Effects of an advanced temperature cycle on smolt development and endocrinology indicate that temperature is not a zeitgeber for smolting in Atlantic salmon
1 USGS, Leetown Science Center, Conte Anadromous Fish Research Center,
Turners Falls, MA 01376, USA
2 Laboratory of Molecular Endocrinology, School of Fisheries, Kitasato
University, Sanriku, Iwate, Japan
3 Fish Endocrinology Laboratory, Department of Zoology, Göteborg
University, Göteborg, Sweden
Present address: Biology Program, University of Northern British Columbia,
Prince George, British Columbia, Canada, V2N 4Z9
* Author for correspondence (e-mail: stephen_mccormick{at}usgs.gov)
Accepted 8 August 2002
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Summary |
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Key words: temperature, photoperiod, smolting, Atlantic salmon, Salmo salar, zeitgeber, gill Na+,K+-ATPase, growth hormone, insulin-like growth factor I, thyroid hormone
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Introduction |
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The physiological changes that comprise smolting are under the control of
the neuroendocrine system. Growth hormone (GH) and cortisol interact to
increase salinity tolerance and the underlying physiological changes such as
gill Na+,K+-ATPase activity
(McCormick, 1995). Thyroid
hormones may interact with these hormones to control osmoregulatory changes,
but have a more direct role in morphological changes (such as silvering) and
the development of behavioral changes that occur during smolting
(Hutchison and Iwata, 1998
).
Although levels of cortisol and thyroid hormones can be influenced by
photoperiod, growth hormone is the most responsive to changes in daylength and
is strongly correlated with the capacity of photoperiod to alter the timing of
smolting (Bjornsson, 1997
). The
effect of temperature on endocrine changes during smolting has received less
attention. Recent work indicates that low temperature can limit the capacity
of photoperiod to advance smolting and that this is controlled by changes in
circulating hormones. However, it is unclear whether other aspects of the
impact of temperature on smolting, particularly its potential as a zeitgeber,
are subject to endocrine control.
The present study was undertaken to determine the impact of temperature on smolt development and the underlying endocrine control mechanisms. A particular aim was to determine whether temperature alone could act as a zeitgeber for smolting. Thus, in addition to keeping fish on a normal photoperiod cycle, fish were also kept on a short-day photoperiod regime to determine if temperature can affect smolting in the absence of any photoperiod cues. Further, under each photoperiod regime, fish were exposed to either an ambient temperature regime (low temperature in winter, increasing in spring), or an advanced temperature regime (same pattern as ambient, but advanced by six weeks). Changes in gill Na+,K+-ATPase activity were used to monitor physiological smolt development, and plasma GH, IGF-I, cortisol and thyroid hormones were measured in order to examine the underlying endocrine signaling pathways.
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Materials and methods |
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Food was withheld for 24 h prior to sampling, which occurred from 10.00-11.00 h Eastern Standard Time. Blood and gill samples were taken approximately every 2 weeks from January 5 through May 19 (N=10 per treatment). Fish were anesthetized with MS-222 (100 mg l-1, neutralized to pH 7.0), and fork length to the nearest mm and mass to the nearest 0.1 g were recorded. Blood was drawn from the caudal vein into a 1 ml ammonium heparinized syringe and centrifuged at 5000 g for 5 min at 4°C. Plasma was divided into portions and stored at -80°C. 4-6 gill filaments were severed above the septum, placed in 100 µl of ice-cold SEI buffer (150 mmol l-1 sucrose, 10 mmol l-1 EDTA, 50 mmol l-1 imidazole, pH 7.3) and frozen at -80°C within 30 min.
Measurement of gill Na+,K+-ATPase activity
Na+,K+-ATPase activity was determined with a kinetic
assay run in 96-well microplates at 25°C and read at a wavelength of 340
nm for 10 min (McCormick,
1993). Gill tissue was homogenized in 125 µl of SEID (SEI
buffer containing 0.1% deoxycholic acid) and centrifuged at 5000 g
for 30 s. 10 µl samples were run in two sets of duplicates, one set
containing assay mixture and the other assay mixture plus 0.5 mmol
l-1 ouabain. The resulting ouabain-sensitive ATPase activity
measurement is expressed as µmol ADP mg-1 protein
h-1. Protein concentrations were determined using bicinchoninic
acid (BCA) Protein Assay (Pierce, Rockford, Il, USA). Both assays were run on
a THERMOmax microplate reader using SOFTmax software (Molecular Devices, Menlo
Park, CA, USA).
Hormone immunoassays
Plasma cortisol levels were measured by a validated direct competitive
enzyme immunoassay as outlined by Carey and McCormick
(1998). The typical measuring
range was 1-400 ng ml-1, with a lower detection limit of 0.3 ng
ml-1. Using a pooled plasma sample, the mean intra-assay variation
was 5.5% (N=10) and the mean inter-assay variation was 8.8%
(N=10). Plasma growth hormone levels were measured by a
radioimmunoassay validated for Atlantic salmon
(Björnsson et al., 1988
).
The typical measuring range was 0.1-50 ng ml-1 with mean
intra-assay and inter-assay variations of 5.4% (N=9) and 3.9%
(N=9), respectively. Plasma IGF-I concentration was measured by
homologous radioimmunoassay, as described by Moriyama et al.
(1994
). The typical measuring
range was 1-250 ng ml-1, with a lower detection limit of 0.20 ng
ml-1. Using a pooled plasma sample, the mean intra-assay variation
was 7% (N=5) and the mean inter-assay variation was 6.5%
(N=5). Thyroxine (T4) and 3,5,3'-triiodo-L-thyronine
(T3) concentrations were measured by a direct radioimmunoassay
(Dickhoff et al., 1978
). The
typical measuring range was 1-64 ng ml-1 for thyroxine and 0.5-16
ng ml-1 for triiodothyronine. Intra-and interassay coefficients of
variation for these assays were 4.3-11% and 3.2-5%, respectively.
Calculations and statistics
A non-parametric three-way analysis of variance (ANOVA) on ranks was used
to determine the significance of photoperiod, temperature and changes over
time. When significant treatment effects were established
(P<0.05), differences among treatments at each time point were
tested using the non-parametric Kruskal-Wallis test. Only sampling points
after initiation of experimental treatments were used in statistical analyses
(thus, the January sampling point is presented graphically, but not included
in statistical analyses).
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Results |
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In the AMB/LDN group condition factor remained relatively stable from February through March and then decreased at a constant rate thereafter (Fig. 1). A stable winter condition factor (massxlength-3)x100 was also seen in the ADV/LDN group, but in late April this group showed a large and rapid decrease in condition factor. Decreased condition factor was not seen in either of the LD 9:15 groups, and the ADV/LD 9:15 group showed an increase in condition factor in mid-April.
Under ambient temperature and normal daylength (AMB/LDN), gill Na+,K+-ATPase activity increased from 2.4 µmol ADP mg-1 protein h-1 in early February to peak values of 12.4 µmol ADP mg-1 protein h-1 in late April (Fig. 2A). The increase was relatively constant from February to early April when the temperature was low, but accelerated from early to late April, coincident with increasing temperature. In the ADV/LDN group, gill Na+,K+-ATPase activity rose more quickly than in the AMB/LDN group, resulting in significant differences between the two groups in late March and early April, but the timing and absolute values of the peak levels were the same. In the AMB/LD 9:15 group, gill Na+,K+-ATPase activity increased at a similar rate to the AMB/LDN group in winter, but rose more slowly than that group from late March onward, reaching only 9.3 µmol ADP mg-1 protein h-1 by the end of the study in mid-May. Gill Na+,K+-ATPase activity of the ADV/LD 9:15 group rose at a rate similar to that of the ADV/LDN group from February to March, but reached peak levels of 7.1 µmol ADP mg-1 protein h-1 in late March and subsequently declined throughout the rest of the study.
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Plasma GH in the AMB/LDN group increased steadily from 1.0 ng ml-1 in February to 1.9 ng ml-1 in early April, and then underwent a rapid increase to peak levels of 8.7 ng ml-1 in late April, coincident with increasing temperature (Fig. 2B). In the ADV/LDN group, plasma GH concentration was low (0.6-1.8 ng ml-1) from February to mid-March, then rose steeply in mid March to 6.2 ng ml-1 several weeks after the increase in temperature, and remained high with peak levels of 8.9 ng ml-1 in late April. In the AMB/LD 9:15 group, plasma GH remained relatively constant from February to the end of March (0.8-1.0 ng ml-1), increased slightly through April and then increased steeply to peak values of 6.9 ng ml-1 in mid-May. Plasma GH concentration of the ADV/LD 9:15 group rose at a rate similar to that of the ADV/LDN group from February to mid-March, but did not show a steep rise in response to temperature, and peak levels in this group were only 3.5 ng ml-1 in late April.
Plasma IGF-I levels of the AMB/LDN group were low (88 ng ml-1) in February and remained relatively constant until mid-April, after which they increased steadily to a peak level of 218 ng ml-1 in mid-May (Fig. 2C). A similar pattern and magnitude of increase was seen in the ADV/LDN group, except that the increase began 2 weeks earlier. Both of the LD 9:15 groups were similar to the AMB/LDN groups and only differed in mid-April.
Plasma thyroxine (T4) levels of the AMB/LDN group remained relatively stable at 10.3-12.8 ng ml-1 from February to late March and then declined to 6.4 ng ml-1 in late April, coincident with increasing temperature (Fig. 3). A similar pattern in plasma T4 concentration was seen in the AMB/LD 9:15 group. By contrast, both of the advanced temperature groups underwent a precipitous decline in plasma T4 levels after the temperature was increased in these groups in early February. Following this decrease, both temperature-advanced groups had increased plasma T4 levels in late March, with the LDN group having substantially higher levels (15.8 ng ml-1) in mid-April than the LD 9:15 group (7.1 ng ml-1).
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Plasma triiodothyronine (T3) levels of the AMB/LDN group were 5.8 ng ml-1 in February, dropping to 4.2 ng ml-1 in mid-March and then rising slowly but steadily to peak levels of 6.9 ng ml-1 in mid-May (Fig. 3). A similar pattern was seen in all of the other groups, the only consistent difference being significantly higher levels of plasma T3 in the ADV/LD 9:15 in early March, late April and May compared to all other groups.
Plasma cortisol levels of the AMB/LDN group were low in February (8.9 ng ml-1) and rose steadily to peak values of 30.5 ng ml-1 in late March, declining to intermediate levels (11.3-19.4 ng ml-1) for the remainder of the study (Fig. 3). In the ADV/LDN group, the plasma cortisol levels rose steadily from February to late March, then rose sharply in early April (38.3 ng ml-1) and again in mid-May (69.7 ng ml-1). In the AMB/LD 9:15 group, the plasma cortisol level was 7.9 ng ml-1 in February, rose through mid-March, declined in early April and rose again in late April to peak values of 40.6 ng ml-1. A similar pattern in plasma cortisol levels was seen in the ADV/LD 9:15 group, except that a secondary increase was not seen and values were significantly lower in late April.
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Discussion |
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The present study agrees with most previous studies that have found an
interaction between photoperiod and temperature in the control of smolt
development (Zaugg, 1981;
Solbakken et al., 1994
;
Sigholt et al., 1998
). In the
present study, the most rapid increase in gill
Na+,K+-ATPase activity occurred under normal
(increasing) daylength and an increasing temperature regime, as has been
observed in several previous studies
(Johnston and Saunders, 1981
;
Sigholt et al., 1998
). This
more rapid increase suggests that there may be stages in the
photoperiod-regulated circannual rhythm that are more sensitive to
temperature. The possible mechanism for such a response may lie in an altered
temperature response of the endocrine system at different times of the
circannual cycle.
Several lines of evidence indicate that an increased level of plasma growth
hormone is causal to the osmoregulatory changes that occur during smolting
(Bjornsson 1997;
McCormick et al., 1998
).
Previous studies have demonstrated that photoperiod-induced alterations in the
timing of smolt development are strongly correlated with changes in
circulating levels of growth hormone. The effect of temperature may also be
mediated in part by changes in plasma growth hormone levels. Exposure of
Atlantic salmon to a temperature increase from 6 to 12°C resulted in a
fivefold increase in plasma growth hormone followed by an advance in
development of seawater tolerance
(Björnsson et al., 1989
).
McCormick et al. (2000
) found
that fish kept at a low winter temperature (<3°C) had lower plasma GH
levels and slower smolt development than fish kept at an elevated temperature,
and that there was a strong correlation between plasma GH levels and gill
Na+,K+-ATPase activity. There was a similar strong
correspondence between changes in plasma GH levels and the timing of smolt
development in the present study, both as a function of temperature and of
photoperiod. In the LDN group, an ADV temperature cycle resulted in earlier
increases in plasma GH levels and gill Na+,K+-ATPase
activity. In the AMB temperature group, a similar increase in both parameters
occurred in late April, corresponding with increased temperatures. In the LD
9:15 group, an increase in temperature resulted in only slight increases in
plasma GH level. This strongly suggests that increased daylength is necessary
for the large increases in GH levels normally seen during smolting, and
increased temperature by itself will have only moderate effects on plasma GH
levels. Together, these data suggest that plasma growth hormone plays a large
role in mediating the effect of temperature on smolt development, although the
mechanism(s) by which this occurs in Atlantic salmon remains to be
elucidated.
An increase in plasma IGF-I (Agustsson
et al., 2001) and hepatic IGF-I mRNA levels occurs during spring
in smolting salmonids (Duan,
1998
), and a significant positive correlation between plasma GH
levels and IGF-I levels has been found during smoltification of Atlantic
salmon (McCormick et al.,
2000
). Such correlation is in agreement with the general view that
plasma IGF-I in vertebrates is mainly of hepatic origin, and that the IGF-I
secretion from the liver is under direct control by GH. However, a closer
inspection of the available data (present study;
McCormick et al., 2000
;
Agustsson et al., 2001
) reveals
that such a causal relationship between GH and IGF-I levels must be modulated
by other factors. Thus, in a number of instances, large increases or decreases
in plasma GH levels are not accompanied by similar changes in IGF-I levels. An
example from the present study is the ADV/LDN group, in which GH levels
increase rapidly in March and decrease in May, without similar changes
occurring in IGF-I. The available plasma IGF-I profiles during Atlantic salmon
smoltification (present study, McCormick
et al., 2000
; Agustsson et al.,
2001
) rather give the general impression of a gradual increase
during spring, irrespective of photoperiod and temperature regimes, or plasma
GH levels. This suggests an endogenous circannual component to IGF-I
secretion, but the mechanism by which plasma IGF-I levels can rise without an
increase in plasma GH levels (see, for example, mid-March plasma values;
Agustsson et al., 2001
) remains
unclear. It could either involve changed GH-receptor densities or activity of
other IGF-I secretagogues.
Relatively little is known of the environmental factors that affect
circulating levels of IGF-I in salmon or in fish in general. Higher plasma
IGF-I levels in response to increased rearing temperatures have been found in
chinook Oncorhynchus tshawytscha and coho salmon O. kisutch
(Beckman et al., 1998;
Larsen et al., 2001
). Higher
plasma IGF-I levels due to elevated temperature were also found in the present
study, though this was limited to one sampling point in mid-April. Although
the ADV temperature regime caused a significant increase in plasma IGF-I
levels in both photoperiod groups at this time, the increase was greater in
the LDN group, suggesting an interaction between temperature and photoperiod
in controlling circulating IGF-I levels. There was a consistent increase in
plasma IGF-I levels in all groups throughout the study, irrespective of
photoperiod and temperature treatment. This suggests that some aspects of the
regulation of plasma IGF-I level may be under an endogenous circannual rhythm.
There was relatively little impact of photoperiod treatment in the present
study, which contrasts with previous work in which increased daylength at an
elevated temperature resulted in significant increases in plasma IGF-I levels
that lasted for almost 2 months (McCormick
et al., 2000
). This affect was only seen under an elevated
temperature regime, and under ambient temperature conditions only moderate
increases in plasma IGF-I levels were observed, similar to the present study.
Based on these limited studies, smolt-related increases in plasma IGF-I can be
expected to be substantially advanced only when both temperature and
photoperiod are advanced.
The clearest effect of environmental manipulation on thyroid hormones in
the present study was a marked decrease in plasma thyroxine concentration that
occurred coincidentally with increased temperature in both temperature regimes
(decreases in late February and late April for the ADV and AMB groups,
respectively). This was a transient increase lasting for 4 weeks in ADV groups
and 2 weeks in AMB. Overall, photoperiod had relatively little impact on
plasma thyroxine and triiodothyronine levels, in agreement with previous work
in which it was concluded that, although photoperiod had some influence on
plasma thyroxine levels (and limited effects on plasma triiodothyronine
levels), plasma thyroxine concentration was substantially higher in Atlantic
salmon smolts reared under cool (ambient) temperatures than at 10°C
(McCormick et al., 2000).
These results are somewhat at odds with the widely observed plasma thyroxine
`surge' during smolting, at a time when water temperatures are normally
increasing. This may be due to rearing conditions and/or stock differences, as
increases in plasma thyroxine levels may also be absent in some
hatchery-reared smolts, although they increase substantially after these fish
are released into the wild (S. D. McCormick, unpublished results). Such
post-release increases in plasma thyroxine concentration may be due to a
number of environmental and biotic changes experienced by the fish, including
flow, turbidity, water quality, food availability and the act of downstream
migration (Iwata, 1995
;
Specker et al., 2000
). These
are environmental signals that do not occur under highly controlled laboratory
settings like the present study.
Plasma cortisol levels increased during the spring, but the magnitude and
timing of the changes differed greatly among the groups. The ADV/LDN group had
significantly greater plasma cortisol levels than other groups in early April
and May, and the increase in April was synchronous with elevated gill
Na+,K+-ATPase activity. There was also a significant
increase in cortisol in the AMB/LD 9:15 group in late April that may have
driven the rise in gill Na+,K+-ATPase activity. However,
little increase in plasma cortisol levels was seen in the AMB/LDN group
despite significant increases in gill Na+,K+-ATPase
activity. Although a seasonal increase in cortisol concentration has been
described as one of the endocrine factors that stimulate smolting
(Hoar, 1988), the available
experimental evidence is often equivocal. A temporal relationship between
plasma cortisol levels and gill Na+,K+-ATPase activity
has been seen previously in this stock of Atlantic salmon
(Shrimpton and McCormick,
1998
). Increases in plasma cortisol levels were seen in response
to increased daylength for fish in warm (10°C) water and cold
(<3°C) water (McCormick et al.,
2000
). At 10°C, elevated cortisol levels were coincident with
an increase in gill Na+,K+-ATPase activity, but this was
not seen at the low temperature. In a different study conducted on the same
stock of Atlantic salmon over 2 years, a seasonal increase in cortisol
concentration was only seen in one year, not in both
(Shrimpton et al., 2000
). The
lack of a strong correspondence between circulating cortisol levels and
physiological changes during smolting, however, does not preclude an important
role for cortisol in these changes. The gill cortisol receptor number increase
during spring (Shrimpton and McCormick,
1998
) and responds to temperature and photoperiod manipulations
(J. M. Shrimpton and S. D. McCormick, unpublished data) potentially altering
tissue responsiveness to cortisol without a significant change in circulating
cortisol levels. This is supported by Patiño et al.
(1985
), who found increased
cortisol turnover during smolting that was coincident with increased gill
Na+,K+-ATPase activity.
The present results indicate that temperature can influence smolt development, most likely by affecting the rate of response to an endogenous circannual rhythm cued by changing photoperiod, and that increased temperature alone probably does not act as a zeitgeber. Plasma thyroxine concentration decreased following increased temperatures, whereas plasma IGF-I, T3 and cortisol levels are only moderately affected by the altered pattern of temperature increases used in this study. In contrast, changes in plasma growth hormone levels precede and are strongly correlated with the physiological changes that resulted from the manipulations of both temperature and photoperiod. The present results therefore provide further evidence that growth hormone in the major endocrine mediator of the environmental effects on the timing of smolt development. There is likely to be an adaptive value involved in the evolution of photoperiod as the main zeitgeber and temperature controlling the rate of development, if it allows for the correct timing of physiological and behavioral development with seasonal environmental changes such as prey abundance in the ocean that are beneficial to survival.
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Acknowledgments |
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