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Factors affecting marine growth of Bristol Bay sockeye salmon
Fisheries Research, 18 ( 1993 ) 8 9 - 1 0 3
89
0 1 6 5 - 7 8 3 6 / 9 3 / $ 0 6 . 0 0 © 1993 - Elsevier Science Publishers B.V. All rights reserved
Factors affecting marine growth of Bristol Bay sockeye salmon Donald E. Rogers*, Gregory T. Ruggerone Fisheries Research Institute, WH-IO, University of Washington, Seattle, WA 98195, USA
Abstract
The growth of Bristol Bay sockeye salmon in freshwater and in the last few months at sea is dependent on their abundance (a negative correlate) and the prevailing water temperature (a positive correlate). In 1990 and 1991, the returning sockeye salmon to Bristol Bay were unusually small relative to their abundances and temperatures and this raised a concern for limited ocean carrying capacity because other stocks of salmon were also very numerous in those years. However, the inclusion of other stocks of sockeye salmon and the abundant runs of Asian chum salmon in a multiple regression analysis did not provide a better predictor of the body size of Bristol Bay sockeye salmon. Growth increments of Nushagak Bay sockeye salmon in their first and second years at sea (from scale measurements) were correlated with temperatures but not with the abundances since 1975. The growth increment in the third year of sea life was uncorrelated with temperature and abundance but was correlated with final adult length. This suggests that concern for carrying capacity limitations should be placed on the migratory routes of returning adults when the fish are probably most concentrated and their growth most limited by their food supply.
Introduction d
Annual runs of sockeye salmon (Oncorhynchus nerka) to Bristol Bay in southwestern Alaska constitute the largest concentration of this species in the North Pacific. Over the past two decades annual runs have averaged 27 million fish, but have varied from 2 million to 62 million fish (Rogers, 1987a). In an average year, Bristol Bay contributed 40% to the North Pacific catch of sockeye. Their abundance was especially high during the 1980s, a period when significant increases were also observed in the runs of sockeye to other areas of North America, record runs of pink salmon ( O. gorbuscha ) to Prince William Sound and Southeast Alaska, and remarkable numbers of chum salmon (0. keta) to Japanese hatcheries. The recent large runs of salmon have raised questions about the rearing capacity of the North Pacific estuaries and high seas. One method to determine whether there is a limitation to the salmon-food*Corresponding author.
90
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
producing capacity of the sea is to test for an inverse relationship between abundance and growth of salmon (or body size at a specific age). Davidson and Vaughan ( 1941 ) showed such an inverse relationship for Southeast Alaska pink salmon by relating fish-per-case estimates from processors to the annual commercial catches during the 1920s and 1930s; however, Marshall and Quinn (1988) reported difficulties in obtaining accurate average weights for pink salmon from processors, even though pinks all mature at a single age. Ricker ( 1989 ) also noted an inverse relationship for Fraser River pink salmon, particularly during their increasing abundance in recent years. However, the recent smaller sizes of pink salmon may have been caused by long-term effects of net selectivity rather than increasing abundance. Bristol Bay sockeye salmon usually spend 1-2 years in freshwater, then 23 years at sea. Average body size of adult sockeye salmon in gill-net catches is mostly affected by ocean age and sex. Sockeye remaining 3 years at sea are 34% heavier, on average, than those spending 2 years, and male sockeye are 14% heavier than females at age .2 and 19% heavier at age. 3 (Rogers, 1980; age x.3 refers to salmon that spent x years in freshwater and 3 years at sea). The ocean ages in the return from a brood year are partly controlled by the ocean ages of the parents (older fish tend to produce older fish) and by the freshwater ages because fish that spend 1 year in freshwater (age 1.x, the fastergrowing juveniles) tend to mature later, and thus at a larger size, than those that spend 2 years in freshwater (Rogers, 1987b ). In addition, growth of Bristol Bay sockeye, in freshwater and in the last few months at sea, is dependent on fish density (higher density is related to poorer growth) and temperature (lower temperature is related to poorer growth); however, there was no evidence that growth during the first or second year at sea was density dependent (Rogers, 1984). During 1958-1973, mean weights of sockeye by age and sex in Bristol Bay runs were inversely correlated with fish abundance and the deviations were directly correlated with April-May air temperature, except for age 1.2 (Rogers, 1980). The statistics were analyzed again after the 1983 run and it was evident that, with the increase in ocean temperatures beginning with the winter of 1976-1977, fish size was greater at a given abundance. Mean lengths by age and sex were now related to April-May sea surface temperatures at Kodiak and the n u m b e r of sockeye in the run (Rogers, 1984, 1987a). In 1990 and 199 l, the sockeye returning to Bristol Bay were exceptionally small, i.e. smaller than predicted from numbers in the run and ocean temperatures, and there were reports that pink salmon were unusually small in those years. Also, in 199 l, we completed scale radii measurements of Nushagak District sockeye that would allow an examination of ocean growth (first and second year) and run size. The purpose of this investigation is to re-examine the question of densitydependent growth of Bristol Bay sockeye by comparing sockeye growth with
D.E. Rogers, G. T. Ruggerone / Fisheries Research 18 (1993) 89-103
91
abundance of sockeye and chum salmon stocks that overlap Bristol Bay sockeye at sea and by including potential sea surface temperature effects in the analysis. Methods
Bristol Bay sockeye salmon, during their ocean residence, are most likely to be associated with chum salmon stocks from Bristol Bay, other Bering Sea (Western Alaska) locations and Asia, and secondarily with sockeye and chum salmon from the upper Gulf of Alaska (French et al., 1976; Neave et al., 1976 ). Overlap of these stocks is especially great during spring and summer months when most growth occurs; however, the distribution of Bristol Bay sockeye probably overlaps that of abundant pink salmon stocks during winter when growth is less (Takagi et al., 1981 ). We updated (1985-1991) the estimates of annual Alaskan sockeye and chum salmon runs presented by Rogers (1987a), which utilized catch and escapement statistics from the Alaska Department of Fish and Game. Asian chum salmon runs were estimated from catch statistics by the International North Pacific Fisheries Commission (e.g. 1990), Japan Fisheries Agency, and Pacific Research Institute of Fisheries and Oceanography (TINRO, Russia). Asian escapements were based on assumed exploitation rates of 0.6 for Russian runs and 1.0 for Japanese hatchery runs. Temperature effects on growth of Bristol Bay sockeye were examined by utilizing air temperatures in Bristol Bay during April-June (averages of monthly means for Dillingham and King Salmon weather stations) and inshore sea surface temperatures during January-June (monthly means for Kodiak in the Gulf of Alaska and Adak in the Aleutian Islands). Most Bristol Bay sockeye migrate to sea during May-July (Rogers, 1988) and the adults return from late June to mid-July; however, adults begin their homeward migrations in May. Surface water temperatures in outer Bristol Bay (offshore from Port Moller) during June were also available, but only since 1967, and temperatures were missing in 2 years (Helton, 1991 ). Mean lengths and weights of sockeye salmon in Bristol Bay runs during 1958-1977 were calculated from measurements of individual fish as described by Rogers (1980). For years 1978-1990, mean lengths and weights (catch only) were obtained from annual reports by Alaska Department of Fish and Game (e.g. Stratton, 1991 ). These reports present mean length and weight by age and sex for commercial catch samples and escapement samples (length only). Weight of sockeye in the escapement was estimated from previously described length-weight relationships (Rogers, 1980). Mean catch values of sockeye salmon were adjusted to live measurements by subtracting 2 m m from lengths and adding 11 g to weights. Catch and escapement means were then weighted by number of fish to obtain the means in the run to each
92
D,E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
of the five fishing districts, and means for the districts were weighted by numbers of fish to obtain means for the total Bristol Bay run. Examination of the relationship between adult sockeye salmon size, abundance, and environmental conditions was simplified by first selecting dominant age groups of the Bristol Bay run and determining which of eight measures of salmon abundance was best correlated with all dominant age groups. Mean lengths of male and female fish, which were more accurate than weights, were averaged (unweighted) to obtain four means for each year: ages 1.2 and 1.3 from the Nushagak District and ages 2.2 and 2.3 from the total Bristol Bay run. The Nushagak runs consistently contained large sample sizes of ages 1.2 and 1.3, whereas sample sizes were sometimes small for these ages in the Naknek-Kvichak, Egegik and Ugashik Districts. Adult length of each of the four age groups was regressed against eight salmon abundance estimates, i.e. runs of Bristol Bay sockeye, Western Alaska sockeye (including the South U n i m a k - S h u m a g i n Islands fishery in June), Western and Central Alaska sockeye, North Pacific sockeye (including Asian runs and catches on the high seas but excluding stocks south of Central Alaska), and sockeye plus chum salmon runs for each of these areas. Correlations were calculated for all years ( 1959-1991 ), and the recent warm period ( 1977-1991 ). All correlations were graphed and examined for non-linearity. The four correlation coefficients associated with each measure of abundance during 1959-1991 were averaged and the measure of abundance having the highest average correlation with mean length of the four age groups was then selected for further stepwise multiple regression with the measures of late-winter and spring temperatures (e.g. Port Moiler, Bristol Bay, air temperatures, and Kodiak and Adak water temperatures). Mean weights of each sockeye age group were also compared with the previously identified measures of abundance and temperature. Sockeye scales collected from commercial harvests in the Nushagak District during 1959-1988 were measured to provide an index of growth during each year at sea. The scales were measured by the Optical Pattern Recognition System (OPRS) at a magnification of 84X, following procedures described by Davis et al. (1990) and Z i m m e r m a n n ( 1991 ). Approximately 95 scales from each age group (ages 1.2 and 1.3) were measured and the unweighted mean of male and female measurements was used as the index of growth. Scale growth during the spring of capture was frequently resorbed and was therefore excluded from analysis. Correlation analysis followed the same procedures as that for adult length and weights. Results
The major Alaskan stocks of sockeye, chum and pink salmon have been under intense exploitation from commercial fisheries since the early 1900s. The exceptions are the c h u m salmon runs to the Yukon and Kuskokwim Riv-
93
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
ers in Western Alaska, which were not fished extensively until the 1970s. Trends in the historical catches of the three species are similar, but are especially close for sockeye and pink salmon (Fig. 1 ). Catches were very low in the early 1970s, then increased in the late 1970s to historical record levels for sockeye in 1990 and pinks in 1991. The low points in catches corresponded to low temperatures in the G u l f o f Alaska and cold winters in Bristol Bay, whereas the increase in catches coincided with mild winters in Bristol Bay and high temperatures at K o d i a k (Figs. 2 and 3). However, for the large catches in 1990 and 1991, winter temperatures in the G u l f o f Alaska were lower, whereas s u m m e r temperatures remained above average, and winter temperatures in the Aleutians ( A d a k ) were well above average (Table 1 ). Annual runs o f salmon (catch plus e s c a p e m e n t ) are better measures of the a b u n d a n c e o f salmon at sea than just the catches; however, we only have estimates of the runs since 1952 (Fig. 4). Most o f the recent increase in North Pacific chum salmon a b u n d a n c e were contributed by Japanese hatcheries (72% in 1989-1991 ), and Bristol Bay contributed most to the North Pacific sockeye runs (60% in 1989-1991 ). The annual runs of Bristol Bay sockeye have largely determined the year-to-year variation in the abundance of sockeye salmon in the North Pacific ( 1952-1991, r = 0 . 9 7 ) . []
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Year Fig. I. A n n u a l c o m m e r c i a l s a l m o n catches in Alaska, ] 9 1 0 - 1 9 9 ].
94
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103 11
=
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Year Fig. 2. Annual summer (Apr.-Oct.) air temperatures in Bristol Bay (Dillingham and King Salmon ), 1921-1991, and sea surface temperatures at Kodiak ( G u l f of Alaska ), 1950-1991.
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beginning
Fig. 3. Annual winter ( N o v . - M a r . ) air temperatures in Bristol Bay, 1919-1920 to 1991-1992, and sea surface temperatures at Kodiak, 1950-1951 to 1991-1992.
The average lengths o f Bristol Bay sockeye did not change much between the colder-low-abundance years, 1 9 5 9 - 1 9 7 6 , and the warmer-high-abundance years of 1 9 7 7 - 1 9 9 1 (Table 2 ). Within Bristol Bay, lengths o f sockeye were similar a m o n g systems, and males were longer than females with the
95
D.E. Rogers, G.T Ruggerone / Fisheries Research I8 (1993) 89-103
Table 1 W i n t e r - s p r i n g temperatures ( ° C) in Southwest Alaska, 1952-1991; mean m o n t h l y temperatures for N o v e m b e r (Year - 1 ) to March (year), with regression estimates of missing data in parentheses Year
1952 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
Bristol Bay air temperature
Nov.Mar.
Apr.May
-8.2 -8.9 -10.8 -7.9 -12.5 -9.3 -6.8 -8.6 -7.5 -7.9 -9.0 -5.8 -9.4 -9.4 -9.5 -8.2 -7.0 -9.2 -7.0 -12.1 - 11.6 -9.1 -9.3 -11.6 -11.2 -3.4 -6.8 -4.3 -7.6 -4.8 -7.8 -5.2 -6.0 -5.4 -4.6 -3.6 -7.2 -9.1 -9.1 -7.7
-0.1 4.2 2.6 0.8 1.0 5.0 4.0 2.9 1.3 3.2 2.8 1.8 0.3 1.0 1.1 4.2 2.8 3.8 2.8 -0.5 -0.6 3.2 4.4 0.1 1.2 0.5 4.6 5.4 3.9 5.4 0.0 4.6 1.8 - 1.7 1.6 2.5 2.4 3.6 5.0 4.1
Port Moiler sea surface temperature, 11-30 June
8.6 6.6 6.8 5.8 2.8 3.3 5.1 (7.8) 5.1 4.4 7.2 7.0 8.8 5.9 10.2 6.1 9.2 9.0 5.6 (5.9) 5.5 7.2 6.1 6.9 5.2
Kodiak sea surface temperature
Adak sea surface temperature
Nov.Mar.
Apr.May
Nov.Mar.
Apr.May
1.6 2.0 1.5 1.6 0.2 0.2 2.2 1.0 2.0 2.1 0.5 2.6 2.1 (0.7) (2.0) 1.7 2.4 2.3 3.8 1.7 1.3 (2.7) 2.4 2.7 3.1 5.8 4.4 4.9 4.8 5.5 2.9 3.5 4.1 3.2 2.8 3.6 3.6 2.3 2.2 2.4
4.4 5.2 5.4 5.3 3.8 5.1 6.2 5.3 4.9 5.6 5.1 5.6 4.6 (5.1) (3.9) 5.7 5.4 5.5 6.1 3.3 3.3 (4.5) 5.0 4.2 5.0 7.7 6.6 7.9 7.4 7.8 4.5 6.5 6.0 5.0 5.1 6.6 7.3 6.4 6.7 6.4
3.6 3.0 2.9 3.4 3.4 3.0 3.2 3.6 3.7 3.2
4.7 4.7 4.2 4.1 4.0 4.5 4.4 4.8 4.1 4.3 4.2 4.7 3.1 3.1 3.2 4.3 3.9 3.8 3.8 3.3 3.6 3.4 3.8 4.0 3.8 4.0 4.6 4.1 3.5 4.1 4.1 3.9 4.2 4.6 (4.4) 5.8 4.5 4.8 5.0 4.7
3.1
3.3 3.5 3.4 3.5 3.4 3.7 3.3 3.1 3.7 3.5 3.4 3.5 3.9 3.6 3.4 3.2 3.9 3.2 3.5 4.5 (3.8) (4.5) 4.3 4.1 4.3 4.6
96
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
Western Alaska ~
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Fig. 4. Annual runs (catch plus escapement) of sockeye and chum salmon to Western Alaska and the North Pacific (Western-Central Alaska plus Asia), 1952-1991. exception of the Naknek stocks. The N a k n e k 2-ocean males were exceptionally small and usually shorter than the females. The annual m e a n lengths o f Nushagak and Bristol Bay sockeye for the runs during 1959-1991 were m o r e closely correlated with the n u m b e r o f sockeye in the Bristol Bay run than with any o f the other seven measures of abundance (Figs. 5 and 6). However, when correlations were calculated separately for the two periods ( 1959-1976 and 1977-1991 ), the North Pacific run o f sockeye plus c h u m salmon provided somewhat higher correlations than the Bristol Bay sockeye runs alone. Therefore, in further stepwise multiple regression analyses, we included the annual n u m b e r o f North Pacific c h u m salmon (essentially Japanese hatchery c h u m s ) as a variable together with abundance of Bristol Bay sockeye and several measures of temperature. In contrast to the significant relationships between m e a n length o f Nushagak and Bristol Bay sockeye and abundance of Bristol Bay sockeye salmon, the unweighted m e a n lengths in the returns from a brood year were not significantly correlated ( P > 0.05 ) with the n u m b e r o f sockeye in the return (i.e.
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
97
Table 2 Mean lengths ( mid-eye to tail fork; mm) of sockeye salmon in Bristol Bay runs and escapements (numbers of fish in millions) District runs Years
Naknek
Kvichak Egegik Ugashik Nushagak
Age 1.2
Age 2.2
Age 1.3
Age 2.3
Run Male Female Run
Male Female Run Male Female Run
Male Female
1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991
2.6 4.8 0.2 0.7 0.3 0.9 1.0 1.7
509 511 521 522 523 527 517 512
497 502 508 508 509 508 496 493
7.0 8.1 1.0 3.0 0.3 1.3 0.3 0.3
521 525 532 535 535 537 527 529
510 514 515 518 514 517 505 507
1.1 3.3 0.3 1.2 0.2 0.9 1.0 3.6
580 579 587 587 591 591 585 584
561 562 568 569 572 569 556 554
1.1 1.7 0.6 1.4 0.1 0.4 0.1 0.2
584 583 591 593 596 595 586 585
567 567 573 575 573 572 558 559
1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991
1.4 1.8 0.2 0.3 0.1 0.2 0.2 0.4 0.5 0.6 0.1 0.1
510 516 487 471 520 517 523 527 512 509 522 537
499 500 485 479 504 501 508 505 491 486 498 509
3.8 3.7 0.4 0.4 0.5 0.6 0.2 0.4 0.1 0.1 <0.1 <0.1
522 529 498 492 531 532 534 536 517 520
507 512 501 498 511 512 511 512 498 498
0.2 0.4 0.2 0.6 0.1 0.2 0.1 0.4 0.3 0.5 0.1 0.3
580 581 576 578 589 592 593 601 577 577 589 598
560 561 556 559 563 569 572 572 550 549 554 561
0.3 0.3 0.2 0.3 0.3 0.3 <0.1 0.1 <0.1 <0.1 <0.1 <0.1
587 587 580 585 591 599 599 605 -
564 567 564 566 570 575 571 574 -
Escapements
Kvichak Naknek
Egegik Ugashik Wood lgushik
age 1.2 in year+ 4, ages 2.2 and 1.3 in year+ 5, and age 2.3 in year+ 6 ). Thus, there was no indication of a brood year effect on adult size. During stepwise multiple regression analyses of length and weight measurements for the four age groups during two sets of years ( 1959-1991 and 19771991 ), different temperature measurements entered the regressions that included Bristol Bay run size. The mean sea surface temperature at Kodiak during January-May (Fig. 5 ) showed the highest average partial correlation and occurred most frequently in the eight regressions; therefore, mean sea surface temperature at Kodiak during January-May was used in all models where temperature was significantly correlated. For age 1.2 sockeye, temperature was more highly correlated with mean lengths and weights than number of sockeye in the run; however, for age 2.3 sockeye during 1977-1991, temperature was not significantly correlated with the deviations from the regressions of length or weight on Bristol Bay run (Table 3). Thus, size of adult sockeye salmon in Bristol Bay was inversely related to Bristol Bay run size and positively related to Kodiak water temperature during winter and spring. In no
98
D.E. Rogers, G. T, Ruggerone / Fisheries Research 18 (1993) 89-103 ....
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Year
Fig. 5. Annual Bristol Bay sockeye runs, mean lengths in the runs and Kodiak sea surface temperatures for winter-spring months. instances were there significant partial correlations with numbers o f chum salmon. Scale radii measurements o f Nushagak District sockeye for each year at sea ( 1 9 5 6 - 1 9 8 8 ) indicated that growth was positively related to temperature during the first (ages 1.2 and 1.3 ) and second (age 1.3 only) years at sea (Fig. 7, Table 4 ) . Growth during the last full year at sea was not correlated with temperature. Since 1974, only growth during the first year at sea of age 1.2 sockeye was correlated with temperature. Salmon run size during the year o f return was not correlated with scale growth during each year at sea. However, adult returns from annual smolt migrations (e.g. ages 1.2 and 2.2 in y e a r + 2 and ages 1.3 and 2.3 in y e a r + 3 ) were positively correlated with growth of age 1.2 sockeye, but not age 1.3 sockeye, during the first year at sea. Scale growth during the first and second years at sea and total scale length at each age were not correlated with adult length. However, growth during the third year (age 1.3 ) was positively correlated with adult length ( r = 0.50 ).
99
D.E. Rogers, G. 72 Ruggerone / Fisheries Research 18 (1993) 89-103 y
E E
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.... I !a . . . . 2030 4050 6070 Bristol Bay run (millions) 10
Fig. 6. Linear regressions o f m e a n length o n Bristol Bay r u n for the 1959-1991 runs (solid points for the 1977-1991 r u n s ) . Table 3 Linear regressions of length and weight on water temperature and abundance of Bristol Bay sockeye salmon Age group
Years
Regression
R2
Nushagak 1.2
1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991
L = 5 0 3 +2.46 (SST) - 0 . 2 9 2 ( R U N ) L = 4 8 1 +5.75 (SST) - 0 . 1 4 4 ( R U N ) W=2.12 +0.037 (SST) - 0 . 0 0 4 4 ( R U N ) W = 1.81 +0.082 (SST) - 0 . 0 0 2 1 ( R U N ) L = 5 6 7 +3.14 (SST) - 0 . 3 5 7 ( R U N ) L = 5 6 2 +3.80 (SST) - 0 . 3 1 2 ( R U N ) W=3.12 +0.072 (SST) -0.0071 ( R U N ) W=3.08 +0.073 (SST) - 0 . 0 0 6 1 ( R U N ) L = 5 1 5 +4.46 (SST) - 0 . 4 1 5 ( R U N ) L = 5 2 4 +2.80 (SST) - 0 . 3 9 1 ( R U N ) W=2.21 +0.065 (SST) - 0 . 0 0 5 7 ( R U N ) W=2.35 +0.038 (SST) - 0 . 0 0 5 2 ( R U N ) L = 5 7 9 +2.04 (SST) - 0 . 2 9 8 ( R U N ) L=591 -0.346 (RUN) W=3.15 +0.056 (SST) - 0 . 0 0 6 5 ( R U N ) W=3.47 - 0 . 0 0 7 7 ( R U N )
0.25 0.52 0.25 0.56 0.49 0.57 0.46 0.52 0.49 0.42 0.53 0.46 0.43 0.51 0.57 0.73
Nushagak 1.3
Bristol Bay 2.2
Bristol Bay 2.3
L, Mean length of males and females, mean of means (mid-eye to tail fork; mm ). W, Mean weight of males and females, mean of means (kg). SST, Mean monthly sea surface temperature ( ° C ) at Kodiak for January-May in the year of the run. RUN, Bristol Bay sockeye run, in millions offish.
100
D.E. Rogers, G. 72 Ruggerone / Fisheries Research 18 (1993) 89-103 11oo
g
lOOO
c
.... I
.
An
900 h5
8(n
800
I
2nd year
g
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.~
55
1100
60
65
I I =
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~ 1000"1styeir~000 ~/~ ~ _o
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75
80
85
90
" ~¢:~p
~ i~
~
o0o ~;
i ar 500 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 55 60 65 70 Year
of
75
80
85
90
growth
Fig. 7. A n n u a l m e a n s o f scale m e a s u r e m e n t s (H) during each year at sea for N u s h a g a k sockeye salmon, ages 1.2 a n d 1.3. C o m m e r c i a l catch samples, 1959-1988.
Table 4 Linear regressions o f scale radii m e a s u r e m e n t s (H) f r o m N u s h a g a k District sockeye d u r i n g each year o f ocean growth on t e m p e r a t u r e a n d a b u n d a n c e o f s a l m o n Age g r o u p
O c e a n year
Years
Regression
1.2 1.2 1.2 1.2 1.3 1.3 1.3 1.3 1.3 "~.3
1 1 2 2 1 1 2 2 3 3
1957-1986 1975-1986 1958-1987 1976-1987 1956-1986 1974-1986 1957-1987 1975-1987 1958-1988 1976-1988
S=864.4+15.59 S=871.6+24.41 S = 8 1 7 . 4 + 19.98 S = 7 6 5 . 2 + 17.01 -
R2 (AIR) +l.01 (RETURN (AIR)
(AIR) (SST)
0.36 0.56 NS NS 0.35 NS 0.22 NS NS NS
S, U n w e i g h t e d m e a n length o f male a n d female scale radii m e a s u r e m e n t s for given t i m e period at sea. AIR, A p r i l - J u n e air t e m p e r a t u r e m e a s u r e d at K i n g S a l m o n a n d Dillingham. R E T U R N , Adults r e t u r n i n g to Bristol Bay ( m i l l i o n s ) f r o m a n n u a l smolt migrations. SST, M e a n m o n t h l y sea surface t e m p e r a t u r e ( ° C ) at K o d i a k d u r i n g N o v e m b e r - M a r c h before the fish's second growing period at sea. NS, N o t significant at ce=0.05.
D.E. Rogers, G.T. Ruggerone /Fisheries Research 18 (1993) 89-103
10 1
Discussion Major changes in salmon runs have generally followed changes in winter temperatures over southwestern Alaska (Rogers, 1980, 1984). Low runs in the early 1970s corresponded to low temperatures in the Gulf of Alaska and cold winters in Bristol Bay, whereas the greater runs beginning in the late 1970s coincided with mild winters in Bristol Bay and high temperatures at Kodiak. However, for the large runs in 1990 and 1991, winter temperatures in the Gulf of Alaska had decreased, whereas s u m m e r temperatures remained above average and winter temperatures in the Aleutians (Adak) were well above average. Mean size of Bristol Bay sockeye was inversely related to Bristol Bay run size and positively related to mean monthly sea surface temperature at Kodiak during January-May. However, sockeye in 1991 were 10-15 m m shorter ( 126-177 g lighter) than predicted and the 2-ocean sockeye in 1990 were 10 m m shorter than predicted. Preliminary data from the large 1992 Bristol Bay run (about 45 million sockeye salmon) indicate that sockeye returning in 1992 were also exceptionally small. The explanation for this unusually small size is unknown, although the exceptionally large consecutive runs of sockeye, chum, and pink salmon since 1990 were probably influential. Nevertheless, the small size of sockeye salmon returning to Bristol Bay in 1992 was a useful factor in developing an in-season forecast of run strength. Year-to-year variation in the maturation rate of sockeye at sea probably affects the mean lengths of fish returning from a given brood year. The 2ocean sockeye that return to Bristol Bay are about 82% heavier than immature 2-ocean sockeye still at sea in July and that will mature as 3-ocean sockeye the following year (Harris and Rogers, 1979). There was usually very little overlap in the length frequencies of mature and immature sockeye in June. Jacks or l-ocean sockeye were not abundant in the Bristol Bay runs, therefore sample sizes were usually small; however, over all years, the age 1.1 males averaged 35 cm and age 2.1 males averaged 37 cm. The age 1.1 immature salmon at sea averaged 30.5 cm and age 2.1 averaged 33 cm; thus jacks were about 4 cm longer than the 1-ocean male and female sockeye at sea. In 1991 and 1992, the small age-specific size of Bristol Bay sockeye salmon was coincident with additional years at sea, i.e. slower maturation rate. In 1992, an unusually large percentage of age .4 sockeye returned, indicating the effect of reduced growth on maturation rate. Density effects on growth probably occur during the homeward migration because Bristol Bay salmon are more concentrated at that time and are actively feeding (Nishiyama, 1984; Helton, 1991). This hypothesis is supported by the little or no correlation between scale growth and adult size, the lack of density-dependent growth during earlier years at sea, and the lack of density-dependent growth associated with brood year returns. Year-to-year variation in spring temperatures affects not only the growth of Bristol Bay
102
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
sockeye, but also their migratory timing and routes of migration (Fujii, 1975 ), which could also indirectly affect their growth. For Bristol Bay sockeye, slower growth early in life leads to larger size at maturity (i.e. older age at maturation), whereas slower growth during the final few months at sea results in smaller than average size. Acknowledgments Funding for this investigation was provided by the Pacific Seafood Processors Association and Washington Sea Grant. M. Zimmermann carefully measured the sockeye scales from the Nushagak District. We are grateful to D. Beauchamp and A. Tyler for their constructive comments.
References Davidson, F.A. and Vaughan, E., 1941. Relation of population size to marine growth and time of spawning migration in the pink salmon (Onchorhynchus gorbuscha) of Southeastern Alaska. J. Mar. Res., 4." 231-246. Davis, N.D., Myers, K.W., Walker, R.V. and Harris, C.K., 1990. The Fisheries Research Institute's high seas salmonid tagging program and methodology for scale pattern analysis. Am. Fish. Soc. Symp., 7: 863-879. French, R., Bilton, H., Osaka, M. and Hartt, A., 1976. Distribution and origin of sockeye salmon (Onchorynchus nerka) in offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull., 34, 113 pp. Fujii, T , 1975. On the relation between homing migration of the western Alaska sockeye salmon Onchorynchus nerka (Walbaum) and oceanic conditions in the eastern Bering Sea. Mere. Fac. Fish. Hokkaido Univ., 22(2): 99-191. Harris, C.K. and Rogers, D.E., 1979. Forecast of the sockeye salmon run to Bristol Bay in 1979. Univ. Wash. Fish. Res. Inst. Circ., 79-2, 50 pp. Helton, D.R., 1991. An analysis of the Port Moller offshore test fishing forecast of sockeye and chum salmon runs to Bristol Bay, Alaska. M.S. Thesis, University of Washington, Seattle, WA, 122 pp. International North Pacific Fisheries Commission, 1990. Statistical Yearbook 1990. INPFC, Vancouver, B.C., 133 pp. Marshall, R.P. and Quinn, II, T.J., 1988. Estimation of average weight and biomass of pink, chum, sockeye and coho salmon in Southeast Alaska commercial harvests. Alaska Dep. Fish Game Fish. Res. Bull., 88-07, 52 pp. Neave, F., Yonemori, T. and Bakkala, R.G., 1976. Distribution and origin of chum salmon in offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull., 35, 79 pp. Nishiyama, T., 1984. Two important factors in the oceanic stages of salmon: food and temperature, In: Proceedings of the Pacific Salmon Biology Conference (USSR, USA, Canada, Japan). Yuzhno-Sakhalinsk, USSR, 1978. TINRO, Vladivostok, pp. 227-258. Ricker, W.E., 1989. History and present state of the odd-year pink salmon runs of the Fraser River Region. Can. Tech. Rep. Fish. Aquat. Sci., 1702, 37 pp. Rogers, D.E., 1980. Density-dependent growth of Bristol Bay sockeye salmon, In: W.J. McNeil and D.C. Himsworth (Editors), Salmonid Ecosystems of the North Pacific. Oregon State University Press, Corvallis, OR, pp. 267-283.
D.E. Rogers, G. 72 Ruggerone / Fisheries Research 18 (1993) 89-103
103
Rogers, D.E., 1984. Trends in abundance of northeastern Pacific stocks of salmon, In: W.G. Pearcy (Editor), The Influence of Ocean Conditions on the Production of Salmonids in the North Pacific. Oregon State University Press, Corvallis, OR, pp. 100-127. Rogers, D.E., 1987a. Pacific salmon, In: D.W. Hood and S.T. Zimmerman (Editors), The Gulf of Alaska: Physical Environment and Biological Resources. US Government Printing Office, Washington, DC, pp. 461-476. Rogers, D.E., 1987b. The regulation of age at maturity in Wood River sockeye salmon (Oncho~ rynchus nerka). In: H.D. Smith, L. Margolis and C.C. Wood (Editors), Sockeye Salmon (Onchorynchus nerka) Population Biology and Future Management. Can. Spec. Publ. Fish. Aquat. Sci., 96: 78-89. Rogers, D.E., 1988. Bristol Bay smolt migrations, In: W.J. McNeil (Editor), Salmon Production, Management, and Allocation. Oregon State University Press, Corvallis, pp. 87-101. Stratton, B.L., 1991. Abundance, age, sex and size statistics for Pacific salmon in Bristol Bay, 1990. Alaska Dep. Fish Game Tech. Fish. Rep., 91-15, 153 pp. Takagi, K., Aro, K.V., Hartt, A.C. and Dell, M.B., 1981. Distribution and origin of pink salmon (Onchorynchus gorbuscha) in offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull., 40, 195 pp. Zimmermann, M., 1991. Trends in the freshwater growth of sockeye salmon (Onchorynchus nerka) from the Wood River Lakes and Nushagak Bay, Alaska. M.S. Thesis, University of Washington, Seattle, WA, 119 pp.
89
0 1 6 5 - 7 8 3 6 / 9 3 / $ 0 6 . 0 0 © 1993 - Elsevier Science Publishers B.V. All rights reserved
Factors affecting marine growth of Bristol Bay sockeye salmon Donald E. Rogers*, Gregory T. Ruggerone Fisheries Research Institute, WH-IO, University of Washington, Seattle, WA 98195, USA
Abstract
The growth of Bristol Bay sockeye salmon in freshwater and in the last few months at sea is dependent on their abundance (a negative correlate) and the prevailing water temperature (a positive correlate). In 1990 and 1991, the returning sockeye salmon to Bristol Bay were unusually small relative to their abundances and temperatures and this raised a concern for limited ocean carrying capacity because other stocks of salmon were also very numerous in those years. However, the inclusion of other stocks of sockeye salmon and the abundant runs of Asian chum salmon in a multiple regression analysis did not provide a better predictor of the body size of Bristol Bay sockeye salmon. Growth increments of Nushagak Bay sockeye salmon in their first and second years at sea (from scale measurements) were correlated with temperatures but not with the abundances since 1975. The growth increment in the third year of sea life was uncorrelated with temperature and abundance but was correlated with final adult length. This suggests that concern for carrying capacity limitations should be placed on the migratory routes of returning adults when the fish are probably most concentrated and their growth most limited by their food supply.
Introduction d
Annual runs of sockeye salmon (Oncorhynchus nerka) to Bristol Bay in southwestern Alaska constitute the largest concentration of this species in the North Pacific. Over the past two decades annual runs have averaged 27 million fish, but have varied from 2 million to 62 million fish (Rogers, 1987a). In an average year, Bristol Bay contributed 40% to the North Pacific catch of sockeye. Their abundance was especially high during the 1980s, a period when significant increases were also observed in the runs of sockeye to other areas of North America, record runs of pink salmon ( O. gorbuscha ) to Prince William Sound and Southeast Alaska, and remarkable numbers of chum salmon (0. keta) to Japanese hatcheries. The recent large runs of salmon have raised questions about the rearing capacity of the North Pacific estuaries and high seas. One method to determine whether there is a limitation to the salmon-food*Corresponding author.
90
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
producing capacity of the sea is to test for an inverse relationship between abundance and growth of salmon (or body size at a specific age). Davidson and Vaughan ( 1941 ) showed such an inverse relationship for Southeast Alaska pink salmon by relating fish-per-case estimates from processors to the annual commercial catches during the 1920s and 1930s; however, Marshall and Quinn (1988) reported difficulties in obtaining accurate average weights for pink salmon from processors, even though pinks all mature at a single age. Ricker ( 1989 ) also noted an inverse relationship for Fraser River pink salmon, particularly during their increasing abundance in recent years. However, the recent smaller sizes of pink salmon may have been caused by long-term effects of net selectivity rather than increasing abundance. Bristol Bay sockeye salmon usually spend 1-2 years in freshwater, then 23 years at sea. Average body size of adult sockeye salmon in gill-net catches is mostly affected by ocean age and sex. Sockeye remaining 3 years at sea are 34% heavier, on average, than those spending 2 years, and male sockeye are 14% heavier than females at age .2 and 19% heavier at age. 3 (Rogers, 1980; age x.3 refers to salmon that spent x years in freshwater and 3 years at sea). The ocean ages in the return from a brood year are partly controlled by the ocean ages of the parents (older fish tend to produce older fish) and by the freshwater ages because fish that spend 1 year in freshwater (age 1.x, the fastergrowing juveniles) tend to mature later, and thus at a larger size, than those that spend 2 years in freshwater (Rogers, 1987b ). In addition, growth of Bristol Bay sockeye, in freshwater and in the last few months at sea, is dependent on fish density (higher density is related to poorer growth) and temperature (lower temperature is related to poorer growth); however, there was no evidence that growth during the first or second year at sea was density dependent (Rogers, 1984). During 1958-1973, mean weights of sockeye by age and sex in Bristol Bay runs were inversely correlated with fish abundance and the deviations were directly correlated with April-May air temperature, except for age 1.2 (Rogers, 1980). The statistics were analyzed again after the 1983 run and it was evident that, with the increase in ocean temperatures beginning with the winter of 1976-1977, fish size was greater at a given abundance. Mean lengths by age and sex were now related to April-May sea surface temperatures at Kodiak and the n u m b e r of sockeye in the run (Rogers, 1984, 1987a). In 1990 and 199 l, the sockeye returning to Bristol Bay were exceptionally small, i.e. smaller than predicted from numbers in the run and ocean temperatures, and there were reports that pink salmon were unusually small in those years. Also, in 199 l, we completed scale radii measurements of Nushagak District sockeye that would allow an examination of ocean growth (first and second year) and run size. The purpose of this investigation is to re-examine the question of densitydependent growth of Bristol Bay sockeye by comparing sockeye growth with
D.E. Rogers, G. T. Ruggerone / Fisheries Research 18 (1993) 89-103
91
abundance of sockeye and chum salmon stocks that overlap Bristol Bay sockeye at sea and by including potential sea surface temperature effects in the analysis. Methods
Bristol Bay sockeye salmon, during their ocean residence, are most likely to be associated with chum salmon stocks from Bristol Bay, other Bering Sea (Western Alaska) locations and Asia, and secondarily with sockeye and chum salmon from the upper Gulf of Alaska (French et al., 1976; Neave et al., 1976 ). Overlap of these stocks is especially great during spring and summer months when most growth occurs; however, the distribution of Bristol Bay sockeye probably overlaps that of abundant pink salmon stocks during winter when growth is less (Takagi et al., 1981 ). We updated (1985-1991) the estimates of annual Alaskan sockeye and chum salmon runs presented by Rogers (1987a), which utilized catch and escapement statistics from the Alaska Department of Fish and Game. Asian chum salmon runs were estimated from catch statistics by the International North Pacific Fisheries Commission (e.g. 1990), Japan Fisheries Agency, and Pacific Research Institute of Fisheries and Oceanography (TINRO, Russia). Asian escapements were based on assumed exploitation rates of 0.6 for Russian runs and 1.0 for Japanese hatchery runs. Temperature effects on growth of Bristol Bay sockeye were examined by utilizing air temperatures in Bristol Bay during April-June (averages of monthly means for Dillingham and King Salmon weather stations) and inshore sea surface temperatures during January-June (monthly means for Kodiak in the Gulf of Alaska and Adak in the Aleutian Islands). Most Bristol Bay sockeye migrate to sea during May-July (Rogers, 1988) and the adults return from late June to mid-July; however, adults begin their homeward migrations in May. Surface water temperatures in outer Bristol Bay (offshore from Port Moller) during June were also available, but only since 1967, and temperatures were missing in 2 years (Helton, 1991 ). Mean lengths and weights of sockeye salmon in Bristol Bay runs during 1958-1977 were calculated from measurements of individual fish as described by Rogers (1980). For years 1978-1990, mean lengths and weights (catch only) were obtained from annual reports by Alaska Department of Fish and Game (e.g. Stratton, 1991 ). These reports present mean length and weight by age and sex for commercial catch samples and escapement samples (length only). Weight of sockeye in the escapement was estimated from previously described length-weight relationships (Rogers, 1980). Mean catch values of sockeye salmon were adjusted to live measurements by subtracting 2 m m from lengths and adding 11 g to weights. Catch and escapement means were then weighted by number of fish to obtain the means in the run to each
92
D,E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
of the five fishing districts, and means for the districts were weighted by numbers of fish to obtain means for the total Bristol Bay run. Examination of the relationship between adult sockeye salmon size, abundance, and environmental conditions was simplified by first selecting dominant age groups of the Bristol Bay run and determining which of eight measures of salmon abundance was best correlated with all dominant age groups. Mean lengths of male and female fish, which were more accurate than weights, were averaged (unweighted) to obtain four means for each year: ages 1.2 and 1.3 from the Nushagak District and ages 2.2 and 2.3 from the total Bristol Bay run. The Nushagak runs consistently contained large sample sizes of ages 1.2 and 1.3, whereas sample sizes were sometimes small for these ages in the Naknek-Kvichak, Egegik and Ugashik Districts. Adult length of each of the four age groups was regressed against eight salmon abundance estimates, i.e. runs of Bristol Bay sockeye, Western Alaska sockeye (including the South U n i m a k - S h u m a g i n Islands fishery in June), Western and Central Alaska sockeye, North Pacific sockeye (including Asian runs and catches on the high seas but excluding stocks south of Central Alaska), and sockeye plus chum salmon runs for each of these areas. Correlations were calculated for all years ( 1959-1991 ), and the recent warm period ( 1977-1991 ). All correlations were graphed and examined for non-linearity. The four correlation coefficients associated with each measure of abundance during 1959-1991 were averaged and the measure of abundance having the highest average correlation with mean length of the four age groups was then selected for further stepwise multiple regression with the measures of late-winter and spring temperatures (e.g. Port Moiler, Bristol Bay, air temperatures, and Kodiak and Adak water temperatures). Mean weights of each sockeye age group were also compared with the previously identified measures of abundance and temperature. Sockeye scales collected from commercial harvests in the Nushagak District during 1959-1988 were measured to provide an index of growth during each year at sea. The scales were measured by the Optical Pattern Recognition System (OPRS) at a magnification of 84X, following procedures described by Davis et al. (1990) and Z i m m e r m a n n ( 1991 ). Approximately 95 scales from each age group (ages 1.2 and 1.3) were measured and the unweighted mean of male and female measurements was used as the index of growth. Scale growth during the spring of capture was frequently resorbed and was therefore excluded from analysis. Correlation analysis followed the same procedures as that for adult length and weights. Results
The major Alaskan stocks of sockeye, chum and pink salmon have been under intense exploitation from commercial fisheries since the early 1900s. The exceptions are the c h u m salmon runs to the Yukon and Kuskokwim Riv-
93
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
ers in Western Alaska, which were not fished extensively until the 1970s. Trends in the historical catches of the three species are similar, but are especially close for sockeye and pink salmon (Fig. 1 ). Catches were very low in the early 1970s, then increased in the late 1970s to historical record levels for sockeye in 1990 and pinks in 1991. The low points in catches corresponded to low temperatures in the G u l f o f Alaska and cold winters in Bristol Bay, whereas the increase in catches coincided with mild winters in Bristol Bay and high temperatures at K o d i a k (Figs. 2 and 3). However, for the large catches in 1990 and 1991, winter temperatures in the G u l f o f Alaska were lower, whereas s u m m e r temperatures remained above average, and winter temperatures in the Aleutians ( A d a k ) were well above average (Table 1 ). Annual runs o f salmon (catch plus e s c a p e m e n t ) are better measures of the a b u n d a n c e o f salmon at sea than just the catches; however, we only have estimates of the runs since 1952 (Fig. 4). Most o f the recent increase in North Pacific chum salmon a b u n d a n c e were contributed by Japanese hatcheries (72% in 1989-1991 ), and Bristol Bay contributed most to the North Pacific sockeye runs (60% in 1989-1991 ). The annual runs of Bristol Bay sockeye have largely determined the year-to-year variation in the abundance of sockeye salmon in the North Pacific ( 1952-1991, r = 0 . 9 7 ) . []
Western
[]
Central
•
Southeast
125 100
........
o
i .........................~ ........ @ P i n k
Salmon-,~ ................. r.................. ~.......... ..., -
75 E
54~
50
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0 ]q5
.........
.........
12
~ .........
i
8 6
~ ...................
.........
~ Chum salmon
, ........................
i
_ _ ~ / ~
',
~
o 60
..........
5 0 o
!
.........
.........
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, ..................................................... !
[
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i
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i
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~ ........................~.
; ............ i -
zo
i
.................... i .....
............ . . . .
...... ............
........................ i ...................- . . . . . . . . . .
~ ....................... ,~............
¢_)
I0
20
30
40
50
60
70
80
90
Year Fig. I. A n n u a l c o m m e r c i a l s a l m o n catches in Alaska, ] 9 1 0 - 1 9 9 ].
94
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103 11
=
10
-Bristol
~ 9 •o_ E
7 6
4O
k~
/V•
Bay . . . . . . .
l ! !
.
~/ viv - v v t
"SI'IJ/ "
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.L -<
4
20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95
i 10
-1
-
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9 --
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8
~
7 ............
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'
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r'
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E
i
I
.................................... , ....
~ 6 i. . . . . . . . . . . . 2 0 2 5 3 0 3 5 4 0 4 5 50 55 6 0 65 7 0 75 8 0 85 9 0 95
Year Fig. 2. Annual summer (Apr.-Oct.) air temperatures in Bristol Bay (Dillingham and King Salmon ), 1921-1991, and sea surface temperatures at Kodiak ( G u l f of Alaska ), 1950-1991.
-2 " " l
.... ! ~ r l i ~
'
it
,:,
o
ivy
~-12
~-~4
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,:.,I....i....i,...i....i.
i
20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 6
~
i
"
= c~ E 4) O~ 09
7'0 2 5 3 0 3 5 4 0 4 5
5 0 55 6 0 6 5 7 0 75 8 0 8 5 9 0 9 5
Winter
beginning
Fig. 3. Annual winter ( N o v . - M a r . ) air temperatures in Bristol Bay, 1919-1920 to 1991-1992, and sea surface temperatures at Kodiak, 1950-1951 to 1991-1992.
The average lengths o f Bristol Bay sockeye did not change much between the colder-low-abundance years, 1 9 5 9 - 1 9 7 6 , and the warmer-high-abundance years of 1 9 7 7 - 1 9 9 1 (Table 2 ). Within Bristol Bay, lengths o f sockeye were similar a m o n g systems, and males were longer than females with the
95
D.E. Rogers, G.T Ruggerone / Fisheries Research I8 (1993) 89-103
Table 1 W i n t e r - s p r i n g temperatures ( ° C) in Southwest Alaska, 1952-1991; mean m o n t h l y temperatures for N o v e m b e r (Year - 1 ) to March (year), with regression estimates of missing data in parentheses Year
1952 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
Bristol Bay air temperature
Nov.Mar.
Apr.May
-8.2 -8.9 -10.8 -7.9 -12.5 -9.3 -6.8 -8.6 -7.5 -7.9 -9.0 -5.8 -9.4 -9.4 -9.5 -8.2 -7.0 -9.2 -7.0 -12.1 - 11.6 -9.1 -9.3 -11.6 -11.2 -3.4 -6.8 -4.3 -7.6 -4.8 -7.8 -5.2 -6.0 -5.4 -4.6 -3.6 -7.2 -9.1 -9.1 -7.7
-0.1 4.2 2.6 0.8 1.0 5.0 4.0 2.9 1.3 3.2 2.8 1.8 0.3 1.0 1.1 4.2 2.8 3.8 2.8 -0.5 -0.6 3.2 4.4 0.1 1.2 0.5 4.6 5.4 3.9 5.4 0.0 4.6 1.8 - 1.7 1.6 2.5 2.4 3.6 5.0 4.1
Port Moiler sea surface temperature, 11-30 June
8.6 6.6 6.8 5.8 2.8 3.3 5.1 (7.8) 5.1 4.4 7.2 7.0 8.8 5.9 10.2 6.1 9.2 9.0 5.6 (5.9) 5.5 7.2 6.1 6.9 5.2
Kodiak sea surface temperature
Adak sea surface temperature
Nov.Mar.
Apr.May
Nov.Mar.
Apr.May
1.6 2.0 1.5 1.6 0.2 0.2 2.2 1.0 2.0 2.1 0.5 2.6 2.1 (0.7) (2.0) 1.7 2.4 2.3 3.8 1.7 1.3 (2.7) 2.4 2.7 3.1 5.8 4.4 4.9 4.8 5.5 2.9 3.5 4.1 3.2 2.8 3.6 3.6 2.3 2.2 2.4
4.4 5.2 5.4 5.3 3.8 5.1 6.2 5.3 4.9 5.6 5.1 5.6 4.6 (5.1) (3.9) 5.7 5.4 5.5 6.1 3.3 3.3 (4.5) 5.0 4.2 5.0 7.7 6.6 7.9 7.4 7.8 4.5 6.5 6.0 5.0 5.1 6.6 7.3 6.4 6.7 6.4
3.6 3.0 2.9 3.4 3.4 3.0 3.2 3.6 3.7 3.2
4.7 4.7 4.2 4.1 4.0 4.5 4.4 4.8 4.1 4.3 4.2 4.7 3.1 3.1 3.2 4.3 3.9 3.8 3.8 3.3 3.6 3.4 3.8 4.0 3.8 4.0 4.6 4.1 3.5 4.1 4.1 3.9 4.2 4.6 (4.4) 5.8 4.5 4.8 5.0 4.7
3.1
3.3 3.5 3.4 3.5 3.4 3.7 3.3 3.1 3.7 3.5 3.4 3.5 3.9 3.6 3.4 3.2 3.9 3.2 3.5 4.5 (3.8) (4.5) 4.3 4.1 4.3 4.6
96
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
Western Alaska ~
i
I
150
!
i, ...........S , ockeye + chum-
o 100
i^-I
!
North Pacific
175
.... I
i
/
E 7s c SO c~ 25 0
50
: -- 55
80 ............i
60
65
i
i
70
....
75
80
85
90
Chum
co 60 ~
i
40
l
o 50
~ , ~ . ,.o:o~. ~ , / ~ SS
60
80
0 50
95
65
i
SS
60
65
70
75
80
85
90
95
80
85
90
95
Sockeye
70
75 Year
Fig. 4. Annual runs (catch plus escapement) of sockeye and chum salmon to Western Alaska and the North Pacific (Western-Central Alaska plus Asia), 1952-1991. exception of the Naknek stocks. The N a k n e k 2-ocean males were exceptionally small and usually shorter than the females. The annual m e a n lengths o f Nushagak and Bristol Bay sockeye for the runs during 1959-1991 were m o r e closely correlated with the n u m b e r o f sockeye in the Bristol Bay run than with any o f the other seven measures of abundance (Figs. 5 and 6). However, when correlations were calculated separately for the two periods ( 1959-1976 and 1977-1991 ), the North Pacific run o f sockeye plus c h u m salmon provided somewhat higher correlations than the Bristol Bay sockeye runs alone. Therefore, in further stepwise multiple regression analyses, we included the annual n u m b e r o f North Pacific c h u m salmon (essentially Japanese hatchery c h u m s ) as a variable together with abundance of Bristol Bay sockeye and several measures of temperature. In contrast to the significant relationships between m e a n length o f Nushagak and Bristol Bay sockeye and abundance of Bristol Bay sockeye salmon, the unweighted m e a n lengths in the returns from a brood year were not significantly correlated ( P > 0.05 ) with the n u m b e r o f sockeye in the return (i.e.
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
97
Table 2 Mean lengths ( mid-eye to tail fork; mm) of sockeye salmon in Bristol Bay runs and escapements (numbers of fish in millions) District runs Years
Naknek
Kvichak Egegik Ugashik Nushagak
Age 1.2
Age 2.2
Age 1.3
Age 2.3
Run Male Female Run
Male Female Run Male Female Run
Male Female
1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991
2.6 4.8 0.2 0.7 0.3 0.9 1.0 1.7
509 511 521 522 523 527 517 512
497 502 508 508 509 508 496 493
7.0 8.1 1.0 3.0 0.3 1.3 0.3 0.3
521 525 532 535 535 537 527 529
510 514 515 518 514 517 505 507
1.1 3.3 0.3 1.2 0.2 0.9 1.0 3.6
580 579 587 587 591 591 585 584
561 562 568 569 572 569 556 554
1.1 1.7 0.6 1.4 0.1 0.4 0.1 0.2
584 583 591 593 596 595 586 585
567 567 573 575 573 572 558 559
1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991 1959-1976 1977-1991
1.4 1.8 0.2 0.3 0.1 0.2 0.2 0.4 0.5 0.6 0.1 0.1
510 516 487 471 520 517 523 527 512 509 522 537
499 500 485 479 504 501 508 505 491 486 498 509
3.8 3.7 0.4 0.4 0.5 0.6 0.2 0.4 0.1 0.1 <0.1 <0.1
522 529 498 492 531 532 534 536 517 520
507 512 501 498 511 512 511 512 498 498
0.2 0.4 0.2 0.6 0.1 0.2 0.1 0.4 0.3 0.5 0.1 0.3
580 581 576 578 589 592 593 601 577 577 589 598
560 561 556 559 563 569 572 572 550 549 554 561
0.3 0.3 0.2 0.3 0.3 0.3 <0.1 0.1 <0.1 <0.1 <0.1 <0.1
587 587 580 585 591 599 599 605 -
564 567 564 566 570 575 571 574 -
Escapements
Kvichak Naknek
Egegik Ugashik Wood lgushik
age 1.2 in year+ 4, ages 2.2 and 1.3 in year+ 5, and age 2.3 in year+ 6 ). Thus, there was no indication of a brood year effect on adult size. During stepwise multiple regression analyses of length and weight measurements for the four age groups during two sets of years ( 1959-1991 and 19771991 ), different temperature measurements entered the regressions that included Bristol Bay run size. The mean sea surface temperature at Kodiak during January-May (Fig. 5 ) showed the highest average partial correlation and occurred most frequently in the eight regressions; therefore, mean sea surface temperature at Kodiak during January-May was used in all models where temperature was significantly correlated. For age 1.2 sockeye, temperature was more highly correlated with mean lengths and weights than number of sockeye in the run; however, for age 2.3 sockeye during 1977-1991, temperature was not significantly correlated with the deviations from the regressions of length or weight on Bristol Bay run (Table 3). Thus, size of adult sockeye salmon in Bristol Bay was inversely related to Bristol Bay run size and positively related to Kodiak water temperature during winter and spring. In no
98
D.E. Rogers, G. T, Ruggerone / Fisheries Research 18 (1993) 89-103 ....
70
+....
Bristol
_o
+ runs
Bay
i
.........
F K
.,,.o
I
+ zo ;o \ 0
AJ\Ji\[~, I
. . . . . . . . . . . .
50
55
+ .....
60
600 "-E E
+-
I "
' . . . . . . . . .
65
•
.
-
+
70
•
•
•
+
75
•
•
•
{
80
.
.
.
F
85
•
•
•
~ ....
90
95
~
580 Nush 1.3 ~%
560 ~'
~
__
540
g s2o Nush 1.2-~
500
480
._._ -
. . . . . . . . . 50
55
7
t
6
60
} ..... 65
J.... I
, 70
. . 75
80
I-
85
.... I
90
95
+
s E >x:
4 3 2
0 50
....
. . . . . . . .
55
60
] . . . . . . . .
65
70
. . . .
75
+ . . . . . . . .
80
85
....
90
95
Year
Fig. 5. Annual Bristol Bay sockeye runs, mean lengths in the runs and Kodiak sea surface temperatures for winter-spring months. instances were there significant partial correlations with numbers o f chum salmon. Scale radii measurements o f Nushagak District sockeye for each year at sea ( 1 9 5 6 - 1 9 8 8 ) indicated that growth was positively related to temperature during the first (ages 1.2 and 1.3 ) and second (age 1.3 only) years at sea (Fig. 7, Table 4 ) . Growth during the last full year at sea was not correlated with temperature. Since 1974, only growth during the first year at sea of age 1.2 sockeye was correlated with temperature. Salmon run size during the year o f return was not correlated with scale growth during each year at sea. However, adult returns from annual smolt migrations (e.g. ages 1.2 and 2.2 in y e a r + 2 and ages 1.3 and 2.3 in y e a r + 3 ) were positively correlated with growth of age 1.2 sockeye, but not age 1.3 sockeye, during the first year at sea. Scale growth during the first and second years at sea and total scale length at each age were not correlated with adult length. However, growth during the third year (age 1.3 ) was positively correlated with adult length ( r = 0.50 ).
99
D.E. Rogers, G. 72 Ruggerone / Fisheries Research 18 (1993) 89-103 y
E E
=
576.11
o
580
- 0.26424x
di
6
~L_
R^2
=
0.273
- - - + - Nush 1 . 3 -
io"
y = 584.24
- 0.23095x
I'o1
] ........
590 ---<~
' ....
i
560570_ ° _ ~ _ ° - - ° ~
~6--
-
b-- - 0 i
ca
' "" 0 I0
20
30
40
y=510.28-O.21911x .......
520
u~ ¢)
ca
'l
"
2.3~
D
---~ 0
9o-T--~
i
90
550
,=,
~--BB !
s
D
= 0.297
~
Ce
580 o)
R^2
!
60
70
R^2=0.144
I .....
~ !
50
535~• .
Nush 1.2
5,o -&
525
soooo
515
490
!
480
1 0
.
.
.
.
.
10
9 0. .-.-. . . . . . . . .-.- 91 ~E~I--T i,,,, 20
30
40
50
60
Bristol Bay run (millions)
70
495
.
.
.
.
.
.
2] ......
505 - i ~
70
y : 527.64 - 0.29249x RA2 = 0.220
i ........
•
560 .... I .... i .... 1.... i .... i_ I. 0 I0 20 30 40 50 60
o~
0
~ .....
e ....
elgO
.... I !a . . . . 2030 4050 6070 Bristol Bay run (millions) 10
Fig. 6. Linear regressions o f m e a n length o n Bristol Bay r u n for the 1959-1991 runs (solid points for the 1977-1991 r u n s ) . Table 3 Linear regressions of length and weight on water temperature and abundance of Bristol Bay sockeye salmon Age group
Years
Regression
R2
Nushagak 1.2
1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991 1959-1991 1977-1991
L = 5 0 3 +2.46 (SST) - 0 . 2 9 2 ( R U N ) L = 4 8 1 +5.75 (SST) - 0 . 1 4 4 ( R U N ) W=2.12 +0.037 (SST) - 0 . 0 0 4 4 ( R U N ) W = 1.81 +0.082 (SST) - 0 . 0 0 2 1 ( R U N ) L = 5 6 7 +3.14 (SST) - 0 . 3 5 7 ( R U N ) L = 5 6 2 +3.80 (SST) - 0 . 3 1 2 ( R U N ) W=3.12 +0.072 (SST) -0.0071 ( R U N ) W=3.08 +0.073 (SST) - 0 . 0 0 6 1 ( R U N ) L = 5 1 5 +4.46 (SST) - 0 . 4 1 5 ( R U N ) L = 5 2 4 +2.80 (SST) - 0 . 3 9 1 ( R U N ) W=2.21 +0.065 (SST) - 0 . 0 0 5 7 ( R U N ) W=2.35 +0.038 (SST) - 0 . 0 0 5 2 ( R U N ) L = 5 7 9 +2.04 (SST) - 0 . 2 9 8 ( R U N ) L=591 -0.346 (RUN) W=3.15 +0.056 (SST) - 0 . 0 0 6 5 ( R U N ) W=3.47 - 0 . 0 0 7 7 ( R U N )
0.25 0.52 0.25 0.56 0.49 0.57 0.46 0.52 0.49 0.42 0.53 0.46 0.43 0.51 0.57 0.73
Nushagak 1.3
Bristol Bay 2.2
Bristol Bay 2.3
L, Mean length of males and females, mean of means (mid-eye to tail fork; mm ). W, Mean weight of males and females, mean of means (kg). SST, Mean monthly sea surface temperature ( ° C ) at Kodiak for January-May in the year of the run. RUN, Bristol Bay sockeye run, in millions offish.
100
D.E. Rogers, G. 72 Ruggerone / Fisheries Research 18 (1993) 89-103 11oo
g
lOOO
c
.... I
.
An
900 h5
8(n
800
I
2nd year
g
6
I
700
Age 1.2 600 500 5o
.~
55
1100
60
65
I I =
70 I Age 1.3
~ 1000"1styeir~000 ~/~ ~ _o
700. ~,~y!
"
75
80
85
90
" ~¢:~p
~ i~
~
o0o ~;
i ar 500 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 55 60 65 70 Year
of
75
80
85
90
growth
Fig. 7. A n n u a l m e a n s o f scale m e a s u r e m e n t s (H) during each year at sea for N u s h a g a k sockeye salmon, ages 1.2 a n d 1.3. C o m m e r c i a l catch samples, 1959-1988.
Table 4 Linear regressions o f scale radii m e a s u r e m e n t s (H) f r o m N u s h a g a k District sockeye d u r i n g each year o f ocean growth on t e m p e r a t u r e a n d a b u n d a n c e o f s a l m o n Age g r o u p
O c e a n year
Years
Regression
1.2 1.2 1.2 1.2 1.3 1.3 1.3 1.3 1.3 "~.3
1 1 2 2 1 1 2 2 3 3
1957-1986 1975-1986 1958-1987 1976-1987 1956-1986 1974-1986 1957-1987 1975-1987 1958-1988 1976-1988
S=864.4+15.59 S=871.6+24.41 S = 8 1 7 . 4 + 19.98 S = 7 6 5 . 2 + 17.01 -
R2 (AIR) +l.01 (RETURN (AIR)
(AIR) (SST)
0.36 0.56 NS NS 0.35 NS 0.22 NS NS NS
S, U n w e i g h t e d m e a n length o f male a n d female scale radii m e a s u r e m e n t s for given t i m e period at sea. AIR, A p r i l - J u n e air t e m p e r a t u r e m e a s u r e d at K i n g S a l m o n a n d Dillingham. R E T U R N , Adults r e t u r n i n g to Bristol Bay ( m i l l i o n s ) f r o m a n n u a l smolt migrations. SST, M e a n m o n t h l y sea surface t e m p e r a t u r e ( ° C ) at K o d i a k d u r i n g N o v e m b e r - M a r c h before the fish's second growing period at sea. NS, N o t significant at ce=0.05.
D.E. Rogers, G.T. Ruggerone /Fisheries Research 18 (1993) 89-103
10 1
Discussion Major changes in salmon runs have generally followed changes in winter temperatures over southwestern Alaska (Rogers, 1980, 1984). Low runs in the early 1970s corresponded to low temperatures in the Gulf of Alaska and cold winters in Bristol Bay, whereas the greater runs beginning in the late 1970s coincided with mild winters in Bristol Bay and high temperatures at Kodiak. However, for the large runs in 1990 and 1991, winter temperatures in the Gulf of Alaska had decreased, whereas s u m m e r temperatures remained above average and winter temperatures in the Aleutians (Adak) were well above average. Mean size of Bristol Bay sockeye was inversely related to Bristol Bay run size and positively related to mean monthly sea surface temperature at Kodiak during January-May. However, sockeye in 1991 were 10-15 m m shorter ( 126-177 g lighter) than predicted and the 2-ocean sockeye in 1990 were 10 m m shorter than predicted. Preliminary data from the large 1992 Bristol Bay run (about 45 million sockeye salmon) indicate that sockeye returning in 1992 were also exceptionally small. The explanation for this unusually small size is unknown, although the exceptionally large consecutive runs of sockeye, chum, and pink salmon since 1990 were probably influential. Nevertheless, the small size of sockeye salmon returning to Bristol Bay in 1992 was a useful factor in developing an in-season forecast of run strength. Year-to-year variation in the maturation rate of sockeye at sea probably affects the mean lengths of fish returning from a given brood year. The 2ocean sockeye that return to Bristol Bay are about 82% heavier than immature 2-ocean sockeye still at sea in July and that will mature as 3-ocean sockeye the following year (Harris and Rogers, 1979). There was usually very little overlap in the length frequencies of mature and immature sockeye in June. Jacks or l-ocean sockeye were not abundant in the Bristol Bay runs, therefore sample sizes were usually small; however, over all years, the age 1.1 males averaged 35 cm and age 2.1 males averaged 37 cm. The age 1.1 immature salmon at sea averaged 30.5 cm and age 2.1 averaged 33 cm; thus jacks were about 4 cm longer than the 1-ocean male and female sockeye at sea. In 1991 and 1992, the small age-specific size of Bristol Bay sockeye salmon was coincident with additional years at sea, i.e. slower maturation rate. In 1992, an unusually large percentage of age .4 sockeye returned, indicating the effect of reduced growth on maturation rate. Density effects on growth probably occur during the homeward migration because Bristol Bay salmon are more concentrated at that time and are actively feeding (Nishiyama, 1984; Helton, 1991). This hypothesis is supported by the little or no correlation between scale growth and adult size, the lack of density-dependent growth during earlier years at sea, and the lack of density-dependent growth associated with brood year returns. Year-to-year variation in spring temperatures affects not only the growth of Bristol Bay
102
D.E. Rogers, G.T. Ruggerone / Fisheries Research 18 (1993) 89-103
sockeye, but also their migratory timing and routes of migration (Fujii, 1975 ), which could also indirectly affect their growth. For Bristol Bay sockeye, slower growth early in life leads to larger size at maturity (i.e. older age at maturation), whereas slower growth during the final few months at sea results in smaller than average size. Acknowledgments Funding for this investigation was provided by the Pacific Seafood Processors Association and Washington Sea Grant. M. Zimmermann carefully measured the sockeye scales from the Nushagak District. We are grateful to D. Beauchamp and A. Tyler for their constructive comments.
References Davidson, F.A. and Vaughan, E., 1941. Relation of population size to marine growth and time of spawning migration in the pink salmon (Onchorhynchus gorbuscha) of Southeastern Alaska. J. Mar. Res., 4." 231-246. Davis, N.D., Myers, K.W., Walker, R.V. and Harris, C.K., 1990. The Fisheries Research Institute's high seas salmonid tagging program and methodology for scale pattern analysis. Am. Fish. Soc. Symp., 7: 863-879. French, R., Bilton, H., Osaka, M. and Hartt, A., 1976. Distribution and origin of sockeye salmon (Onchorynchus nerka) in offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull., 34, 113 pp. Fujii, T , 1975. On the relation between homing migration of the western Alaska sockeye salmon Onchorynchus nerka (Walbaum) and oceanic conditions in the eastern Bering Sea. Mere. Fac. Fish. Hokkaido Univ., 22(2): 99-191. Harris, C.K. and Rogers, D.E., 1979. Forecast of the sockeye salmon run to Bristol Bay in 1979. Univ. Wash. Fish. Res. Inst. Circ., 79-2, 50 pp. Helton, D.R., 1991. An analysis of the Port Moller offshore test fishing forecast of sockeye and chum salmon runs to Bristol Bay, Alaska. M.S. Thesis, University of Washington, Seattle, WA, 122 pp. International North Pacific Fisheries Commission, 1990. Statistical Yearbook 1990. INPFC, Vancouver, B.C., 133 pp. Marshall, R.P. and Quinn, II, T.J., 1988. Estimation of average weight and biomass of pink, chum, sockeye and coho salmon in Southeast Alaska commercial harvests. Alaska Dep. Fish Game Fish. Res. Bull., 88-07, 52 pp. Neave, F., Yonemori, T. and Bakkala, R.G., 1976. Distribution and origin of chum salmon in offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull., 35, 79 pp. Nishiyama, T., 1984. Two important factors in the oceanic stages of salmon: food and temperature, In: Proceedings of the Pacific Salmon Biology Conference (USSR, USA, Canada, Japan). Yuzhno-Sakhalinsk, USSR, 1978. TINRO, Vladivostok, pp. 227-258. Ricker, W.E., 1989. History and present state of the odd-year pink salmon runs of the Fraser River Region. Can. Tech. Rep. Fish. Aquat. Sci., 1702, 37 pp. Rogers, D.E., 1980. Density-dependent growth of Bristol Bay sockeye salmon, In: W.J. McNeil and D.C. Himsworth (Editors), Salmonid Ecosystems of the North Pacific. Oregon State University Press, Corvallis, OR, pp. 267-283.
D.E. Rogers, G. 72 Ruggerone / Fisheries Research 18 (1993) 89-103
103
Rogers, D.E., 1984. Trends in abundance of northeastern Pacific stocks of salmon, In: W.G. Pearcy (Editor), The Influence of Ocean Conditions on the Production of Salmonids in the North Pacific. Oregon State University Press, Corvallis, OR, pp. 100-127. Rogers, D.E., 1987a. Pacific salmon, In: D.W. Hood and S.T. Zimmerman (Editors), The Gulf of Alaska: Physical Environment and Biological Resources. US Government Printing Office, Washington, DC, pp. 461-476. Rogers, D.E., 1987b. The regulation of age at maturity in Wood River sockeye salmon (Oncho~ rynchus nerka). In: H.D. Smith, L. Margolis and C.C. Wood (Editors), Sockeye Salmon (Onchorynchus nerka) Population Biology and Future Management. Can. Spec. Publ. Fish. Aquat. Sci., 96: 78-89. Rogers, D.E., 1988. Bristol Bay smolt migrations, In: W.J. McNeil (Editor), Salmon Production, Management, and Allocation. Oregon State University Press, Corvallis, pp. 87-101. Stratton, B.L., 1991. Abundance, age, sex and size statistics for Pacific salmon in Bristol Bay, 1990. Alaska Dep. Fish Game Tech. Fish. Rep., 91-15, 153 pp. Takagi, K., Aro, K.V., Hartt, A.C. and Dell, M.B., 1981. Distribution and origin of pink salmon (Onchorynchus gorbuscha) in offshore waters of the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull., 40, 195 pp. Zimmermann, M., 1991. Trends in the freshwater growth of sockeye salmon (Onchorynchus nerka) from the Wood River Lakes and Nushagak Bay, Alaska. M.S. Thesis, University of Washington, Seattle, WA, 119 pp.