Journal of Fish Biology (2009) 75, 1287–1301
doi:10.1111/j.1095-8649.2009.02364.x, available online at www.interscience.wiley.com
Linking marine and freshwater growth in western Alaska
Chinook salmon Oncorhynchus tshawytscha
G. T. Ruggerone*†, J. L. Nielsen‡ and B. A. Agler§
*Natural Resources Consultants, 4039 21st Avenue West, Suite 404, Seattle, WA 98199,
U.S.A., ‡U.S. Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage,
AK 99508, U.S.A. and §Alaska Department of Fish and Game, Division of Commercial
Fisheries, Mark, Tag, and Age Lab, 10107 Bentwood Place, Juneau AK 99801, U.S.A.
(Received 4 December 2008, Accepted 28 May 2009)
The hypothesis that growth in Pacific salmon Oncorhynchus spp. is dependent on previous growth
was tested using annual scale growth measurements of wild Chinook salmon Oncorhynchus
tshawytscha returning to the Yukon and Kuskokwim Rivers, Alaska, from 1964 to 2004. Firstyear marine growth in individual O. tshawytscha was significantly correlated with growth in fresh
water. Furthermore, growth during each of 3 or 4 years at sea was related to growth during the
previous year. The magnitude of the growth response to the previous year’s growth was greater
when mean year-class growth during the previous year was relatively low. Length (eye to tail fork,
LETF ) of adult O. tshawytscha was correlated with cumulative scale growth after the first year
at sea. Adult LETF was also weakly correlated with scale growth that occurred during freshwater
residence 4 to 5 years earlier, indicating the importance of growth in fresh water. Positive growth
response to previous growth in O. tshawytscha was probably related to piscivorous diet and foraging
benefits of large body size. Faster growth among O. tshawytscha year classes that initially grew
slowly may reflect high mortality in slow growing fish and subsequent compensatory growth in
survivors. Oncorhynchus tshawytscha in this study exhibited complex growth patterns showing a
positive relationship with previous growth and a possible compensatory response to environmental
 2009 The Authors
factors affecting growth of the age class.
Journal compilation  2009 The Fisheries Society of the British Isles
Key words: Bering Sea; compensatory growth; enhanced growth; salmon recovery; scales.
INTRODUCTION
Growth in Pacific salmon Oncorhynchus spp. has a strong influence on survival
to maturity, life-history characteristics and reproductive success (Beamish et al .,
2004; Vøllestad et al ., 2004; Quinn, 2005). Greater growth of Oncorhynchus spp.
in fresh water (Henderson & Cass, 1991; Koenings et al ., 1993), early marine life
(Ruggerone & Goetz, 2004; Moss et al ., 2005; Farley et al ., 2007) and during the
second year at sea (Ruggerone et al ., 2003) has been associated with greater survival.
Mechanisms linking growth to survival involve higher rates of predation on smaller
slow growing individuals and higher lipid content of faster growing individuals that
may enable Oncorhynchus spp. to survive through the winter when prey are less
available (Beamish & Mahnken, 2001). Outside of harvest, however, the cause of
†Author to whom correspondence should be addressed. Tel.: +1 206 285 3480; fax: +1 206 283 8263;
email: GRuggerone@nrccorp.com
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death at sea is rarely quantified. Growth also affects key salmonid life-history traits,
such as age at maturation, fecundity and egg size (Healey, 1986; Jonsson et al ., 1996;
Quinn et al ., 2004). Larger Oncorhynchus spp. have greater competitive ability during mating, although large body size is disadvantageous in shallow streams (Blair
et al ., 1993; Hamon & Foote, 2005). The evolution of anadromy in Oncorhynchus
spp. is probably a response to increased growth and associated benefits gained by
migrating to sea where numerous large prey can be found (Gross et al ., 1988; Helle,
1989; Quinn & Myers, 2005).
Genetic and environmental factors influence the growth rates of Oncorhynchus
spp. In nature, some fishes may encounter periods of low prey availability or low
temperatures leading to reduced growth. Compensatory growth is a phase of accelerated growth when favourable conditions are restored after a period of depressed
growth (Ali et al ., 2003). Although reduced growth may lead to higher risks of
predation and mortality, a variety of studies indicate individual fishes can undergo
compensatory growth such that their growth rate exceeds that of fishes that were
initially larger (Bilton & Robins, 1973; Damsgard & Dill, 1998; Ali et al ., 2003).
Salmonids can exhibit enhanced growth at different life stages, such as during an
ontogenetic shift in diet from zooplankton to forage fishes and squid (Kaeriyama
et al ., 2000; Kelley, 2001). At higher latitudes, fish growth at sea is typically faster
than growth in fresh water (Gross, 1987; Vøllestad et al ., 2004). Faster growing
fishes may be more capable of capturing larger prey at an earlier age, leading to
greater metabolic efficiency, increased growth and higher survival rates (Mortensen
et al ., 2000; Quinn, 2005). Timing of an ontogenetic shift in diet among pink
Oncorhynchus gorbuscha (Walbaum) and sockeye salmon Oncorhynchus nerka (Walbaum) in the North Pacific Ocean may be important for subsequent growth (Aydin,
2000, Aydin et al ., 2005). Salminen (1997, 2002) reported that large Atlantic salmon
Salmo salar L. smolts experienced enhanced growth relative to small members of
the cohort because large salmon had greater access to large and energy-rich herring
Clupea harengus L.
The hypotheses of compensatory, enhanced or random growth responses of fishes
to previous growth were tested among Chinook salmon Oncorhynchus tshawytscha
(Walbaum). These tests examined whether O. tshawytscha growth at sea was dependent on preceding growth in fresh water and the extent to which growth dependency
continued through each of 3 or 4 years of marine residence. The approach utilized
a long-term collection of scales, which provide an index of growth during each life
stage (Clutter & Whitesel, 1956; Bilton, 1975; Fukuwaka & Kaeriyama, 1997; Fisher
& Pearcy, 2005). Growth of individual O. tshawytscha during each year or life stage,
based on scale annuli, was compared with growth during the previous year. A positive correlation within each year class of O. tshawytscha would indicate growth
enhancement, a negative correlation would suggest growth compensation and a lack
of correlation would suggest random growth.
MATERIALS AND METHODS
SCALE COLLECTION AND MEASUREMENTS
The study utilized scales from adult wild O. tshawytscha returning to the Yukon (64◦ 00"
N; 164◦ 14" W) and Kuskokwim Rivers (59◦ 58" N; 162◦ 26" W), Alaska, from 1964 to 2004.
 2009 The Authors
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These catchments, the largest in Alaska, have supported annual O. tshawytscha harvests (commercial and subsistence) averaging 147 000 and 99 000 fish, respectively, since 1961 (Bue &
Hayes, 2006; Whitmore et al ., 2008). Scales were obtained from the Alaska Department of
Fish and Game (ADFG) archive in Anchorage, Alaska (http://www.adfg.state.ak.us/). For the
Yukon River, scales were selected for measurement only when they were from O. tshawytscha
captured with set gillnets (21·6 cm stretched mesh) located in the lower river (river km
20–30). Fewer scales were available from fish harvested in the Kuskokwim River; therefore,
these scales were selected from multiple gear types. In most years, Kuskokwim O. tshawytscha
scales were selected from fish captured by gillnets (15·2 or 21·6 cm mesh) in the mainstem
river near Bethel, but some scales were sampled at tributary weirs. The scales were typically
obtained from one gear type within a given year. In both catchments, scales were primarily
collected from June to July in an attempt to consistently select fish from the same stocks.
Approximately 50 scales from each of the two dominant O. tshawytscha age groups from
both the Yukon and Kuskokwim Rivers were measured, i.e. c. 200 scales per year. These fish
spent one winter in fresh water (i.e. river-type fish) and three (age 1·3) or four winters (age
1·4) in the ocean. Scales were selected for measurement only when: (1) the age determination agreed with the one previously made by ADFG, (2) the scale shape indicated the scale
was removed from the preferred area (Koo, 1962) and (3) the circuli and annuli were clearly
defined and not affected by scale regeneration or significant resorption along the measurement
axis.
Scale measurements followed procedures described by Hagen et al . (2001). After selecting a scale for measurement, the scale was scanned from a microfiche reader and stored as
a high resolution digital file. The high resolution image (3352 × 4425 pixels) allowed the
entire scale to be viewed and provided enough pixels between narrow circuli to ensure accurate measurements of circuli spacing. The digital image was loaded in Optimas 6·5 image
processing software (www.mediacy.com) to collect measurement data using a customized
programme. The scale image was displayed on an LCD monitor, and the scale measurement
axis was defined as the longest axis extending from the scale focus. Distance (mm) between
circuli was measured within each growth zone, i.e. growth through the first winter in fresh
water from the scale focus to the outer circulus of the first freshwater annulus (FW1), spring
plus growth zone (FWPL) extending from the last FW1 circulus to the first marine circulus
(smolt transition period), each annual ocean growth zone (SW1, SW2, SW3 and SW4), and
from the last ocean annulus to the edge of the scale (SWPL). Data associated with each scale,
such as date of collection, location, sex, fish length (mid-eye to tail fork, LETF ) and capture
method, were included in the dataset.
D ATA A N A LY S I S
Linear regressions were performed to determine whether scale growth during each life
stage (FWPL, SW1, SW2, SW3, SW4 and SWPL) could be explained by scale growth during
the previous stage. Regressions were performed annually for scale growth measurements of
individual fish from each stock (Yukon and Kuskokwim) and each age group (ages 1·3 and
1·4). Sample groups having <20 scale measurements were excluded from regression analysis.
Exploratory analyses indicated that the best explanatory variable was the distance across the
five widest (adjacent) circuli during the previous stage (four circuli in FW1). Total annual scale
growth could have also been used as the primary explanatory variable. It yielded comparable
results, but peak circuli growth consistently provided the highest correlation. When comparing
growth during the smolt transition period (FWPL) with growth in fresh water, the entire FW1
scale growth was used because juvenile size has been shown to affect timing of Oncorhynchus
spp. smolt migration and therefore growth during this brief transition period (Burgner, 1962).
It was hypothesized that growth of individual O. tshawytscha during the past four decades
was dependent on the previous year’s growth. A t-test was used to examine whether regression
slopes (mm per mm of scale growth) calculated for each year class, age group, stock and life
stage were statistically different from zero (α = 0·05).
Growth of O. tshawytscha during each life stage was expected to vary from year to year.
Therefore, additional regressions were calculated to determine whether the regression slopes
(scale growth v. previous year’s growth) were related to mean scale size of the year class
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during the previous life stage. In other words, was the magnitude of the growth response
dependent on prior mean scale growth of the fish year class? Scale growth values were based
on the mean of ages 1·3 and 1·4 fish. Mean scale size was calculated from the mean of
normalized values (s.d. > or < the long-term mean) for males and females, which may
experience differential growth. This analysis only involved Yukon River fish because scales
from Yukon River fish were collected consistently across all years (same location, gear and
mesh size), thereby minimizing possible bias in annual mean values associated with different
sampling methods. The Durbin–Watson statistic (Kutner et al ., 2005) was used to test for
autocorrelation among regression residuals. If the presence of autocorrelation was significant
or inconclusive, then the slope of the previous year class was included in a multiple regression
as a means to remove autocorrelation. Partial residual analysis (Larsen & McCleary, 1972)
was used to show the relationship between the regression slope of a year class and the growth
during the previous year after removing the autocorrelation effect.
The adult LETF of individual O. tshawytscha (all stocks and ages combined) was compared
with their scale measurements using regression analysis to examine whether scale growth
was related to LETF . Exploratory analyses indicated a variety of scale measurements were
correlated with adult LETF , but the analysis presented here was based on cumulative scale
growth from the second year at sea (SW2) through to the third circulus of the homeward
migration period (SWPL). The outer SWPL zone was excluded due to scale resorption beyond
the third circuli in some scales.
Correlation between adult LETF and scale growth in fresh water 4 to 5 years earlier was
expected to be weak. Correlation coefficients were calculated for each stock, age group and
year of adult return. Two methods were used to test for positive correlation across all years.
First, a χ 2 test using Yates correction for continuity was used to test the null hypothesis that
the frequency of positive correlations across the past four decades was random (i.e. 0·5), as
expected if growth in fresh water had no effect on adult LETF . Second, a t-test was used to
evaluate whether the mean annual correlation coefficient during the past four decades was >0.
RESULTS
G R O W T H R E L AT I O N S H I P S W I T H I N I N D I V I D U A L
O N C O R H Y N C H U S T S H AW Y T S C H A
A total of 690 regressions were performed to evaluate the relationship between
annual scale growth of individual O. tshawytscha and previous year’s growth for
each year of adult return from 1964 to 2004. Age 1·4 scales from O. tshawytscha
returning to the Yukon River in 1991 provided an example of these regressions during
each life stage (Fig. 1). Annual growth during each life stage at sea was correlated
with the previous year’s growth (P < 0·001), with one exception. Annual growth
during the smolt transition from fresh to marine waters (brief transition and minimal
growth) was not correlated with freshwater growth (P > 0·05).
On average, 48% of the 131 regressions of early marine growth (SW1) on freshwater growth (FW1) were positively correlated and statistically significant (P < 0·05),
indicating that growth during the first year at sea was related to growth during freshwater residence (Table I). This pattern held for each stock and age group. Negative
correlations represented only 15% of the total, and none were statistically significant.
The variability in early marine growth explained by peak growth in fresh water was
13%, on average, but it reached as much as 55% for age 1·3 fish returning to the
Kuskokwim River in 1975 (Table I).
The relationship of scale growth to the previous year’s growth increased during
later life stages in the ocean. On average, 71% of the 131 regressions of SW2 on SW1
growth had a positive slope and were statistically significant (P < 0·05), and 98% of
 2009 The Authors
Journal compilation  2009 The Fisheries Society of the British Isles, Journal of Fish Biology 2009, 75, 1287–1301
Number of
years
3%
21%
9 ± 9%
41 ± 14%
0·05 ± 0·01
0·39
37·0
40·7
38%
41%
48 ± 13%
85 ± 12%
0·13 ± 0·03
0·55
47%
67%
SW1
on FW1
52%
72%
71 ± 13%
98 ± 3%
0·22 ± 0·04
0·81
79%
79%
SW2
on SW1
41%
59%
64 ± 21%
96 ± 2%
0·19 ± 0·07
0·59
62%
92%
SW3
on SW2
NA
48%
60 ± 17%
97 ± 4%
0·15 ± 0·03
0·48
NA
72%
SW4
on SW3
76%
100%
90 ± 10%
99 ± 2%
0·40 ± 0·03
0·73
95%
89%
SWPL on
SW3 or SW4
FWPL, scale growth during the smolt transition period in spring from fresh water to the ocean; FW1, scale growth during the first year in fresh water; SW1, scale
growth during the first year at sea; SW2, scale growth during the second year at sea; SW3, scale growth during the third year at sea; SW4, scale growth during the
fourth year at sea; SWPL, scale growth during the homeward migration.
0%
13%
FWPL
on FW1
42·7
50·0
Average scales
per year
Yukon (1966–2004)
Age 1·3
34
Age 1·4
39
Kuskokwim (1964–2004)
Age 1·3
29
Age 1·4
29
Mean ± s.d. % significant regressions
Mean ± 1 s.d. % positive slopes
Mean ± s.d. coefficient of determination (r 2 )
Maximum coefficient of determination (r 2 )
Stock & Age
Regression
Table I. Percentage of annual life-stage growth regressions for each stock and age group of Oncorhynchus tshawytscha during the past three to four
decades that were statistically significant (P < 0·05). Dependent variables were total scale growth during each life stage, and independent variables
were either peak or total (FWPL on FW1 only) scale growth during the previous life stage. The mean percentage of annual regressions, including
non-significant regressions, having a positive slope and the mean and maximum annual correlation coefficient (r 2 ) for each life stage are shown
G R O W T H O F O N C O R H Y N C H U S T S H AW Y T S C H A
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G . T. R U G G E R O N E E T A L .
0·3
1·6
r2 = 0·01
r2 = 0·36
SW1 (mm)
FWPL (mm)
1·4
0·2
0·1
1·2
1·0
0·8
0·0
0·12
0·16
0·20
0·24
0·28
0·32
0·6
0·04
0·36
0·06
FW1 (mm)
1·3
1·4
r2 = 0·45
SW3 (mm)
SW2 (mm)
0·12
0·14
r2 = 0·38
1·2
0·9
0·7
1·0
0·8
0·6
0·5
0·20
0·24
0·28
0·32
0.36
0·4
0·15
0.40
0·20
SW1 (mm)
0·25
0·30
0·35
SW2 (mm)
0·20
r2 = 0·27
0·18
SWPL (mm)
1·0
SW4 (mm)
0·10
FW1 (mm)
1·1
1·2
0·08
0·8
0·6
r2 = 0·69
0·16
0·14
0·12
0·10
0·08
0·4
0·15
0·20
0·25
0·30
SW3 (mm)
0·35
0·40
0·06
0·15
0·20
0·25
0·30
0·35
0·40
SW4 (mm)
Fig. 1. Regressions of scale growth during each life stage with growth during the previous year (FWPL,
scale growth during transition from fresh water to the ocean; FW1, first year in fresh water; SW1,
first year at sea; SW2, second year at sea; SW3, third year at sea; SW4, fourth year at sea; SWPL,
homeward migration). Regressions are based on individual age 1·4 Oncorhynchus tshawytscha returning
to the Yukon River, Alaska, in 1991. This cohort exhibited relatively high growth correlations. The
independent variables were peak scale growth during each life stage (except FWPL regressed with
annual scale growth during the first year in fresh water, FW1). Regressions were statistically significant
(P < 0·001) except for FWPL (P > 0·05).
all correlations were positive. Likewise, 64, 60 and 90% of the correlations involving
the dependent variables SW3, SW4 and SWPL had a positive slope and were statistically significant with previous year’s growth (Table I). The percentage of positive
correlations ranged from 84 to 99% of the total. On average, 15 to 40% of the variability in marine scale growth was explained by the previous year’s growth, depending on life stage. For some cohorts, previous growth explained up to 48 to 81% of the
variability in marine growth, depending on life stage. The strength of the relationships
tended to be greater for age 1·4 fish rather than age 1·3 fish during each life stage.
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In contrast, O. tshawytscha scale growth during FWPL was typically not related to
growth during the previous year in fresh water. Only 9% of the 131 regressions were
statistically significant, including both positive and negative relationships (Table I).
The few significant correlations could be due to chance.
G R O W T H R E L AT I O N S H I P S A C R O S S Y E A R S
When comparing across all years, the mean slope of the annual regressions of
growth on the previous year’s growth was statistically greater than zero for each
stock, age group and life stage of O. tshawytscha (P < 0·001), except during FWPL
(Fig. 2), indicating that growth was related to previous year’s growth throughout
most life stages during the study period. Mean slope of the regressions of FWPL
on freshwater growth during the previous year was significantly <0 for three of
the four tests (Fig. 2), indicating a unique relationship involving FWPL and FW1
growth. Annual regression slopes of most life stages did not vary with time or with
ocean climate shifts observed in 1977, 1989 and 1997 (Kruse, 1998; Hare & Mantua,
2000), except the magnitude of slopes for FWPL (r = 0·66) and SW1 (r = 0·42)
were positively correlated with time (P < 0·05).
G R O W T H R E L AT I O N S H I P S R E L AT I V E T O M E A N S C A L E
G ROW T H O F T H E Y E A R C L A S S
The relationship of O. tshawytscha scale growth with previous year’s growth
was stronger when previous year’s growth of the population was relatively low,
especially during early marine life. Slope of the annual regressions of scale growth
on the previous year’s growth was negatively correlated with mean scale growth
of the year class during the previous year for all life stages except those during
late marine life, i.e. SW4 and SWPL (Fig. 3). Autocorrelation was non-significant
(P > 0·05) when comparing the SW1 and SW2 slopes with mean growth during the
previous year. The potential effect of autocorrelation, based on inconclusive statistical
tests, on the FWPL and SW3 relationships was removed by inclusion of the slope
from the previous year class (P < 0·05). In these multiple regression models, the
negative relationship between mean SW2 growth and SW3 slope was significant
(partial P < 0·05), whereas the negative relationship between mean growth in fresh
water (FW1) and FWPL slope was not significant (P > 0·05).
A D U LT LETF A N D S C A L E G R O W T H
Regressions of individual adult O. tshawytscha LETF and scale measurements
(SW2 to SWPL) were statistically significant for 97% of the annual regressions since
1964 (P < 0·05). On average, 32% of the variability in adult LETF was explained
by cumulative scale growth during the second year at sea to the homeward migration
period (SWPL first three circuli). In some years, adult LETF was highly correlated
with scale growth (Fig. 4).
Adult LETF was significantly, albeit weakly, related to growth during the freshwater period. Adult LETF of individual age 1·3 and 1·4 Yukon and Kuskokwim fish was
positively correlated with total growth in FW1 for 63 and 64% of the annual tests,
respectively. These percentages include statistically significant and non-significant
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G . T. R U G G E R O N E E T A L .
Y 1·4
SWPL on
SW3 or SW4
Y 1·3
K 1·4
K 1·3
Older
Y 1·4
SW4 on SW3
Y 1·3
K 1·4
K 1·3
Y 1·4
SW3 on SW2
Y 1·3
K 1·4
Age
K 1·3
Y 1·4
SW2 on SW1
Y 1·3
K 1·4
K 1·3
Younger
Y 1·4
SW1 on FW1
Y 1·3
K 1·4
K 1·3
FWPL on FW1
−2·5
−1·5
Y 1·4
P < 0·05
Y 1·3
P < 0·01
K 1·4
P > 0·05
K 1·3
P < 0·05
−0·5
0·5
1·5
Scale growth slope (mm mm–1)
2·5
3·5
4·5
Fig. 2. Mean rate of scale growth change in relation to previous year’s growth during each life stage and age
class (1·3 and 1·4) of Yukon River (Y) and Kuskokwim River (K) Oncorhynchus tshawytscha. Rate of
scale growth change is mean ± 95% CI slope calculated from annual regressions of scale growth on
previous year’s growth (see Fig. 1). Slope values were statistically significant (P < 0·001) except as
noted.
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SW2 slope (mm mm–1)
2·0
1·5
r2 = 0·13
1·0
1·5
r2 = 0·11
1·0
0·5
0·0
−0·5
−1·0
−1·5
−1·5 −1·0 −0·5 0·0 0·5
SW1 (Z )
1·0
1·5
2·0
SW1 slope (mm mm–1)
1·5
1·0
0·5
0·0
−0·5
−1·0
−1·5
−2·0
−2·5
−3·0
−1·5 −1·0 −0·5 0·0 0·5
FW1 (Z )
2·0
SW3 slope (mm mm–1)
FWPL slope (mm mm–1)
G R O W T H O F O N C O R H Y N C H U S T S H AW Y T S C H A
2·0
1·5
r2 = 0·22
1·0
0·5
0·0
−0·5
−1·0
−1·5
−1·5 −1·0 −0·5 0·0 0·5
FW1 (Z )
1·0
1 ·5
2·0
3 ·0
r2 = 0·16
2 ·5
2 ·0
1 ·5
1 ·0
0 ·5
0·0
−0·5
−1·0
−1·5
−2·5 −2·0 −1·5 −1·0 −0·5 0·0 0·5 1·0 1·5 2·0
SW2 (Z )
Fig. 3. Regressions of normalized annual scale growth slopes of Yukon River Oncorhynchus tshawytscha on
normalized mean scale growth (Z) of the year class during the previous year (see Fig. 1). Scale slopes
were calculated from regressions of scale growth of individual O. tshawytscha on the previous year’s
growth. The FWPL and SW3 plots were based on partial residuals of multiple regressions that included
the slope of the previous year class to remove autocorrelation. In these cases, r 2 is based on the partial
correlation coefficient. All correlations were statistically significant (P < 0·05) except the FWPL slope
(partial P > 0·05). Regressions involving SW4 and SWPL life stages were non-significant and are not
shown (P > 0·05).
correlations. χ 2 analysis indicated that the frequency of positive v. negative correlations was not random among Yukon River (χ 2 , n = 73, P < 0·05), Kuskokwim River
(χ 2 , n = 58, P < 0·05) and both stocks combined (χ 2 , n = 131, P < 0·05). Likewise, annual correlation coefficients (r) were statistically >0 for both Yukon (t-test,
mean r = 0·07, d.f. = 76, P = 0·001) and Kuskokwim (mean r = 0·07, d.f. = 59,
P < 0·01) O. tshawytscha.
DISCUSSION
Analysis of Yukon and Kuskokwim O. tshawytscha scale growth within each year
during the past four decades indicated that annual growth of individuals was related
to growth during the previous year. This relationship was maintained between fresh
water and early marine life stages and among each life stage in the ocean. The degree
of growth relationship, as indicated by the magnitude of the regression slope, was
greater when mean growth of the year class was relatively low during the previous
year. Adult LETF of O. tshawytscha was most closely correlated with cumulative
scale growth after the first year at sea. Adult LETF , however, was also weakly related
to growth that occurred during freshwater residence 4 to 5 years earlier.
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G . T. R U G G E R O N E E T A L .
1100
(a)
1000
900
800
700
600
LETF (mm)
500
1·5
1100
2·0
2·5
3·0
3·5
4·0
2·0
2·5
3·0
Scale radius (mm)
3·5
4·0
(b)
1000
900
800
700
600
500
1·5
Fig. 4. Examples of the relationship between adult length (eye to tail fork, LETF ) of individual Yukon River
Oncorhynchus tshawytscha and scale radius during (a) 1980 and (b) 1986. Scale radius is the sum of the
second, third and fourth years of marine growth (SW2, SW3 and SW4) and the first three circuli during
the home migration period (SWPL). Age 1·3 and 1·4 fish were included in the regressions. The curves
were fitted by (a) y = 142·2x + 454(r 2 = 0·73) and (b) y = 145·6x + 396(r 2 = 0·73).
The relationship of individual O. tshawytscha growth to the previous year’s growth
may relate to their piscivorous feeding habits and their tendency to select relatively large prey including squid while foraging in the ocean (Major et al ., 1978;
Healey, 1991; Farley et al ., 2009). Greater growth may beget greater growth because
larger Oncorhynchus spp. can consume larger prey (Ruggerone, 1992; Juanes, 1994),
thereby enhancing overall availability and energy content of prey for larger
Oncorhynchus spp. (Salminen, 1997; Aydin et al ., 2005). Somatic growth may be
especially important for O. tshawytscha because they mature at a large size relative to
other species of Oncorhynchus spp. Rapid growth and large body size may enhance
survival (Healey, 1982) and lead to greater fecundity at a given age (Quinn, 2005).
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Investigations to determine whether Oncorhynchus spp. smolt size has an effect
on post-smolt growth have led to inconsistent findings. Studies on S. salar indicated
growth was compensatory or negatively correlated with smolt size (Skilbrei, 1989;
Nicieza & Braña, 1993; Einum et al ., 2002), independent of smolt size (Friedland
et al ., 2006) or positively correlated with smolt size (Salminen, 1997). Friedland
et al . (2006) also reported that growth at sea of S. salar during summer was positively correlated with their growth during spring. Post-smolt growth of steelhead
Oncorhynchus mykiss (Walbaum) was positively correlated with smolt size, whereas
post-smolt growth of coho salmon Oncorhynchus kisutch (Walbaum) was either negatively correlated or not correlated with smolt size (Johnsson et al ., 1997; Snover
et al ., 2005). In Bristol Bay, Alaska, scale growth of individual O. nerka during the second year at sea was not correlated with growth during the first year
(G. T. Ruggerone, unpubl. data). The relationship between growth and size may
depend, in part, on whether the fish is consuming relatively large mobile prey versus
smaller less mobile prey.
The degree of growth enhancement (magnitude of positive regression slope) among
O. tshawytscha varied from year to year. It was greatest when the mean growth of
the year class was relatively low indicating the tendency for fish growth to increase
even more when previous growth was relatively low. This form of compensatory
growth, or ‘catch-up’ growth, might be related to both physiological and ecological
factors. The O. tshawytscha scales used in this study were from fish that survived 3
or 4 years at sea. Conceivably, mortality may have been relatively high for slower
growing individuals, leading to the observed rapid growth increase when body size
of the population was relatively small. This pattern was also observed among Bristol
Bay O. nerka in which mean growth of the population during the second year at sea
was inversely correlated with early marine growth (Ruggerone et al ., 2005).
Oncorhynchus tshawytscha scale growth during the FWPL tended to be negatively correlated with growth in fresh water during the previous year, although the
relationships were weak. This relationship probably reflects a behavioural response of
O. tshawytscha rather than compensatory growth. Smaller, slow growing
Oncorhynchus spp. tend to delay the date of smoltification, leading to greater time
and growth during the spring transition period from fresh to marine waters (Burgner,
1962). This transition growth was reflected in the FWPL measurements.
Adult LETF of O. tshawytscha was correlated with scale growth, but variability
explained by scale measurements was only 32%, on average. The low LETF and
scale correlation at the adult stage compared with the juvenile and immature stages
(Fukuwaka & Kaeriyama, 1997; Fisher & Pearcy, 2005) probably reflects a change in
the length and scale relationship caused by rapid growth of maturing Oncorhynchus
spp., as they migrate toward their natal river (Brett, 1995) followed by reduced feeding and resorption of the scale with the onset of maturation (Bilton, 1985; Price &
Schreck, 2003). Still, the adult LETF and scale relationship provides evidence that
the observed scale growth relationships between adjacent life stages were related to
body growth rather than an artifact of scale growth.
Evidence suggests that climate shifts and associated oceanic conditions can influence Oncorhynchus spp. abundance through their effects on growth during early
marine life (Peyronnet et al ., 2007; Ruggerone et al ., 2007). Abundance of western Alaska O. tshawytscha, including those in the Yukon and Kuskokwim Rivers,
increased after the 1977 regime shift, then declined after the 1997 to 1998 El Niño
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G . T. R U G G E R O N E E T A L .
(Kruse, 1998). The present study did not identify distinct and immediate shifts in
O. tshawytscha growth in relation to climate shifts, possibly because O. tshawytscha
feed in the ocean at a relatively high trophic level that involves complex species
interactions (Hunt et al ., 2002) that may delay a response to climate shifts. Furthermore, the present study indicated that growth of O. tshawytscha was influenced, in
part, by growth during earlier life stages, suggesting that effects of climate shifts on
growth may be mediated by earlier growth.
The dependency of early marine growth and adult LETF of O. tshawytscha on
growth in fresh water has important implications for maintaining habitat quality in
fresh water. Oncorhynchus spp. habitat from California to the Pacific Northwest is
often degraded by human activities leading to depleted stocks and protection under
the United States Endangered Species Act (Yoshiyama et al ., 1998; Good et al .,
2005). Atmospheric warming is predicted to lead to amplification of precipitation
extremes affecting freshwater systems (Allen & Ingram, 2002). Predicted increases in
extreme precipitation events correlate with changes in sea surface temperature (Allan
& Soden, 2008) and by implication change in the ocean prey resource for salmonids.
Although O. tshawytscha may compensate for small size in fresh water, the present
study suggests that rapid growth during early life stages, including the freshwater
period, is important to subsequent growth and presumably survival throughout life.
Thus, growth in freshwater habitats may be especially important during periods of
low ocean productivity because large size at ocean entry may enable fish to consume
a wider spectrum of prey.
The manuscript was partially prepared under award NA06FP0387 from the National
Oceanic and Atmospheric Administration, U.S. Department of Commerce, administered by
the Alaska Department of Fish and Game. This investigation was funded by the Arctic-YukonKuskokwim Sustainable Salmon Initiative and the U.S. Geological Survey’s Global Change
Initiative Program. We thank ADFG biologists, especially D. Molyneaux, who provided access
to numerous reports. We also appreciate efforts to gather, measure and catalogue scales by
D. Folletti, M. Lovejoy, A. Norman, D. Oxman, W. Rosky and W. Whelan. Constructive
comments on the manuscript were provided by S. Goodman, P. Hagen, E. Ivaska and two
anonymous reviewers. Use of any trade names or products is for descriptive purposes only
and does not imply endorsement of the U.S. Government. The statements, findings, conclusions and recommendations are those of the authors and do not necessarily reflect the views
of the National Oceanic and Atmospheric Administration, the U.S. Department of Commerce,
the U.S. Department of Interior or the Alaska Department of Fish and Game.
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