Precocial male maturation in laboratory-reared populations of chinook salmon, Oncorhynchus tshawytscha

ERIC B. TAYLOR Department of Zoology, University of British Columbia, Vancouver, B. C. , Canada V6T 2A9

Received August 8, 1988

TAYLOR, E. B. 1989. Precocial male maturation in laboratory-reared populations of chinook salmon, Onchorhynchus tshawyt- scha. Can. J. Zool. 67: 1665-1669.

The incidence of precocial male maturation in yearling chinook salmon, Oncorhynchus tshawytscha, was examined in four laboratory-reared populations. Slim Creek and Bowron River chinook salmon were about 4 weeks older than Harrison and Nanaimo river chinook salmon when sampled (14 vs. 13 months of age), but were also 20-40 g smaller. Approximately 29, 12, 0, and 0 % of all males were precocious in Bowron River, Slim Creek, Harrison River, and Nanaimo River chinook salmon, respectively. Precocial male chinook salmon had gonadosomatic indices of about 5 -6%, whereas immature salmon from all populations had indices under 1 % . Precocial male chinook salmon were more robust bodied than immature salmon; precocial males had deeper bodies, deeper heads, and larger adipose fins. Variation among the study populations in the inci- dence of precocial male maturation may be related to differences among the populations in migration distance to the sea or in juvenile freshwater rearing life history. The chinook salmon would probably be a productive species with which to study the evolutionary ecology of precocial maturity in Pacific salmonids.

TAYLOR, E. B. 1989. Precocial male maturation in laboratory-reared populations of chinook salmon, Onchorhynchus tshawyt- scha. Can. J. Zool. 67 : 1665-1669.

La frkquence de la maturation prCcoce des miles chez des Saumons chinook, Oncorhynchus tshawytscha, de 1 an a fait l'objet d'une Ctude chez quatre populations de laboratoire. Les saumons du ruisseau Slim et de la rivikre Bowron Ctaient igCs d'environ 4 semaines de plus que les saumons des rivikres Harrison et Nanaimo au moment de la capture (14 vs. 13 mois), mais ils Ctaient aussi de 20 h 40 g plus 1Cgers. Environ 29% de tous les saumons miles de la rivikre Bowron, 12% des saumons miles du ruisseau Slim et 0% des saumons miles des rivikres Harrison et Nanaimo Ctaient prCcocks. Les saumons prCcoces avaient un indice gonadosomatique d'environ 5 -6%, alors que les saumons immatures de toutes les populations avaient un indice infkrieur h 1 % . Les miles prCcoces avaient le corps plus robuste que les saumons immatures; les miles prCcoces avaient le corps plus haut, la tCte plus haute et les nigeoires adipeuses plus grandes. La variation dans la maturation des miles prCcoces chez les populations CtudiCes est probablement relike h des diffkrences dans la distance parcourue au cours de la migration ii la mer chez les populations d'origine, ou h des diffkrences dans le cycle en eau douce au cours de 1'Clevage chez les jeunes saumons. Le Saumon chinook constitue probablement un espkce propice h 1'Ctude de 1'Ccologie kvolutive de la maturitC prCcoce chez les salmonidCs du Pacifique.

[Traduit par la revue]

Introduction Size polymorphism in breeding populations of mature

males, consisting of "large" and "small" individuals, occurs in a number of fish families (Hanson and Smith 1967; Kodric- Brown 1977; Dominey 1980; Warner and Hoffman 1980; Gross 1982, 1985; Ryan 1988). The smaller and sometimes younger mature males are often called precocial males. In anadromous species of Salmonidae, precocial maturation may include males that mature without going to sea, a situation par- ticularly well documented for Atlantic salmon, Salmo salar (Dalley et al. 1983; Myers et al. 1986; Meerburg 1986). Myers et al. (1986) reported that in some Atlantic Canada populations of S. salar , as high as 100% of the male parr population may mature precociously. In the Pacific salmon Oncorhynchus, precocial sexual maturation has received less concentrated study but has been reported in sockeye, 0. nerka, chinook, 0. tshawytscha, and masu salmon, 0. masou (Ricker 1938; Robertson 1957; Gebhards 1960; Utoh 1977). There are several reports of precocial chinook males occurring in wild populations (Rutter 1904; Rich 1920; Synder 193 1 ; Gebhards 1960; Flain 1970). In the Salmon River, a tributary of the upper Columbia River, precocial males were found to occur at a frequency of about 2.6% (Gebhards 1960), whereas as many as 29 % of examined males were precocious in a New Zealand population (Flain 1970).

Documentation of precocial maturation is important both for its demographic and evolutionary implications and in an

applied sense because precocial maturation may limit produc- tion in aquacultural operations. Here, I document the inci- dence of precocial males in four populations of chinook salmon reared from eggs in the laboratory for 14 months.

Materials and methods The chinook salmon sampled in this study were from four popula-

tions used in a laboratory study of behavior of juvenile chinook from stream- and ocean-type populations (E. B. Taylor, in preparation). The four populations were the following: Slim Creek, Bowron River, Nanaimo River, and Harrison River. Bowron River and Slim Creek are upper Fraser River tributaries located about 60 and 80 km upstream, respectively, from Prince George, B. C. The Harrison River empties into the Fraser River about 100 km upstream from Vancouver, and the Nanaimo River drains into the Strait of Georgia at Nanaimo, B. C., on southeastern Vancouver Island. The Nanaimo River gametes were obtained from the "middle river'' spawning sub- population (see Carl and Healey 1984). For each population, eggs and milt were obtained from mature adult chinook salmon and the eggs were fertilized in the field during the fall of 1986. Procedures for the collection of adults, field spawning of gametes, and transpor- tation of zygotes are detailed by Taylor (1988). For each population, gametes were obtained from a small number of males and females (Slim Creek: 6 males x 7 females; Bowron River: 10 males x 10 females; Nanaimo River: 8 males x 6 females; Harrison River: 5 males x 5 females). Incubation of zygotes and larvae was com- pleted at 8OC in an apparatus described by Murray and McPhail (1988). Briefly, the incubation apparatus consisted of a 1.8 x 0.6 x 0.9 m insulated cooling unit. Zygotes were placed on plastic trays

Printed in Canada 1 Imprime au Canada

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

McM

aste

r U

nive

rsity

on

11/1

2/14

For

pers

onal

use

onl

y.

1666 CAN. J. ZOOL. VOL. 67, 1989

situated on racks within the cooling tank. Aeration was provided by air bubblers and water flow was set at about 2 Llmin. Incubating zygotes and larvae were kept in darkness, except for brief daily inspection periods.

Upon emergence (when yolk sacs of larvae have almost been absorbed) about 1500 fry from each population were placed in 97-L fiberglass troughs supplied with dechlorinated water at 4 Llmin. Thereafter, juveniles were fed Oregon moist pellet fish food on a schedule of rations and pellet sizes available from the manufacturer and designed to promote maximum growth. Light-dark schedule followed the natural photoperiod and included a 0.5-h dawn and dusk period each day. Water temperature fluctuated seasonally between 5 and 16°C. To accommodate the increasing size of the growing salmon, 250 juvenile chinook from each population were transfered to 900 L oval fiberglass tanks at 3 months of age. In these tanks water flow, photoperiod, and temperature conditions were as described for the rearing troughs. In this manner, under identical conditions, the juvenile salmon were maintained until they reached approximately 14 months of age. Growth was monitored at monthly intervals by tak- ing weight and length (standard and fork length) measurements on a random sample of 30 individuals per population. Specific growth rates (SGR) were calculated as

SGR = ln(W,IWo) . 100. d- '

where W, and Wo are the final and initial mean wet weights over the time period (in days) for each experimental population (Clarke and Shelbourn 1986).

At between 12.5 and 14 months of age, all surviving juveniles ( < 20 % natural mortality for each population) were killed in a strong solution of 2-phenoxyethanol and scored for male sexual maturity on the basis of external appearance. Mature males were recognized by dark coloration and by the presence of running milt when slight pres- sure was applied to the abdomen. After this preliminary sorting, all mature males and 50 randomly selected immature fish per population were preserved (10% formain) for more detailed- exiiination. Detailed examination consisted in enumerating the number of males and females by gonad examination and in excising the gonads from all males. Body weight and gonad weight were then determined for all precocial males and for all males in the subsamples of 50 fish for each population. I estimated the percent occurrence of precocial males in the following way. First, I estimated the total number of males in each population from the ma1e:female ratios in the sample of 50 immature fish per population. For each population I then divided the number of precocial males by the estimated total number of males in each sample population and multiplied this value by 100 to obtain the estimated percentages of precocial males per popula- tion. Gonadosomatic index was calculated as gonad weightlbody weight x 100.

After gonad excision, body shape differences between mature and immature male chinook salmon were quantified by measuring stan- dard length, head length, head depth, body depth (Hubbs and Lagler 1967), the distance from the snout to the anterior insertion of the pel- vic fin (Riddell and Leggett 1981) and adipose fin length (Beacham and Murray 1983). Measurements were taken with dial calipers on the left side of each fish. Group means (precocial vs. immature males within populations) were compared after adjustment to a common standard length, using analysis of covariance after slope homogeneity and variance homogeneity (Bartlett 's test), were verified.

Results Juvenile chinook salmon from the Harrison and Nanaimo

rivers were heavier at emergence and had higher specific growth rates over their first 12 months of age than did the laboratory-reared chinook from Slim Creek and Bowron River (Table 1). Of the four populations sampled only Bowron River and Slim Creek had precocious males: approximately 29 and 12 % of males, respectively (Table 2). These percentages can

only be considered approximations because the total number of males in each population was not determined. Rather, I used the male:female ratios from the subsample of 50 immature fish from each population (Table 2) to calculate the approximate percent incidence of precocial males. Gonadosomatic index averaged about 5 - 6 % for precocious males from both popula- tions in contrast to values well below 1 % for immature males from Slim Creek and Bowron River and for the larger, imma- ture males from Nanaimo and Harrison rivers (Table 3). The gonads of all immature males appeared "threadlike" with some anterior widening corresponding to gonad development stages I to I1 of Utoh (1977). In contrast, gonads of precocious males filled most of the abdominal cavity (stages V to VI of Utoh 1977).

Precocious males were readily identifiable on sight because of their distinct bronze -yellow body coloration, parr marks, and heavy black speclding on their dorsolateral surfaces, which faded to fine dark speckling and yellow coloration along the ventrolateral surfaces. The anal fins of precocious males had distinct white anterior margins and a general yellow shad- ing with heavy black speckling. In contrast, immature males (and females) had characteristic smolt shading; they were bright silver along the sides, with no distinct parr markings, and they had dark dorsal surfaces. The anal fins of immature male chinook salmon lacked distinct white margins and were largely transparent. For both Slim Creek and Bowron River chinook salmon, precocious males were also morphologically distinct from immature males; mature males were more robust bodied with deeper bodies and heads and with larger adipose fins (Table 4). Slim Creek precocious and immature males also differed in the distance from the snout to the anterior insertion of the pelvic fin but not in head length, whereas Bowron River precocious and immature chinook males did not differ in either of these two characters (Table 4). For both Slim Creek and Bowron River chinook salmon, precocious males were significantly larger than immature males of the same age (t-tests, both P < 0.001, Table 4).

Discussion Evidence for interpopulation variation in the incidence of

precocial male maturation exists in salmonids (Dalley et al. 1983; Myers et al. 1986; Shirahata 1985 cited in Thorpe 1987) and includes anecdotal information for chinook salmon (Rich 1920; Synder 1931). Variation in the percentage of precocial males among the laboratory-reared chinook salmon popula- tions must, however, be interpreted with caution because in the populations without precocial males (Harrison and Nanaimo rivers), males were up to 6 weeks younger and, in nature, would not spawn for a further 3 months. These two limitations of the data may have precluded detection of preco- cial maturation in male Nanaimo and Harrison chinook salmon. Nevertheless, several factors suggest that the study populations differ in the incidence of precocial male matura- tion (see also Ricker 1972). First, Harrison and Nanaimo chinook salmon were larger and grew faster over their first 6 and 12 months than Bowron and Slim chinook (Table 1). From their experiments on brook trout, Salvelinus fontinalis, McCormick and Naiman (1984) concluded that age and growth rate were subordinate to size in influencing maturation rate; yet, in my study the larger, faster growing Harrison and Nanaimo chinook salmon showed no signs of imminent maturity. Second, Harrison and Nanaimo chinook salmon are

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

McM

aste

r U

nive

rsity

on

11/1

2/14

For

pers

onal

use

onl

y.

TAYLOR

TABLE 1. Mean f SE wet weights at emergence and at 6 and 12 months of age (N = 30), and mean specific growth rates at 6 (N = 6) and 12 (N = 12) months of age for

juvenile chinook salmon from the four study populations

Specific growth rate Body weight (g) ( % body wt. /day)

Population Emergence 6 months 12 months 6 months 12 months

Bowron River 0.34f 0.005 9.51 f 0.37 28.7f1.51 1.68 1.07 Slim Creek 0.37f 0.005 5.62f 0.27 28.3f 1.49 1.60 1.01 Harrison River 0.47f 0.009 38.1 f 2.30 69.4f 2.53 2.49 1.68 Nanaimo River 0.41 f 0.003 13.3f 0.64 76.8f 4.41 2.08 1.74

TABLE 2. Numbers of precocious male chinook salmon from the laboratory-reared populations

No. of Age No. precocious Sex ratio % precocious

Population (months) examined males (M:F)" males

Harrison River 12.5 176 0 1.1:l 0 Nanaimo River 13.5 204 0 1.2: 1 0 Bowron River 14.0 173 22 1:1.2 29 Slim Creek 14.0 220 15 1.3: 1 12

'Determined from a subsample of 50 individuals.

TABLE 3. Body weight, gonad weight, and gonadosomatic index (GSI) of mature and immature male chinook salmon from the labora-

tory-reared populations

Body weight Gonad weight Population N (g) (g) GSI

Harrison River 20 64.5 f 4.37 0.12f 0.02 0.19f 0.04 NanaimoRiver 20 81.0f4.01 0.49f0.09 0.50f0.18 Bowron River

Immature 20 36.7f 1.41 0.03 f 0.01 0.09f 0.03 Precocious 20 47.4f 2.61 2.68f 0.36 5.48f 0.39

Slim Creek Immature 20 37.9f 1.10 0.03 f 0.01 0.08f 0.01 Precocious 15 58.8f 4.61 3.29f0.46 5.78f 0.53

NOTE: Values are means f SE.

predominantly ocean type, undergoing smoltification and sea- ward migration within 3 months after emergence (Carl and Healey 1984; Shepherd et al. 1986). In contrast, Slim Creek and Bowron River chinook salmon are predominately stream type and migrate seaward as yearlings (Fraser et al. 1982; Shepherd et al. 1986). Consequently, wild Harrison and Nanaimo chinook males probably do not mature precociously in freshwater since they are normally ocean residents during the late summer and fall of their 1st year or the spring of their 2nd year when precocial male chinook are found in wild popu- lations (Rutter 1904; Gebhards 1960; Flain 1970). Third, Slim Creek and Bowron River are interior populations located at least 600 km upstream from the sea, whereas Harrison River and Nanaimo River are lower Fraser River or coastal popula- tions. Migration distance (as a measure of migration difficulty) may promote differentiation among salmonid populations in age at maturity (Ricker 1972; Schaffer and Elson 1975; Thorpe and Mitchell 1981) and a "cost of migration vs. preco- cial maturation" argument predicts a higher incidence of

precocial male maturation in inland populations of chinook salmon (e.g., Slim Creek and Bowron River). In support of this argument, both Rich (1920) for the Columbia River and Synder (1931) for the Klamath River found precocial chinook salmon males in upstream reaches of each drainage but not in short, coastal streams.

Precocial male maturation in Bowron and Slim chinook salmon was probably not an artifact of laboratory rearing. I located a preserved chinook salmon specimen in the Univer- sity of British Columbia Fish Museum which was collected from the Bowron River in August 1956 (catalogue No. BC 56-608). This specimen had a preserved weight of 26.1 g and a gonadosomatic index of 7.01, was robust bodied, and appeared much as the precocial males from the laboratory- reared Bowron population. Furthermore, the author has seen large (100- 150 mm, SL) and what appeared to be precocious, chinook salmon juveniles on the spawning grounds in Slim Creek while snorkelling during late July of 1985 and 1986. Both Bowron River and Slim Creek adult chinook salmon initiate spawning in middle to late August (Shepherd et al. 1986; personal observation). Finally, the age of the precocial males from my laboratory-reared populations (14 months) cor- responds closely with Gebhards' (1960) observation that in the Lemhi River (upper Columbia River drainage) "all the yearling chinook salmon found in the drainage after high water in June were precocious males."

Precocial males were significantly larger than immature males at 14 months of age (Table 3). The precocious males may have been the faster growing members of the cohort or may have been larger than average at emergence and main- tained this size advantage over the rearing period. The former explanation is consistent with the positive correlation between growth rate and maturation rate in salmonids (Thorpe 1986), but my data are inadequate to evaluate these alternative expla- nations. Body coloration and morphology also differentiated precocial and immature male chinook salmon (Table 4),

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

McM

aste

r U

nive

rsity

on

11/1

2/14

For

pers

onal

use

onl

y.

CAN. J. ZOOL. VOL. 67, 1989

TABLE 4. Mean f SE (cm) body and fin dimensions for immature and precocious male chinook salmon

Adipose fin Population N Body depth Head depth Head length SNAPE length

-

Bowron River Precocious 20 3.42f0.04 a 2.85f 0.04 a 3.57f 0.05 a 7.75f 0.04 a 1.20f 0.02 a Immature 20 2.93f0.04 b 2.56f 0.04 b 3.46f 0.05 a 7.74f 0.04 a 1.03f 0.03 b

Slim Creek Precocious 15 3.52f 0.07 a 2.84f 0.04 a 3.54f 0.10 a 7.92f 0.05 a 1.32f 0.02 a Immature 20 2.98f 0.05 b 2.50f 0.03 b 3.53f 0.09 a 7.76f 0.04 b 1.01 f 0.02 b

NOTE: Means are adjusted to a standard length of 14.1 cm for Bowron River chinook and 14.3 cm for Slim Creek chinook salmon. Within populations, those means not followed by the same letter are significantly different from each other (P < 0.05). SNAPE, distance from the snout to the anterior insertion of the pelvic fin.

differences that may be functionally important. The silvery countershading of immature males reflects their recent status as yearling smolts (Hoar 1988). In contrast, robust body form and coloration may be important in male -male interactions during breeding in salmon (Hanson and Smith 1967; Schroder 1982; Myers and Hutchings 1987; Foote 1987), and precocial males interact to establish size-related dominance hierarchies behind pairs of spawning adults (Gebhards 1960; Myers and Hutchings 1987). The greater size of the adipose fin of pre- cocial male chinook salmon in my study is consistent with the data of Beacham and Murray (1986) and suggests that, in addi- tion to sexual dimorphism (Beacham and Murray 1983), male adipose fin size may depend on the state of maturity. The large size, distinctive coloration, and robust bodies of precocial male chinook salmon in my study are also consistent with observations by Robertson (1 957), Gebhards (1 960), and Flain (1970) for other chinook salmon populations.

Acknowledgements

I thank the staffs of the Quesnel, Harrison, and Nanaimo rivers hatcheries and C. J. Foote for field assistance. C. J. Foote also provided helpful suggestions and discussion. I also appreciate the constructive comments on this paper by Dr. T. D. Beacham and an anonymous reviewer. This research was supported by a Natural Sciences and Engineering Research Council of Canada operating grant awarded to P. A. Larkin.

BEACHAM, T. D., and MURRAY, C. B. 1983. Sexual dimorphism in the adipose fin of Pacific salmon (Oncorhynchus). Can. J. Fish. Aquat. Sci. 40: 2019-2024.

1986. Sexual dimorphism in length of upper jaw and adipose fin of immature and maturing Pacific salmon (Oncorhynchus). Aquaculture, 58: 269-276.

CARL, L. M., and HEALEY, M. C. 1984. Differences in enzyme fre- quency and body morphology among three juvenile life history types of chinook salmon (Oncorhynchus tshawytscha) in the Nanaimo River, British Columbia. Can. J. Fish. Aquat. Sci. 41: 1070 - 1077.

CLARKE, W. C., and SHELBOURN, J. E. 1986. Delayed photoperiod produces more uniform growth and greater seawater adaptability in underyearling coho salmon (Oncorhynchus kisutch) . Aquaculture, 56: 287 -299.

DALLEY, E. L., ANDREWS, C. W., and GREEN, J. M. 1983. Preco- cious male Atlantic Salmon parr (Salmo salar) in insular New- foundland. Can. J. Fish. Aquat. Sci. 40: 647-652.

DOMINEY, W. J. 1980. Female mimicry in male bluegill sunfish - a genetic polymorphism? Nature (London), 284: 546 - 548.

FLAIN, M. 1970. Precocious male quinnat salmon Oncorhynchus tshawytschu (Walbaum) in New Zealand. N.Z. J. Mar. Freshwater Res. 4: 217-222.

FOOTE, C. J. 1987. An experimental examination of behavioural isola- tion between sockeye salmon and kokanee, the anadromous and nonanadromous forms of Oncorhynchus nerka. Ph.D. thesis, University of British Columbia, Vancouver.

FRASER, E. J., STARR, P. J., and FEDORENKO, A. Y. 1982. A review of the chinook and coho salmon of the Fraser River. Can. Tech. Rep. Fish. Aquat. Sci. No. 1126.

GEBHARDS, S. V. 1960. Biological notes on precocious male chinook salmon parr in the Salmon River drainage, Idaho. Prog. Fish-Cult. 22: 121 -123.

GROSS, M. R. 1982. Sneakers, satellites and parentals: polymorphic mating strategies in North American sunfishes. Z. Tierpsychol. 60: 1-26.

1985. Disruptive selection for alternative life histories in salmon. Nature (London), 313: 47 -48.

HANSON, A. J., and SMITH, A. D. 1967. Mate selection in a popula- tion of Sockeye salmon (Oncorhynchus nerka) of mixed age groups. J. Fish. Res. Board Can. 24: 1955 - 1977.

HOAR, W. S. 1988. The physiology of smolting salmonids. Fish Physiol. 1969- 1988, 11: 275-234.

HUBBS, C. L., and LAGLER, K. F. 1967. Fishes of the Great Lakes Region. Cranbrook Inst. Sci. Bull. No. 26.

KODRICK-BROWN, A. 1977. Reproductive success and the evolution of breeding territories in pupfish (Cyprinodon). Evolution, 31: 750- 766.

MCCORMICK, S. D., and NAIMAN, R. J. 1984. Some determinants of maturation in brook trout, Salvelinus fontinalis. Aquaculture, 43: 269 - 278.

MEERBURG, D. J. (Editor.) 1986. Salmonid age at maturity. Can. Spec. Publ. Fish. Aquat. Sci. No. 89.

MURRAY, C. B., and MCPHAIL, J. D. 1988. Effect of incubation tem- perature on the development of five species of Pacific salmon (Oncorhynchus) embryos and alevins. Can. J. Zool. 66: 266-273.

MYERS, R. A., and HUTCHINGS, J. A. 1987. Mating of anadromous Atlantic salmon, Salmo salar L., with mature male parr. J. Fish Biol. 31: 143 - 146.

MYERS, R. A., HUTCHINGS, J. A., and GIBSON, R. J. 1986. Variation in male parr maturation within and among populations of Atlantic salmon, Salmo salar. Can. J. Fish. Aquat. Sci. 43: 1242-1248.

RICH, W. H. 1920. Early history and seaward migration of chinook salmon in the Columbia and Sacramento Rivers. Bull. U.S. Bur. Fish. 37: 1-73.

RICKER, W. E. 1938. "Residual" and kokanee salmon in Cultus Lake. J. Fish. Res. Board Can. 4: 192-218.

1972. Hereditary and environmental factors affecting certain salmonid populations. In The stock concept in Pacific salmon. H. R. MacMillan Lectures in Fisheries, 1970. Edited by R. C. Simon and P. A. Larkin. University of British Columbia, Vancou- ver. pp. 19-160.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

McM

aste

r U

nive

rsity

on

11/1

2/14

For

pers

onal

use

onl

y.

TAYLOR

RIDDELL, B. E., and LEGGETT, W. C. 198 1 . Evidence of an adaptive basis for geographic variation in body morphology and time of downstream migration of juvenile Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 38: 308-320.

ROBERTSON, 0. H. 1957. Survival of precociously mature king salmon male parr (Oncorhynchus tshawytscha (Juv.)) after spawn- ing. Calif. Fish Game, 43: 119 - 130.

RUTTER, C. 1904. Natural history of the quinnat salmon. Bull. U.S. Fish. Cornm. 22: 65-141.

RYAN, M. J. 1988. Phenotype, genotype, swimming endurance and sexual selection in a swordtail (Xiphophorus nigrensis). Copeia, 1988: 484 -487.

SCHAFFER, W. M., and ELSON, P. F. 1975. The adaptive significance of variation in life-history among local populations of Atlantic salmon in North America. Ecology, 56: 577 -590.

SCHRODER, S. L. 1982. The influence of intrasexual competition on the distribution of chum salmon in an experimental stream. In Salmon and trout migratory behavior symposium, University of Washington, Seattle, WA, June 3 -5, 1981. Edited by E. L. Brannon and E. 0. Salo. University of Washington Press, Seattle, WA. pp. 275 - 285.

SHEPHERD, B. G., HILLABY, J. E., and HUTTON, R. J. 1986. Studies on Pacific salmon (Oncorhynchus spp.) in phase 1 of the salmonid enhancement program. Vol. 1. Summary. Can. Tech. Rep. Fish. Aquat. Sci. No. 1482.

SHIRATA, S. 1985. Present status of salmonid smolt production in Japan. In Preliminary report of the salmonid workshop on biologi-

cal and economic optimization of smolt production. Ministry of Agriculture, Forestry, and Fisheries, Tokyo, Japan.

SYNDER, J. 0. 1931. Salmon of the Klamath River. Calif. Dep. Fish Game Fish Bull. 34: 1 - 130.

TAYLOR, E. B. 1988. Adaptive variation in rheotactic and agonistic behaviour in newly emerged fry of chinook salmon, Oncorhynchus tshawytscha, from ocean- and stream-type populations. Can. J. Fish. Aquat. Sci. 44: 237-243.

THORPE, J. E. 1986. Age at first maturity in Atlantic salmon, Salmo salar: freshwater influences and conflicts with smolting. In Salmonid age at maturity. Edited by D. J. Meerburg. Can. Spec. Publ. Fish. Aquat. Sci. No. 89. pp. 7- 14.

1987. Smolting vs residency: developmental conflicts in salmonids. Am. Fish. Soc. Symp. 1: 244-252.

THORPE, J. E., and MITCHELL, K. A. 198 1 . Stocks of Atlantic salmon (Salmo salar) in Britain and Ireland: discreetness, and current management. Can. J. Fish. Aquat. Sci. 38: 1576- 1590.

UTOH, H. 1977. Study of the mechanism of differentiation between the stream resident form and the seaward migratory form in masu salmon, Oncorhynchus masou Brevoort. 11. Growth and sexual maturity of precocious salmon parr. 2. Bull. Fac. Fish. Hokkaido Univ. 28: 66-73.

WARNER, R. R., and HOFFMAN, S. G. 1980. Local population size as a determinant of mating system and sexual composition in two trop- ical marine fishes (Thalassoma spp.) . Evolution, 34: 508 - 5 18.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

McM

aste

r U

nive

rsity

on

11/1

2/14

For

pers

onal

use

onl

y.