.04 g), but the difference was not significant. However, juveniles reared in the fullsib tanks were still more variable in weight than those reared in the other environments (Table 3). When the experiment was terminated on October 28, 1986, no significant difference in overall mean weight was observed in the three rearing environments. Extensive variation in growth rates occurred among families within rearing environments, with the two fastest-growing families more than 100% heavier than the two slowest-growing families at the end of the experiment (Fig. 1). Relative variation in juvenile weight remained the same throughout the experiment, with the least variation observed in the communal tanks and the greatest variation observed in the full-sib tanks (Table 3). Significantly less variation in weight within families was, on average, observed in the communal environment relative to the half-sib (35 +, 15 -; P < 0.05) or full-sib environments (33+, 17-; P < 0.05) (Table 2). No significant difference was observed between the half-sib and full-sib environments (27 , 23 - ; P > 0.05). In all three environments, maternal effects generally declined as the fish grew, and were absent after 30 weeks of growth (Table 2). Variation between replicates usually accounted for less than 3% of the total observed phenotypic variation (Table 2), indicating that environmental differences among tanks did not tend to accumulate.

P > 0.05). However, after 24 weeks of rearing, significant differences in the relative weights of families in the three rearing environments were observed (Flo,21m = 1.9 1, P < 0.05), indicating a genotype -environment interaction. Significant interactions were also observed in the two-environment comparisons between the full-sib and half-sib, full-sib and communal, and half-sib and communal environments. At the end of the experiment, the interactions remained significant (F10,21m= 2.19, P < 0.05), with the family x environment interaction accounting for an increasing proportion (0% at 6 weeks, 1% at 30 weeks) of phenotypic variation in juvenile weight over time. This interaction occurred because the same family did not necessarily have the same relative body weight in all three environments. For example, at the end of the experiment, juveniles from family 4 were the fifth lightest in the full-sib environment but the third lightest in the half-sib and communal environments (Fig. 1). The rearing density was equal in all tanks in the three environments, so that the growth performance of a family could be dependent upon other genotypes present. Increasing genotype-environment interactions could be detected by a declining genetic correlation between juvenile weights in the different environments as the juveniles grew. A declining genetic correlation indicates that predictability of weight of a specific family reared in different environments becomes more uncertain. This decrease in predictability is illustrated by the genetic correlation based upon dam (family) variance components between juvenile weights in the full-sib environment and those in the other two environments (Table 4). The genetic correlations declined with rearing time, indicating an increasing interaction and different relative trends among families in the three environments with respect to growth (Fig. 1).

Effect of siblings The significance of the effect of the social environment was investigated by examining the magnitude of the family x rearing environment interaction in eq. 4. After 6 weeks of rearing after marking, no significant interaction was observed (F10,2111 = 1.06, P > 0. lo), indicating that the relative growth of a family was independent of its rearing environment. Similar results were also observed after 12 (F10,2111 1.65, P > 0.05) and 18 weeks of rearing (F10,2108 = 1.74,

Discussion The results of the experiment suggest that social environment can influence the growth rates of individual juvenile coho salmon, as well as the amount of phenotypic variation in body size within a family. Phenotypic variation in body weight was the greatest when full-sibs were reared together, and least when families were reared communally. The more uniform body weight of families in the communal environment and the intermediate variation in the half-sib environment suggests

+

CAN. J. ZOOL. VOL. 67, 1989

604


2 '

: 0

I

I

6

12

I

18

COMMUNAL

H A L F -SIB

ISOLATION

I

24

I

I

30

0

I

I

6

12

WEEKS

I

18

AFTER

I

I

24

30

I

'

0

I

6

I

12

I

18

lo

/

1

24

I

30

MARKING

FIG. 1. Mean weight (g) for 10 families of coho salmon reared for 30 weeks after initial marking with families isolated from each other (full-sib), with paternal half-sibs reared in the same tank (half-sib), and with all 10 families in a tank (communal). TABLE4. Genetic correlations based upon sire and dam variance components for juvenile weight up to 30 weeks after marking for juveniles reared with full-sibs (F), with their paternal half-sibs (H), and in a communal environment (C) (standard errors of the estimates are in parentheses)

Period (weeks)

Sire components F vs. H

F vs. C

Dam components H vs. C

some socially mediated effect on the phenotypic expression of body weight that is proportional to the degree of kinship or the number of nonsiblings in the environment. The different growth responses of juvenile coho salmon reared in the three environments suggest that kin can recognize each other, even though all families were maintained in a common environment (the vertical stack incubator) until emergence of fry. Coho salmon siblings may recognize each other by phenotype matching (Holmes and Sherman 1983), whereby an individual learns its own phenotype or those of its familar kin by association. For coho salmon, this appears to occur by chemoreception (Quinn and Hara 1986). The coho salmon juveniles appear to have learned the characteristics of their siblings during rearing before they were marked. Coho salmon do not distinguish siblings from nonsiblings and maternal halfsiblings if they are reared in a common environment from fertilization until a few months after fry emergence (Quinn and Hara 1986). The general adaptive value of sibling recognition

F vs. H

F vs. C

H vs. C

may be that it encourages schooling behaviour, which may enhance survival rate by a number of means (Shaw 1978). However, coho salmon juveniles usually establish territories a few weeks after fry emergence (Chapman 1962), so the adaptive value of sibling recognition in coho salmon needs to be examined further. It may be that sibling recognition is simply a subset of a population recognition response (Quinn and Hara 1986), particularly if, as my study suggests, population recognition or imprinting in wild populations occurs shortly after fry emergence from the redd. Maternal effects on body weight generally declined as the juveniles grew, as they did among other juvenile salmonids (Robinson and Luempert 1984; Iwamoto r :al. 1984; McKay et al. 1986). Maternal effects are largely due to initial egg size or quality differences among females. Substantial additive genetic variation for juvenile body weight was observed in the Big Qualicum River coho salmon population, similar to populations in other locations (Hershberger et al. 1982; Iwamoto


BEACHAM

et al. 1984). However, the expression of the additive genetic variation was dependent upon the rearing environment. In an evaluation of strain performance of growth rates, one procedure has been to rear different strains in a communal environment to reduce the number of tanks or ponds allocated to the experiment (Dunham et al. 1982; Moav and Wohlfarth 1974; Wolhfarth and Moav 1985). The objective of such work is to identify the faster-growing strains that can be subsequently used in commercial production. In commercial production, the strain would be reared in isolation, so it is necessary to confirm that growth rates are the same in both environments. No significant intergenotypic competition has been observed for fish species reared in commercial environments (Dunham et al. 1982; Wohlfarth and Moav 1985). The coho salmon study was terminated 30 weeks after marking because of logistical limitations; an extension of the study would be to evaluate growth rates of specific families in different social environments until they reached sexual maturity.

Acknowledgments The study on the effect of social environment on body weight of juvenile coho salmon was developed from unpublished work of Dr. Craig A. Busack. Clyde Murray and Wally Barner branded ,the juvenile coho salmon, Grant Johnston weighed the juveniles at the appropriate times, and ,the rest of the staff at the Rosewall Creek hatchery maintained ,the salmon. Two anonymous referees provided constructive criticism of the manuscript. BILTON,H. T., ALDERDICE, D. F., and SCHNUTE, J. T. 1982. Influence of time and size at release of juvenile coho salmon (Oncorhynchus kisutch) on return at maturity. Can. J. Fish. Aquat. Sci. 39: 426-447. CHAPMAN, D. W. 1962. Aggressive behaviour in juvenile coho salmon as a cause of emigration. J. Fish. Res. Board Can. 19: 1047- 1080. DUNHAM, R. A., SM~THERMAN, R. O., CHAPPELL, J. A., YOUNGBLOOD, P. N., and BICE,T. 0 . 1982. Communal stocking and multiple rearing technique for catfish genetics research. J. World Maric.

605

SOC.13: 26 1- 267. HENDERSON, C. R. 1953. Estimation of variance and covariance components. Biometrics, 9: 226 -252. R. N., and SAXTON, A. M. 1982. HERSHBERGER, W. K., IWAMOTO, Genetic potential for fresh- and seawater growth of net-pen cultured coho salmon. In Proceedings of the North Pacific aquaculture symposium, Anchorage, AK, August 1980. Edited by B. R. Melteff and R. A. NevC. University of Alaska, Alaska Sea Grant Report 88-2. pp. 185-192. HOLMES,W. G., and SHERMAN, P. W. 1983. Kin recognition in animals. Am. Sci. 71: 46-55. IWAMOTO, R. N., ALEXANDER, B. A., and HERSHBERGER, W. K. 1984. Genotypic and environmental effects on the incidence of sexual precocity in coho salmon (Oncorhynchus kisutch). Aquaculture, 43: 105- 121. MCKAY,L. R., IHSSEN,P. E., and FRIARS,G. W. 1986. Genetic parameters of growth in rainbow trout, Salmo gairdneri, prior to maturation. Can. J. Genet. Cytol. 28: 306 - 3 12. MENDENHALL, W. 1971. Introduction to probability and statistics, 3rd ed. Duxbury Press, Belmont, CA. MOAV,R., and WOHLFARTH, G. W. 1966. Genetic improvement of yield in carp. FA0 Fish. Rep. 44(4): 12- 29. 1974. Magnification through competition of genetic differences in yield capacity in carp. Heredity, 33: 181-202. MODE,C. J., and ROBINSON, H. F. 1959. Pleiotropism and the genetic variance and covariance. Biometrics, 15: 5 18-537. QUINN,T. P., and BUSACK, C. A. 1985. Chemosensory recognition of siblings in juvenile coho salmon (Oncorhynchus kisutch). Anim. Behav. 33: 51 -56. QUINN, T. P., and HARA, T. J. 1986. Sibling recognition and olfactory sensitivity in juvenile coho salmon (Oncorhynchus kisutch). Can. J. Zool. 64: 921 -925. QUINN,T. P., and TOISON,G. M. 1986. Evidence of chemically mediated population recognition in coho salmon (Oncorhynchus kistuch). Can. J. Zool. 64: 84 - 87. 0. W., and LUEMPERT, L. G. 1984. Genetic variation in ROBINSON, weight and survival of brook trout (Salvelinus fontinalis). Aquaculture, 38: 155 - 170. SHAW,E. 1978. Schooling fishes. Am. Sci. 66: 166- 175. WOHLFARTH, G. W., and MOAV,R. 1985. Communal testing, a method of testing the growth of different genetic groups of common carp in eastern ponds. Aquaculture, 48: 143- 157.