The effects of acclimation to reversed seasonal temperatures on the swimming performance of adult brown trout Salmo trutta
School of Biosciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
* Author for correspondence (e-mail: n.day{at}bham.ac.uk)
Accepted 4 May 2005
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Summary |
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Key words: brown trout, Salmo trutta, swimming, morphometry, temperature
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Introduction |
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At lower temperatures, the metabolic rate is reduced and this may reduce
locomotory capacity, due to decreased contractile rates in both the red and
white swimming muscles and the heart
(Vornanen, 1994). As a
compensatory response to exposure to low environmental temperature,
biochemical and morphological changes occur in the slow oxidative (red) muscle
fibres in a variety of species including salmonids. These changes include
increases in the relative proportion and in the capillary density of these
fibres, increases in both mitochondrial densities and mitochondrial cristae
surface densities (and hence aerobic enzyme activity), decreases in the length
of the diffusion path between the sarcoplasmic and mitochondrial compartments,
and changes in the proportions of muscle enzymatic and myosin heavy chain
isoforms (see Johnston, 1982
;
Jones and Sidell, 1982
;
Blier and Guderley, 1988
;
Egginton and Sidell, 1989
;
Londraville and Sidell, 1996
;
Cordiner and Egginton, 1997
;
Egginton and Cordiner, 1997
;
Guderley and St-Pierre, 2002
;
Watabe, 2002
). In addition,
acclimation to lower temperatures is often accompanied by an increase in the
lipid content of aerobic muscle, which may enhance oxygen transport as well as
acting as an intracellular oxygen store
(Hoofd and Egginton,
1997
).
In most studies where swimming performance has been investigated, the water temperatures and photoperiods under which experimental animals have been maintained have been quoted. However, few have mentioned at what time of the year such experiments have been performed or whether water quality (pH, dissolved ions, etc.) was maintained constant throughout the experimental period. Also, it is rarely indicated whether the experiments were carried out at seasonally appropriate temperatures and photoperiods.
Previous studies (Butler et al.,
1992; Beaumont et al.,
1995
; Day and Butler,
1996
) have revealed that adult brown trout, Salmo trutta,
can maintain their swimming performance (as determined by
Ucrit) independently of the seasonal temperature to which
they were acclimatised (5°C in winter; 15°C in summer). In these
experiments, no attempt was made to control photoperiod, so that all animals
were also exposed to the natural (i.e. seasonal) light/dark cycle. Similar
results were obtained for white crappie (Pomonis annularis)
acclimated to three different temperatures and exposed to five different
photoperiods (Smiley and Parsons,
1997
). To date, this latter study, together with that carried out
by Kolok (1991
) on large-mouth
bass, Micropterus salmoides, appear to be the only ones where the
determination of Ucrit has been performed under conditions
where both photoperiod and environmental temperature have been manipulated.
However, there have been other studies on the effects of season and thermal
acclimation on the locomotory apparatus. For example, Guderley et al.
(2001
) demonstrated the
effects of these factors on the speed of locomotion of the three-spine
stickleback (Gasterosteus aculeatus) during experimentally elicited
startle responses, and Kilarski et al.
(1996
) demonstrated the
effects of season on short-term thermal acclimation and on changes in the
inner mitochondrial membranes of oxidative (`red') skeletal muscle of crucian
carp (Carassius carassius).
The primary purpose of the present study was to see whether the ability of
brown trout to maintain swimming performance at 5°C or 15°C was
independent of season while other environmental variables (water quality,
stocking density and the availability of food) were maintained constant and
the animals exposed to the natural (i.e. seasonally changing) photoperiod
(Butler et al., 1992;
Butler and Day, 1993
;
Day and Butler, 1996
).
Briefly, fish were acclimatised to both seasonal temperatures (5°C in
winter, 15°C in summer) or acclimated to reversed seasonal temperatures
(15°C in winter, 5°C in summer) in moving water and then swum in a
variable-speed water channel up to their Ucrit. Tissue
samples were subsequently taken for biochemical and morphometric analysis to
determine if any observable differences in data obtained from these analyses
could be related to any differences in Ucrit. A
preliminary report of part of this study was given in Day and Butler
(1999
).
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Materials and methods |
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Experimental design
Data were obtained from four groups of 12 resting fish and four comparable
groups of fish that were swum up to their Ucrit. Each
group was acclimatised to one of the `seasonal' temperatures (5°C in
winter, 15°C in summer) or acclimated to one of the reversed seasonal
temperatures (15°C in winter and 5°C in summer)
(Table 1). During the winter,
all experiments were performed between mid-November and January, while during
the summer, experiments were performed from mid-June to August. These periods
correspond approximately to minimum and maximum daylengths of the palaearctic
seasonal photoperiod and the minimum and maximum temperatures experienced by
stockfish at the fish farm (Fig.
1).
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Red muscle, white muscle and liver were immediately removed, weighed and freeze-clamped with aluminium tongs that had been pre-cooled in liquid N2. Red muscle was removed as a thin 57 cm strip posteriorly from the left flank and finishing 3 cm from the base of the tail fin. White muscle was taken as a longitudinal block of tissue, approximately 6 cm in length and 1 cm in diameter, from deep epaxial (dorso-lateral) muscle in the same region. All tissue samples that were to be used for subsequent biochemical analyses were removed, processed and stored in liquid N2 within approximately 90 s from the time of death of the animal. These were later ground to a fine powder under liquid N2, prior to subsequent biochemical analysis.
Determination of gonadosomatic indices and condition factors
The condition factor for each fish was determined and the gonads removed
and weighed for the determination of the gonadosomatic index
(Anderson and Gutreuter, 1983)
(see Table 1).
Muscle morphometry
The remainder of the red and white muscles from the left flank of each
animal was dissected out separately and weighed. The accumulated muscle masses
for both red muscle and white muscle were calculated and then doubled.
Preliminary investigations had shown that contralateral differences between
total masses for both red and white muscles did not vary by more than
±3.5%.
For detailed morphometric studies, whole blocks of tissue containing both
red muscle and white muscle were removed from the right flank of the animal
(within 5 min after death) by directly cutting deep through the skin in the
region of the lateral line. These were then quickly coated in Tissue-Tek
mountant medium (Gurr) and frozen in a small (50 ml) plastic beaker containing
isopentane that had been previously cooled in liquid N2. Sections
of muscle (thickness, 10 µm) were cut at 20°C in a cryostat
(Bright Instruments, UK) and stained for alkaline phosphatase activity at room
temperature by the method of Ziada et al.
(1984) so that blood
capillaries became visible. These were then examined under a microscope fitted
with a camera lucida attachment (Carl Zeiss) which projected images onto a
digitising tablet (GTCO Corporation, Rockville, USA). All images were
processed using Sigma Scan PC digitising software (Jandel Scientific
California, USA). Mean muscle fibre cross-sectional areas, tissue capillary
densities, and the mean number of capillaries per muscle fibre were determined
with the aid of a randomly placed `unbiased sampling' counting frame
(Egginton, 1990
).
Muscle biochemistry
Phosphofructokinase (PFK) and citrate synthase (CS) activities were assayed
at 15°C in muscle samples taken from resting animals. PFK was assayed
according to the method of Su and Storey
(1994) at 340 nm using a
Shimadzu UV-160A spectrophotometer fitted with a CPS240A temperature
controller (Shimadzu Corp., Japan). CS activity was determined in the same
samples at 412 nm by the method of Srere et al.
(1963
), as modified by Hansen
and Sidell (1983
). PFK was
extracted by homogenising muscle samples on ice (3 x15 s bursts at 20
500 r.p.m. with a Ultra-Turrax T25 homogeniser) in an extraction buffer
containing 75 mmol l1 Tris, 1 mmol l1
EDTA, 2 mmol l1 MgCl2 and 2 mmol
l1 DTT (pH 7.4). This medium (minus the DTT) was also used
to extract CS. Prior to analysis, all samples were clarified by centrifugation
at 300 g for 5 min at 15°C. It should be noted that
preliminary assays for both of these enzymes were carried out at 5°C but,
for some reason, the data obtained were highly variable between aliquots of
tissue homogenate. There was no sign of condensation at 5°C and the
variability was eliminated when aliquots of homogenised samples were analysed
at 15°C. All values of enzyme activities are given per unit wet mass.
Muscle glycogen and free glucose levels were determined by the method of
Keppler and Decker (1974). For
determination of lactate concentrations, a 100120 mg sample of frozen,
powdered tissue was homogenised with ice-cold 1 mol l1
perchloric acid (dilution factor 1:5, mass:volume). After centrifugation at
8000 g for 10 min, the supernatant was neutralised with 2 mol
l1 KOH and then assayed at 340 nm and 25°C by the method
of Gutman and Wahlefeld
(1974
). Total muscle lipid
content was determined by the method of Bligh and Dyer
(1959
). For total ammonia
concentration [Tamm], weighed (approximately 100 mg) portions of frozen,
powdered red muscle and white muscle were homogenised and deproteinised in
ice-cold 1 mol l1 perchloric acid (dilution factor 1:5
mass:volume) and then centrifuged at 10 000 g for 2 min to
remove precipitated proteins. The supernatant was neutralised with 2 mol
l1 KHCO3 (Kun
and Kearney, 1984
) and then analysed for total ammonia content
([NH3]+[NH4+]) using the Sigma 171-A diagnostic kit
(Day and Butler, 1996
).
Statistical analyses
All data were analysed by analysis of variance (ANOVA). Between-treatment
comparisons were made using the post-hoc Tukey multi-comparison test
(Zar, 1984), and significance
was taken to be when P<0.05. When any variable is quoted as being
`different' from another, this means that the difference is statistically
significant. All means are plotted with their standard errors
(S.E.M.).
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Results |
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Swimming performance
There was no difference between the Ucrits of the two
groups of fish swum at seasonal temperatures (5°C in winter, 15°C in
summer; Table 2). However, in
both winter and summer, the Ucrits of these groups were
significantly higher than those for the groups acclimated to the reversed
seasonal temperatures (5°C in winter, 15°C in summer). In winter, fish
acclimated to 15°C exhibited a 32% lower Ucrit
compared with those acclimatised to 5°C, while in summer, fish acclimated
to 5°C showed a 30% lower Ucrit than those fish
maintained at 15°C. At reversed seasonal temperatures, the mean
Ucrit of fish swum at 15°C in winter was 11% lower
than that for fish swum at 5°C in summer
(Table 2).
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Morphometry
Masses of heart, red muscle and white muscles
While there was little effect of season or temperature on the mass of the
white muscle, fish acclimated to 5°C had greater amounts of both red and
heart muscles than those acclimated to 15°C, and the difference was
greater in winter (Table 2). Thus, the amounts of red and heart muscles in fish acclimatised to 5°C in
winter were 42% and 61% greater, respectively, than those in fish acclimatised
to 15°C in summer, but in fish acclimated to 5°C in summer, the
amounts of red and heart muscles were only 20% and 41% greater, respectively,
than those in fish acclimatised to 15°C in summer.
Morphometry of red and white muscles
Again, there was little systematic difference in any of the measured
parameters in white muscle between the different groups
(Table 2), whereas mean fibre
cross-sectional area of the red muscle showed a similar pattern to the amount
of red muscle (see above). In fish acclimatised to 5°C in winter, mean
fibre cross-sectional area of the red muscle was 34% greater than in fish
acclimatised to 15°C in summer, but in fish acclimated to 5°C in
summer, mean fibre cross-sectional area of the red muscle was only 13% greater
than that in fish acclimatised to 15°C in summer
(Table 2). Although capillary
density was greatest in red muscle of fish acclimated to 5°C in summer and
lowest in fish acclimatised to 5°C in winter, the mean number of
capillaries per muscle fibre was approximately 15% greater in red muscle of
fish acclimated to 5°C than in those acclimated to 15°C, irrespective
of season (Table 2).
Enzyme activities
The activities of CS were approximately 5.5 times greater in red muscle
than in white muscle (Table 2),
and in both muscles showed similar patterns among the groups of fish to those
seen with the amount of red muscle and mean fibre cross-sectional area for red
muscle (see above). In fish acclimatised to 5°C in winter, CS activity in
red and white muscles was 65% and 82%, respectively, higher than in those of
fish acclimatised to 15°C in summer, but in fish acclimated to 5°C in
summer, CS activity in red and white muscles was only 28% and 34% higher than
in those of fish acclimatised to 15°C in summer
(Table 2). The activities of
PFK were between 5 and 5.5 times greater in white muscle than in red muscle in
the various groups of fish (Table
2), but within each muscle, the activities were similar in all
groups of fish, except in those acclimated to 15°C in summer. In this
group, activity of PFK was approximately 80% higher than that in the other
groups (Table 2).
Metabolic substrates and metabolites
In resting fish, the concentrations of glycogen in the liver were
710 times greater than those in white muscle and 818 times
greater than those in red muscle (Fig.
2). In resting fish, there was no difference in the concentrations
of glycogen in the red muscles between any of the groups of fish, whereas in
white muscle and liver, the concentrations were greatest in fish acclimatised
to 5°C in winter and lowest in fish acclimatised to 15°C in summer. In
all tissues, the concentrations of glycogen were lower in fish that had swum
to Ucrit than in those at rest, but, after swimming to
Ucrit, the concentrations were not as low in fish
acclimated to reversed seasonal temperatures as in those acclimatised to
seasonal temperatures (Fig.
2).
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The concentrations of lipid in red muscle of resting fish were between 6 and 13 times higher than those in white muscle (Fig. 4). In white muscle of resting fish, lipid concentrations differed little between groups of fish, except for those acclimated to 5°C in summer, in which it was approximately 20% lower than in the other groups. However, in red muscle of resting fish, those acclimated to 5°C had greater concentrations of lipid than those acclimated to 15°C, and the difference was greater in summer. Lipid concentration in the red muscle of resting fish acclimatised to 5°C in winter was 110% greater than that in fish acclimatised to 15°C in summer, but in resting fish acclimated to 5°C in summer, lipid concentration was only 83% greater than that in fish acclimatised to 15°C in summer. The concentrations of lipid were lower in both red and white muscles in all groups of fish swum to Ucrit compared to those in the groups of resting fish, except in the white muscle of those acclimated to 5°C in summer, and the proportional reduction was similar in each case (Fig. 4).
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In resting fish, the concentrations of lactate were between 150 and 200% greater in white muscle than in red muscle and, within each muscle, the concentrations were similar in all groups of fish (Fig. 5A,B). The concentrations of lactate in both muscles of fish that had swum to Ucrit were higher than in those at rest and, in red muscle, the concentrations were similar in all groups. However, in white muscle, the concentrations of lactate in the fish swum to Ucrit were 4555% lower in those acclimated to reversed seasonal temperatures compared with those in fish acclimatised to seasonal temperatures (Fig. 5).
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A similar pattern to that seen with lactate concentrations occurred with total ammonia [Tamm] in the muscles, with greater [Tamm] present in both muscles in fish swum to Ucrit compared with those in resting fish (Fig. 5C,D). However, in white muscle, [Tamm] of fish swum to Ucrit were lower in those acclimated to reversed seasonal temperatures than in those acclimatised to seasonal temperatures.
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Discussion |
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Swimming performance
The present study clearly demonstrates that acclimation to reversed
seasonal temperatures lowers swimming performance (Ucrit)
in adult brown trout. This appears to be due, at least in part, to a reduction
in the use of white muscle, as the increases in lactate and ammonia in white
muscle in the fish swimming to Ucrit at reversed seasonal
temperatures were not as great as those observed in fish swum at seasonal
temperatures. Thus, this reduction in swimming performance with acclimation to
reversed seasonal temperatures cannot be explained by unusually high levels of
plasma and muscle ammonia, as occurs in fish exposed to low pH
(Beaumont et al., 2000). In
addition, the animals held at reversed seasonal temperatures were sampled
after having acclimated to these conditions over an extended period. Thus,
other, comparatively long-term, changes must have been responsible for the
differences in swimming performance between the groups of fish acclimatised to
seasonal and acclimated to reversed seasonal temperatures.
Effects of acclimatisation to seasonal temperatures on muscle morphometry and biochemistry
There is increasing evidence that acclimation to low temperature causes
many fish to undergo anatomical and biochemical changes to their locomotory
apparatus. In the current study, the capillary-to-fibre ratio, mean
cross-sectional fibre area and mass of red muscle were significantly greater
in fish acclimatised to 5°C in winter than in those acclimatised to
15°C in summer.
The greater mass of red muscle in fish acclimatised to 5°C in winter
than in those acclimated to 15°C in summer was the result of an increase
in mean fibre cross-sectional area of this tissue. This phenomenon of
`bulking-up' of aerobic muscle at low temperature has been demonstrated in a
number of species including Carassius auratus
(Johnston and Lucking, 1978)
and Morone saxatilis (Jones and
Sidell, 1982
). As observed in other species, including rainbow
trout (Egginton and Cordiner,
1997
), the capillary to red muscle fibre ratio increased with
acclimation to the lower temperature in the present study, although the
capillary density per unit area decreased due to the increase in fibre
diameter. Such changes, together with the cardiac hypertrophy, could
potentially increase blood flow to aerobic muscle, which would enhance aerobic
metabolism of this tissue during winter.
White muscle changed little with acclimatisation to the lower winter
temperature or to 5°C in summer. This is somewhat surprising, since it
suggests that white muscle has low `plasticity' in response to changes in
abiotic conditions. Undoubtedly, white muscle must adapt to environmental
temperature in some way, since there is no difference in
Ucrit between animals maintained at the two seasonal
temperatures, despite a lack of change in the speed at which white muscle is
recruited (approximately 1 body length s1;
Day and Butler, 1996).
The phenomenon of increased aerobic enzyme activity at lower temperatures
is well known and has been demonstrated in a number of species (see
Introduction), where it appears to be related to an enhancement in the ability
of the fish to utilise lipid as an energy source at low temperatures
(Hazel and Prosser, 1974). The
current study demonstrates that, when assayed at the same temperature
(15°C), CS activities in both red and white muscles were greater in winter
fish at 5°C than in summer fish at 15°C (see also
Battersby and Moyes, 1998
), and
the reverse was true for PFK. Unfortunately, it did not provide an indication
of in situ (physiological) activities of CS and PFK in the winter
fish. For this, activities of both of these enzymes should have been
determined at 5°C for the winter fish but, as we have previously indicated
(see Results), we were unable to obtain consistent data at this temperature.
Therefore, the data only demonstrate changes in absolute capacity and do not
provide evidence for true thermal compensation.
Nathanailides (1996) used
the term EQ10 to describe the extent to which the activity
of an enzyme increases with every 10°C decrease in acclimation temperature
and compared this with the Q10 of the enzyme. If
EQ10 equals Q10, there is perfect compensation.
Assuming a Q10 of 1.46 for CS
(Nathanailides, 1996
), the
ratio of EQ10/Q10 is 1.13 for seasonally
acclimated brown trout and 0.88 for those at 5 and 15°C in summer. Thus,
this analysis clearly demonstrates that compensation of CS activity is greater
at a low seasonal temperature than at a low non-seasonal temperature.
Effects of acclimation to reversed seasonal temperatures on muscle morphometry and biochemistry
The differences between the variables measured in fish at seasonal and
reversed temperatures indicate that environmental temperature is not the only
factor responsible for these observations. `Seasonal' effects also seem to be
at work. For example, PFK levels in animals at 15°C were considerably
lower in winter than in summer and indeed were no different from those
observed in animals acclimated to 5°C in winter. In addition, at 5°C,
the capillary density of red muscle was higher in summer compared with in
winter, probably due to the observed decrease in fibre size. The activities of
CS in red and white muscle, the masses of red and heart muscle and mean red
muscle fibre cross-sectional area were all lower in fish acclimated to 5°C
in summer than in those acclimatised to the same temperature in winter. This
suggests that, at the lower temperature, full thermal compensation is only
possible during winter.
It would appear, therefore, that the changes in muscle morphometry and
biochemistry that accompany acclimation to reversed seasonal temperatures are
`incomplete', when compared with changes observed in fish acclimated to
seasonal temperatures, or, at the very least, take longer than the duration of
acclimation period used in the present study. Further evidence for this comes
from a study by Kilarski et al.
(1996) on the mitochondrial
morphometrics of oxidative muscle of crucian carp that were acclimated for 6
weeks to 5°C and 25°C in both winter and summer. In this study, it was
demonstrated that at 5°C the surface density of outer mitochondrial
membrane per muscle was higher in summer than in winter. At 25°C the
surface density of inner mitochondrial membrane per fibre and the surface
density of the inner mitochondrial membrane were higher in summer than in
winter. In addition, Bouchard and Guderley
(2003
) studied the time course
of acclimation, as determined by red muscle mitochondrial enzyme activity and
respirometry, of groups of rainbow trout that were either `warm acclimated'
(water temperature raised from 5°C to 15°C during winter) or `cold
acclimated' (water temperature lowered from 15°C to 5°C during
summer). They found that warm acclimation appeared to be completed within 8
weeks whereas cold acclimation appeared to be incomplete after 10 weeks.
The only other comparable biochemical data for the effects of reversed
seasonal temperatures on enzyme activity concern the three-spine stickleback,
Gasterosteus aculeatus (Guderley
et al., 2001). In this study, fish were acclimated to 8°C and
23°C in both spring and autumn, and enzyme activities were determined (at
10°C and 20°C) for pectoral and axial muscle. It was observed that, in
spring, the highest level of PFK activity was observed in axial muscle from
fish acclimated to the lower temperature in spring and assayed at 20°C
(there was no difference at 10°C and no data were presented for the autumn
experiment). This is the opposite of that observed in the current study for
brown trout acclimated to 15°C in winter.
Guderley et al. (2001) also
demonstrated that for pectoral (i.e. aerobic) muscle (in contrast to what was
observed in axial muscle) there was no significant difference between the
levels of CS activity between the two groups of fish that were acclimated to
8°C and 23°C in the spring. This again was the reverse of what we
observed in the brown trout, where the highest levels in red muscle occurred
at 5°C. In spite of these contradictory data (which may be related to
differences in life cycle or taxonomy), both of these studies do suggest that
a seasonally changing environmental temperature is not the only factor that
influences changes in muscle morphology and physiology.
What is the primary influence on swimming performance?
The biochemical and morphological data in the present study provide
evidence that full thermal compensation does not occur in the fish that are
acclimated to reversed seasonal temperatures. Thus, there must have been a
factor or factors in addition to temperature that were responsible for the
differences in Ucrit between the groups of fish
acclimatised to `seasonal' and acclimated to `reversed seasonal' temperatures.
In fact, with few possible exceptions (e.g.
Staurnes et al., 1994), there
appears to be little experimental evidence to support the idea that
temperature alone can act as a zeitgeber in fish, although it can, in
conjunction with photoperiod, influence physiological changes
(McCormick et al., 2002
).
Seddon and Prosser (1997
)
concluded that acclimation to environmental temperature was `not an all or
none phenomenon' and may depend on a variety of seasonal factors, including
time of collection, nutritional and reproductive state, and circannual
cycles.
Photoperiod is probably the most important environmental cue influencing
changes in the locomotory apparatus and Ucrit of brown
trout, since it has previously been demonstrated to be the dominant
zeitgeber for several endogenous rhythms and physiological changes in
other fish species including circadian rhythmicity in heart rate
(Pennec and Le Bras, 1988) and
the timing of smolting in anadromous salmonids
(Hoar, 1988
;
Duston and Saunders, 1990
). In
addition, studies on the effects of light exposure on sexual maturation of the
stickleback (G. aculeatus) have revealed endogenous daily and annual
rhythms of changing photoreactivity
(Baggerman, 1985
). In this
species, the onset of sexual maturation can be experimentally triggered by a
short (2 h) exposure to light during the scotophase in winter. Because of its
predictable annual variation, photoperiod undoubtedly functions as a
synchroniser of such rhythms in the natural cycle. Assuming that such rhythms
exist in brown trout, it would be intriguing to perform swimming experiments,
such as those described in the present study, on fish that were subjected to
both reversed seasonal temperatures and reversed seasonal photoperiods.
What other factors may influence swimming performance?
In addition to photoperiod, there are a number of naturally occurring,
seasonally changing environmental factors that may have influenced adaptation
of the locomotory apparatus of brown trout to unseasonal temperatures. One
example is the annual and semi-annual variation in the earth's geomagnetic
field (see Malin et al., 1999)
to which animals, including salmonids, are known to be sensitive (see e.g.
Yokoi et al., 2003
;
Diebel et al., 2000
). So, it
is conceivable that changes in geomagnetism could be an exogenous cue that,
probably in combination with others, affects changes in the locomotory
apparatus of brown trout. Indeed, there is increasing evidence that in
migratory animals, including salmonids, photoreception and geomagnetic
detection are inextricably linked
(Deutschlander et al.,
1999
).
Endogenous biological clocks may also play an important role, since their
powerful influence on organisms is well known. For example, Saether et al.
(1996) demonstrated that
arctic char (Salvelinus alpinus) showed seasonal changes in food
consumption and growth that were endogenously driven, being unaffected by
experimental manipulation of photoperiod. Perhaps it is the `regularity' of
one or more of these internal clocks that prevents the locomotory apparatus of
brown trout from becoming fully adapted to unseasonal environmental
temperatures.
The present study is the first to investigate the effects of acclimation to reversed seasonal temperatures on Ucrit and the morphometrics and biochemistry of the locomotory apparatus of a salmonid fish. It illustrates the importance of ensuring that experiments performed on fish such as brown trout should be performed under conditions of temperature and photoperiod that approximate those occurring in the natural environment at the time of the year when they are performed. It is only under these conditions that the data produced from such studies will be of relevance to animals in their natural environment.
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Acknowledgments |
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