Ionoregulatory changes in different populations of maturing sockeye salmon Oncorhynchus nerka during ocean and river migration
1 Ecosystem Science and Management Program, University of Northern British
Columbia, Prince George, BC, V2N 4Z9, Canada
2 Fisheries and Oceans Canada, Science Branch, Pacific Region, Cooperative
Resource Management Institute, School of Resource and Environmental
Management, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada
3 Department of Zoology, University of British Columbia, Vancouver, BC, V6T
1Z4, Canada
4 Centre for Applied Conservation Research, Department of Forest Sciences,
University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
5 Faculty of Agricultural Sciences, University of British Columbia,
Vancouver, BC, V6T 1Z4, Canada
* Author for correspondence (e-mail: shrimptm{at}unbc.ca)
Accepted 5 September 2005
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Summary |
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Key words: sockeye salmon, Oncorhynchus nerka, ionoregulation, migration, salinity, spawning
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Introduction |
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The elevated gill Na+,K+-ATPase activity limits ionic
perturbation in plasma of fish following movement into seawater. Fish
transferred to seawater that are not prepared for the increased salinity
showed large perturbations in plasma ions, decreased survival
(Shrimpton et al., 1994) and
reduced swimming performance (Brauner et
al., 1992
). While similar preparatory physiological changes are
expected to occur in preparation for maturing adult salmon returning to
freshwater, their nature and their consequences on plasma osmolality and ion
levels are unknown. Whatever these changes are, they are unlikely to exactly
mirror the parr-smolt transformation. Juvenile salmon that are prevented from
migrating into the ocean survive in freshwater
(Shrimpton et al., 2000
); in
contrast, there is evidence that maturing adult salmon cannot remain in
seawater, but must move into freshwater. Hirano et al.
(1978
) showed that maturing
chum salmon O. keta did not survive transfer from freshwater into
full strength seawater, and the physiological changes in ionoregulatory
ability that accompany maturation appear to be irreversible.
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For this analysis, we focussed our sampling efforts on four geographically
isolated spawning aggregates, each comprising multiple spawning populations of
sockeye salmon: Harrison, Late Shuswap, Chilko and Quesnel. Most populations
of sockeye that spawn in the Fraser River watershed (Chilko and Quesnel) enter
the river within a week of arriving at the mouth of the estuary. In contrast,
late-run sockeye salmon (Harrison and Late Shuswap), named for their late
summer arrival, normally congregate in the Fraser River estuary for 3-6 weeks
prior to entering freshwater and initiating their upriver migration to natal
spawning grounds (Cooke et al.,
2004). The stocks we selected also varied in their migration
distances in the freshwater of the Fraser River watershed, ranging from less
than 120 km (Harrison) to over 700 km (Quesnel).
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Materials and methods |
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During their upstream migration, sockeye were caught in the lower Fraser River at Cottonwood (C, 11 km), which is estuarine and at Whonnock (W, 50 km), which is beyond the saltwater intrusion. Lower Fraser sockeye of the Harrison stock were sampled on the spawning grounds in Weaver Creek (H, 117 km). Mid-Fraser sockeye of the Late Shuswap stock were sampled in the Thompson River near Ashcroft (T, 270 km), and on the spawning grounds in the Adams River (Sh, 484 km). Two stocks of Upper Fraser sockeye were sampled, Chilko and Quesnel. Chilko stock was sampled sampled at Hells Gate (HG, 200 km) and on the spawning grounds in the Chilko River (Ch, 562 km). Quesnel stock was sampled at Hells Gate, near Churn Creek on the Fraser River (Cc, 440 km) and on the spawning grounds in the Horsefly River (Q, 748 km).
Fish were collected using a variety of methods specific to each location. The following methods were employed: trolling off the west coast of the Queen Charlotte Islands and in Georgia Strait; purse seine off the coast of Vancouver Island near Port Renfrew and in Johnstone Strait; gill net near the mouth of the Fraser River at Cottonwood and at Whonnock; long dip nets at Hells Gate; beach seines at Ashcroft and Churn Creek; beach seines to capture sockeye arriving at the spawning grounds; and small dip nets to capture actively spawning fish. All groups were sampled on the spawning grounds at least twice in each year and fish were assessed for stage of maturation.
There is considerable knowledge of run timing for each of the stocks
sampled; therefore, sampling was timed to intercept the stocks of interest.
Stock identification for each fish sampled was determined by variation in
genetic markers, as outlined by Beacham et al.
(1995). Genetic determination,
however, meant that stock identification was determined a posteriori.
As a result, sample size varied considerably for each stock examined, among
locations, and also between years. The fish caught during migration were
grouped based on spawning aggregate and represent multiple spawning
populations within a watershed. In contrast, the fish sampled on the spawning
grounds were from a single spawning population in that aggregate. In all
cases, however, the single spawning populations chosen were the largest
spawning population for that aggregate in both sampling years.
Tissue sampling
In most cases these fish were sampled as part of normal test fishery or
stock assessment operations and specific treatment of the fish was dependant
on the gear type. Every effort was made to minimize the time from capture to
tissue sampling. In those cases involving seine nets, fish remained in the
ocean constrained by the seine net until they were individually dip-netted out
for sampling. Fish caught using a troll line or dip net were landed and
sampled within minutes. Where possible the soak time for gill nets was reduced
to less than 15 min and only fish that were still vigorous at capture were
sampled. Fish were killed with a single blow to the head and immediately
sampled for blood and gill tissue. 10 ml of blood was collected from the
caudal vasculature using a vacutainer syringe (1.5'', 21 gauge) for
assessing plasma chemistry, and the tips of 6-8 filaments from the first gill
arch were removed for analysis of Na+,K+-ATPase
activity. Gill tissue and centrifuged plasma samples were stored on dry ice
for several days before transfer to a -80°C freezer where they were held
until analysis. Fork length (FL, cm) was measured and an adipose fin
clip was removed for DNA stock identification.
Analysis of gill Na+,K+-ATPase activity
Gill Na+,K+-ATPase activity was measured according to
the microassay protocol of McCormick
(1993). Gill filaments were
homogenized in SEI buffer (150 mmol l-1 sucrose, 10 mmol
l-1 Na2EDTA, 50 mmol l-1 imidazole, pH 7.3)
containing 0.1% sodium deoxycholate. Following centrifugation (3000
g for 0.5 min), the supernatant was used to determine
Na+,K+-ATPase activity by linking ATP hydrolysis to the
oxidation of nicotinamide adenine dinucleotide (NADH), measured at 340 nm for
10 min at 25°C, in the presence and absence of 0.5 mmol l-1
ouabain. Protein content in the gill homogenate was measured using a
bicinchoninic acid (BCA) protein assay (Pierce, Rockford, IL, USA). Specific
activities were expressed as mol ADP mg-1 protein
h-1.
Determination of plasma osmolality and chloride
Plasma samples were thawed, vortexed and centrifuged for 5 min immediately
before analysis. Osmolality was measured in duplicate on 10 µl samples
using a model 5500 Wescor Vapour Pressure meter (Logan, UT, USA). Plasma
chloride concentrations were measured in duplicate using a model 4425000 Haake
Buchler digital chloridometer (Kansas City, MO, USA); values were checked
against a chloride standard (100 mmol l-1 NaCl) before and after
approximately every 10 duplicates.
Gill Na+,K+-ATPase 1a and
1b isoform expression
An analysis of Na+,K+-ATPase -subunit isoforms
expression, as described by Richards et al.
(2003
), was performed on a
subset of gill samples from Upper Fraser stocks caught (i) in the Georgia
Strait, (ii) at Whonnock, (iii) during migration at Hell's Gate (river 200
km), (iv) while the fish were holding on the spawning grounds before spawning
(green), and (v) fully mature fish (spawners). Fish captured on the spawning
grounds were sampled from the Horsefly River, Quesnel Watershed.
Briefly, total RNA was extracted from gill tissue using TriPure Isolation
Reagent (Roche Diagnostics, Montreal, QC, Canada) and quantified
spectrophotometrically. First-strand cDNA was synthesized from 5 µg of
total RNA using oligo(dT15) primer and RevertAidTM H-Minus
M-MuLV reverse transcripase (MBI Fermentas Inc., Burlington, ON, Canada). The
expression of Na+,K+-ATPase -1a and -
1b
isoforms was estimated using quantitative real-time PCR (qRT-PCR; ABI Prism
7000 sequence analysis system; Applied Biosystems Inc., Foster City, CA, USA).
PCR reactions contained 1 µl of cDNA, 4 pmoles of each isoform-specific
primer and Universal SYBR green master mix (Applied Biosystems Inc.) in a
total volume of 20 µl. Primers were designed from trout
Na+,K+-ATPase
1a (GenBank Accession No.
AY319391), Na+,K+-ATPase
1b (Accession No.
AY319390) and elongation factor 1
(Accession No. AF498320). Primer
sequences were as follows: Na+,K+-ATPase -
1a
forward, 5' GGC CGG CGA GTC CAA T 3';
Na+,K+-ATPase -
1a reverse, 5' GAG CAG CTG
TCC AGG ATC CT 3'; Na+,K+-ATPase -
1b
forward, 5' CTG CTA CAT CTC AAC CAA CAA CAT T 3';
Na+,K+-ATPase -
1b reverse, 5' CAG CAT CAC
AGT GTT CAT TGG AT 3'; and elongation factor-1
forward, 5'
GAG ACC CAT TGA AAA GTT CGA GAA G 3'; elongation factor-1
reverse, 5' GCA CCC AGG CAT ACT TGA AAG 3'. All qRT-PCR reactions
were performed as follows: 2 min at 50°C, 10 min at 95°C, followed by
40 cycles of 95°C for 15 s and 60°C for 1 min. Melt curve analysis was
performed following each reaction to confirm the presence of only a single
product of the reaction. The melting temperature of the amplicon obtained with
cDNA from sockeye salmon was identical to that of the trout amplicon, strongly
indicating that the primers developed for trout also amplify the expected
target in salmon. Negative control reactions were performed for a selection of
samples using RNA that had not been reverse transcribed to control for the
possible presence of genomic contamination. Genomic DNA contamination never
constituted more than 1:4096 starting copies for any gene examined. One
randomly selected sample was used to develop a standard curve relating
threshold cycle to cDNA amount for each primer set and all results are
expressed relative to these standard curves. mRNA amounts are normalized
relative to elongation factor 1
and expressed relative to the gill
samples collected from fish caught in Georgia Strait. Freshwater migration did
not affect the expression of elongation factor 1
when expressed
relative to total mRNA reverse transcribed; therefore, any changes in gene
expression are due to changes in Na+,K+-ATPase and not
due to changes in the control.
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Results |
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Ionoregulatory changes in seawater
Fish were sampled in the sea at four locations, one 850 km, a second
300 km, a third 200 km, and a fourth <25 km from the mouth of the Fraser
River. Depending on stock, there were significant decreases in gill
Na+,K+-ATPase activity, plasma osmolality and chloride
levels as the sockeye salmon moved between these three saltwater locations
(Figs 2,
3,
4,
5); enzyme activity declined
significantly for Shuswap sockeye between the Queen Charlotte Islands and
Georgia Strait. The pattern was similar for the other stocks, but small sample
size and no Quesnel and Chilko sockeye caught in Georgia Strait for 2003
limited statistical power and sample comparisons. Plasma osmolality and
[chloride] values declined significantly for Shuswap and Harrison stocks,
respectively, between Queen Charlotte Island and Georgia Strait; but not
Chilko and Quesnel. These data provide evidence for pre-freshwater
ionoregulatory preparations occurring before fish encountered and entered the
Fraser River.
Ionoregulatory changes with freshwater entry
The Cottonwood sample site (river, 11 km) is estuarine. For the Shuswap and
Harrison stocks intercepted at Cottonwood, both plasma osmolality and chloride
had declined significantly compared with Strait of Georgia samples (Figs
2 and
3).
At the Whonnock sample site (river, 50 km) fish are in freshwater. Here gill Na+,K+-ATPase activity had significantly declined in three of the four stocks compared with the Cottonwood and Georgia Strait samples. Two-way ANOVA indicated that there were no significant differences among stocks (P=0.097) or between years (P=0.378) for gill Na+,K+-ATPase activity. Except for plasma osmolality in the Shuswap stock, which showed a significant increase, there was no significant change in plasma osmolality and [chloride] between the Cottonwood and Whonnock samples (Fig. 3). Gill Na+,K+-ATPase activity differed significantly between Georgia Strait and Whonnock for Shuswap (2002) and Harrison and Shuswap stocks in 2003.
Ionoregulatory changes during freshwater migration
For all stocks examined, gill Na+,K+-ATPase activity,
as well as plasma osmolality and [chloride] values, of fish arriving at the
spawning grounds were significantly lower than values from the Georgia Strait.
Thus, from the Queen Charlotte Islands to the spawning areas, there was a
fairly consistent decline in gill Na+,K+-ATPase
activity, with the exception of values from fish captured shortly after entry
into freshwater.
Because the different fish stocks migrated different distances in freshwater, it was possible to examine the effects of freshwater migration time and distance on the ionoregulatory changes. The loss of Na+,K+-ATPase activity per unit distance was highest for the fish stock that migrated the shortest distance (Harrison stock), and least for the fish stock migrating the longer distances (over 750 km in freshwater for the Quesnel stock; Figs 2, 3, 4, 5). Regardless, all stocks arrived at the spawning grounds with levels of gill Na+,K+-ATPase activity that were very low (approximately 1 µmol ADP mg-1 protein h-1). There were significant differences among the stocks and between years (Fig. 6A); however, there was no apparent trend and Na+,K+-ATPase activities of fish holding on the spawning grounds were not related to migration distance. Instead, the decline in enzyme activity appeared to be dependent on time in freshwater. This is evident when the absolute change in enzyme activity is plotted against the estimated time in freshwater for fish sampled at the spawning grounds (Fig. 6B). The exception to this trend was the Harrison, 2003 data, but these data were limited in that only three green fish were sampled on the Weaver Creek spawning grounds in 2003.
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Discussion |
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Do sockeye salmon prepare for freshwater in advance of arrival at the estuary?
A decrease in gill Na+,K+-ATPase activity indicates
that seawater ionoregulatory capacity of migrating sockeye declines before the
fish enter freshwater. The changes in enzyme activity that occur in seawater
are probably preparatory for movement into freshwater. Uchida et al.
(1997) also suggest that
physiological and histological changes in the gill of chum salmon are
preparatory for upstream migration. These authors showed that gill
Na+,K+-ATPase continued to decrease in maturing chum
captured before river entry and held in seawater; chum held in seawater showed
elevated plasma osmolality and increased mortality. Although physiological
changes in seawater appear adaptive for river entry, there is also evidence
that hypo-osmoregulatory function is directly impaired in sexually maturing
adult salmon (Clarke and Hirano,
1995
). Changes observed in seawater salmon may be associated with
elevated reproductive hormones. Endocrine factors associated with maturation
impair ionoregulatory ability in seawater
(Lundqvist et al., 1989
;
Madsen and Korsgaard, 1989
).
In a parallel study, an increase in reproductive hormones for Fraser River
sockeye tagged in Johnstone Strait was found before entry into freshwater (S.
J. Cooke, S. G. Hinch, G. T. Crossin, D. A. Patterson, K. K. English, M. C.
Healey, S. Macdonald, J. M. Shrimpton, J. L. Young, A. Lister, G. Van Der
Kraak and A. P. Farrell, manuscript submitted for publication). These authors,
however, found no significant differences in reproductive hormones among the
populations of sockeye, suggesting that differences between populations are
not a function of reproductive state.
Despite the decline observed in gill Na+,K+-ATPase
activity, changes in osmolality and chloride values for seawater fish do not
suggest an impairment in ionoregulatory performance. Plasma osmolality and
chloride did not differ among seawater sampling sites for the Chilko and
Quesnel stocks (Figs 4 and
5). There was a parallel
decline in plasma osmolytes with the changes in gill
Na+,K+-ATPase activity for the Shuswap sockeye migrating
from the Queen Charlotte Islands (850 km from the Fraser River mouth) to
Johnstone Strait (210 km from the Fraser River mouth)
(Fig. 3). Lower enzyme
activities would be expected to correspond with an increase in plasma
osmolality for fish maintained in seawater, as has been demonstrated in
juvenile salmon during the parr-smolt transformation
(McCormick and Saunders, 1987;
Shrimpton et al., 1994
).
Waters for these two areas are hyperosmotic to plasma levels, so it is
difficult to interpret the declines in chloride and osmolality. Harrison
sockeye are the only population to show a significant change in plasma
chloride for seawater fish; there is a significant decline in values for fish
caught in Johnson Strait compared to Georgia Strait
(Fig. 2). There is considerable
influence of the Fraser River within this region and the declines in
[chloride] may reflect lower environmental salinities (Thompson, 1981).
Our sampling of fish in seawater for 2003 was much more extensive than in 2002, but we sampled fish in Georgia Strait in both years. The troll fishery in Georgia Strait is selective for late-run fish and few Quesnel and no Chilko fish were caught. Values in Georgia Strait were similar for both years, with the exception of gill Na+,K+-ATPase activity for Harrison fish (Fig. 2). The difference between years may reflect differences in holding time for fish within Georgia Strait. S. J. Cooke, S. G. Hinch, G. T. Crossin, D. A. Patterson, K. K. English, M. C. Healey, S. Macdonald, J. M. Shrimpton, J. L. Young, A. Lister, G. Van Der Kraak and A. P. Farrell (manuscript submitted for publication), however, examined Fraser River late-run sockeye that showed variable delay in migration and found no difference in gill Na+,K+-ATPase activities with delay time in Georgia Strait.
Are freshwater ionoregulatory changes complete before fish leave the ocean?
The first freshwater sampling point was at Cottonwood, which is 11 km from
the mouth of the Fraser River, yet there are still saltwater intrusions at
this location. As a consequence, fish sampled from Cottonwood may still have
access to increased salinity, but the decrease in plasma osmolality and
[chloride] in the four populations examined (Figs
2,
3,
4,
5) suggest that fish sampled
were in full freshwater. The switch from seawater ionoregulation to chloride
uptake for fish directly transferred from seawater to freshwater has been
shown to take approximately 4 days (Battram
and Eddy, 1990). Perturbations in plasma osmolality and
[chloride], although in the opposite direction, are similar in magnitude to
those seen in smolting (Blackburn and Clarke, 1987); suggesting ionoregulatory
changes that are preparatory for freshwater entry have already occured in
seawater. Gill Na+,K+-ATPase activity showed little
change between the Georgia Strait and Cottonwood samples (Figs
2 and
3); however,
Na+,K+-ATPase
1a mRNA expression indicates that
physiological changes continue after movement into freshwater
(Fig. 7).
In the 2003 fish sampled, we found a signficant decline in gill
Na+,K+-ATPase activity between fish sampled at
Cottonwood and Whonnock for three of the populations. We do not know the
actual temporal difference for fish caught between the two locations, but fish
may travel the 40 km in less than 24 h
(English et al., 2004).
Modifications of enzyme activity have adaptive significance and occur when
euryhaline teleosts move between changing salinities
(McCormick, 1995
). The
response normally takes several days, suggesting transcriptional regulation.
Short-term regulation of this enzyme, however, has been demonstrated in
killifish transferred between salinities
(Mancera and McCormick, 2000
).
Elevated cyclic AMP levels in brown trout have also been found to decrease
maximal Na+,K+-ATPase activity in gills of brown trout
(Tipsmark and Madsen, 2001
).
The authors suggest that phosphorylation may regulate
Na+,K+-ATPase activity in teleosts. The significant
differences in gill Na+,K+-ATPase activity between fish
sampled at Cottonwood and Whonnock could also be due to rapid modulation of
the enzyme (Tipsmark and Madsen,
2001
).
Isoform switching between two Na+,K+-ATPase
-subunit isoforms (
1a and
1b) during salinity transfer is
thought to be an important component in changing the salmonid gill from an
ion-absorbing epithelium in freshwater to an ion-secreting epithelium in
seawater (Richards et al.,
2003
). Consistent with this notion, the expression of
Na+,K+-ATPase
1a increased in wild sockeye salmon
following movement from seawater in Georgia Strait to freshwater in Whonnock
and is associated with a decrease in Na+,K+-ATPase
activity (Fig. 7). These
results suggest that the gill ionoregulatory changes necessary for freshwater
acclimation, at least in terms of mRNA expression and enzyme activity, are not
complete before the fish enters freshwater
(Fig. 7). The lack of change in
Na+,K+-ATPase
1b mRNA in the gills of wild
sockeye salmon following movement from seawater to freshwater are consistent
with the results of Richards et al.
(2003
), who found that
expression of Na+,K+-ATPase
1b increases
transiently following seawater transfer, and returns to the levels observed in
freshwater acclimated individuals within 10 days post-transfer. Overall,
enhanced expression of Na+,K+-ATPase
1a during
freshwater migration is consistent with the isoform switching proposed by
Richards et al. (2003
).
Concurrent with the changes in enzyme activity at Whonnock is a rebound in
plasma osmolality and [chloride]. Based on changes in plasma parameters and
gill Na+,K+-ATPase activity, the chloride uptake is not
likely to have achieved freshwater values
(Battram and Eddy, 1990), but
may be adjusted as the fish move upriver.
Are maturing sockeye in an ionoregulatory steady state during migration?
Gill Na+,K+-ATPase activity, plasma osmolality and
[chloride] declined with the time and distance covered while migrating
upriver. Migrating adult sockeye, therefore, are not in an ionoregulatory
steady state. Generally the lowest values of gill
Na+,K+-ATPase were observed for fish approaching or
first arriving on the spawning grounds. For all stocks, enzyme activities and
plasma osmolalities had significantly declined from seawater values (Figs
2,
3,
4,
5). The factors measured in the
present study of freshwater migrating fish suggest continued physiological
changes throughout migration. Physiological changes associated with migration
distance have previously been observed in smolting salmonids with distance
moved downstream (Muir et al.,
1994). Therefore, the decline in gill
Na+,K+-ATPase activity as sockeye migrate to spawning
areas may reflect physiological adjustments that continue to occur as the fish
migrate. The absolute changes in gill Na+,K+-ATPase
activity were related to estimated time in freshwater. English et al.
(2004
) used radiotelemetry to
determine migration rates in maturing late-run sockeye salmon in freshwater.
They found that sockeye after entering freshwater migrated at a fairly
consistent rate and tagged sockeye maintained their chronological order during
migration as assessed by detection at monitoring stations along the Fraser
River. The Harrison sockeye, however, hold in freshwater for a relatively
longer period given their short river migration distance (117 km).
Does final maturation affect ionoregulatory status?
Plasma osmolality and chloride levels measured in spawning fish suggest
that they are no longer able to maintain adequate homeostasis in freshwater.
Sockeye are semelparous and die shortly after spawning. The physiological
perturbation that the fish experience may be of little consequence, however;
gill Na+,K+-ATPase activities in spawners are generally
higher than for fish holding on the spawning grounds
(Fig. 6). The higher gill
Na+,K+-ATPase activities observed in spawners suggests
that the fish may be attempting to compensate for the osmotic
perturbation.
Spawning sockeye salmon are characterized by a marked increase in gill
Na+,K+-ATPase 1b mRNA compared to individuals
holding on the spawning grounds. Previous work demonstrated a transient
increase in the expression of this isoform following transfer to seawater
(Richards et al., 2003
) and
these authors speculated that the expression of
Na+,K+-ATPase
1b might be under the regulation of
circulating glucocorticoid levels. No change in
Na+,K+-ATPase
1b expression was observed in
response to seawater to freshwater movement; however, large increases in
Na+,K+-ATPase
1b mRNA levels were observed in
spawning sockeye. Previous work has shown that circulating cortisol levels
increase during maturation (Donaldson and
Fagerlund, 1972
; Carruth et al., 2000) and the gene is possibly
responsive to the higher cortisol levels.
In conclusion, in the present study we found that ionoregulatory changes
preparatory for freshwater residence occur in adult sockeye salmon while they
are migrating in seawater. The entry into freshwater was accompanied by
further physiological adjustments. Fish from the four stocks caught at
Whonnock, the first sampling location that was fully freshwater, however, did
not differ in our measures of ionoregulatory performance. A large difference
in freshwater migration distance and time in freshwater before spawning
existed in the four stocks of sockeye examined. All stocks arrived on the
spawning grounds in similar physiological condition, as indicated by our
measurements and consistent with measures of energy partitioning reported by
Patterson et al. (2004) and
Crossin et al. (2004
).
Physiological changes observed in spawners suggest that sockeye attempt to
minimize the osmotic perturbation that is associated with final
maturation.
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Acknowledgments |
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References |
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