Relationship between individual variation in morphological characters and swimming costs in brook charr (Salvelinus fontinalis) and yellow perch (Perca flavescens)
Département de chimie-biologie, Université du Québec à Trois-Rivières, CP 500, Trois-Rivières (Québec) G9A 5H7, Canada
* Author for correspondence at present address: Department of Biological Sciences, University of New Orleans, New Orleans, LA 70148, USA (e-mail: pboily{at}uno.edu )
Accepted 14 January 2002
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Summary |
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Key words: brook charr, Salvelinus fontinalis, yellow perch, Perca flavescens, swimming cost, standard metabolic rate, morphology, body shape
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Introduction |
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Variation in morphological characters can affect swimming ability in three
different ways; it can affect the ability to perform precise maneuvers, the
ability to perform powerful acceleration, or the energetic cost of sustained
swimming (Webb, 1982).
Morphological characters that are likely to affect the energetic cost of
sustained swimming are those related to thrust production and to drag forces
such as body shape, caudal peduncle depth, the size and aspect ratio of the
caudal fin (Webb, 1982
;
Webb and Weihs, 1986
). Of
these, the overall body shape of fishes is particularly interesting because of
its possible link with energy reserves. The accumulation of energy reserves
may lead to an overall body shape that is more stout and less elongated, which
can potentially increase drag forces and, as a consequence, swimming costs.
Such a conflict between the accumulation of energy reserves and locomotor
efficiency is well documented in small birds, where the accumulation of fat
causes an increase in the energetic cost of flight
(Chai and Millard, 1997
), which
may even lead to an increase in mortality caused by predation
(Gosler et al., 1995
).
In this study, we analyzed metabolic and morphological data obtained as
part of another study (P. Boily, D. Boisclair and P. Magnan, unpublished
results) to investigate the existence of functional relationships between
individual variation in morphological characters and swimming costs. For this
purpose, we used wild and domestic brook charr (Salvelinus
fontinalis), a species for which individual variation in morphology is
often correlated to habitat use (Bourke et
al., 1997; Dynes et al.,
1999
; McLaughlin and Grant,
1994
; McLaughlin,
2001
). Charrs in general can exhibit high levels of phenotypic
plasticity and may not be representative of most teleosts. Therefore, we also
used the yellow perch (Perca flavescens), an unrelated freshwater
species that lives in similar oligotrophic lakes and has a swimming mode
similar to brook charr (Scott and
Crossman, 1974
; Lindsey,
1978
; Webb,
1984a
).
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Materials and Methods |
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All fish were maintained in large temperature-controlled, dechlorinated freshwater tanks. Water quality was tested regularly throughout the study and fish appeared to be in good health. The photoperiod was maintained at 12 h: 12 h L:D and fish were fed ad libitum once a day with commercial trout pellets (WBC and DBC) or equal parts of commercial trout pellets and Tetramin flakes (WYP). When fishes were first brought to the laboratory, the water temperature was set to a value similar to that of their origin. Gradually, water temperature was adjusted by 1 °C per day to the coldest experimental water temperature, i.e. 8 °C for DBC and 12 °C for WYP as they did not swim consistently at 8 °C in preliminary experiments. Because of the limited number of individuals from the WBC group that had an appropriate size, metabolic rate measurements on this population were obtained only at 12 °C. To minimize mortality, water temperature was changed from the coldest to warmest temperatures (from 8 or 12 °C, to 16, 18 and 20 °C). The experiments began after fish had acclimated to laboratory conditions for 2 months and were completed less than 3 months afterwards. After the 2 month acclimation period, charr and perch seemed to behave and swim normally in their holding tanks, without any erratic movements as the experimenter approached. We assumed that any bias due to laboratory rearing conditions would be additive on fish behavior and physiological performances. Fish were acclimated to their experimental temperature for 6-12 days prior to measurements and any given fish was used at only one water temperature.
Open-flow respirometry system and experimental protocol
Respirometers were modified Blazka-type swim tunnels (3.37±0.031),
similar to those described by Beamish et al.
(1989), and for which the
velocity profile is approximately rectilinear. Respirometers were connected to
an open-flow system, through which fresh, oxygenated water flowed at a rate
ranging from 20 to 80 ml min-1, depending on the experimental
temperature. Water velocities (15-35 cm s-1) were adjusted by
varying the voltage of the submersible pump that created water movement inside
each respirometer; the relationship between pump voltage and water speed was
calibrated using a miniature water speed meter (OTT, Kempten, Germany; blade
number 2-3). A mildly electrified (0-5 V) metallic grid at the end of the swim
tunnel was used to motivate the fish to swim against the water current.
Respirometers were submerged into a temperature-controlled water tank
(±0.5 °C). Water flowed continuously at a stable rate through all
respirometers.
Six to eight respirometers were connected simultaneously to the
respirometry system and a single fish was placed in each respirometer.
Solenoid valves directed water flow so that the oxygen concentration of the
water entering and leaving each chamber was measured once every hour. Oxygen
concentration was measured by directing the water flow to sub-sampling
chambers in which the temperature-compensated probe of an oxygen meter (YSI
model 54) was located. A computer using a BASIC program (W. Beamish, personal
communication) recorded outputs from oxygen meters. Oxygen meters were
calibrated daily using air-saturated water maintained at the experimental
temperature, and their accuracy was verified weekly using the Winkler
titration method modified for small volumes
(APHA, 1989). Water flow rate
through each respirometer was measured twice daily. Rates of O2
consumption (
O2;
mg O2 h-1) were corrected for the oxygen consumption
occurring in empty respirometers and for the time lag associated with
open-flow respirometry systems (Niimi,
1978
).
Two days prior to experiments, between 16:00 h and 18:00 h, 6-8 individuals
were isolated and fasted in a tank in which the water was recirculated from
the respirometry system. On the day prior to the experiments, between 16:00 h
and 18:00 h, fish were individually placed in a respirometer in which current
speed was set at 15 cm s-1. The following morning, starting at
08:00 h, rates of oxygen consumption were recorded while gradually increasing
current speed every 2 h, by intervals of 5 cm s-1, up to 35 cm
s-1. Fish swam normally in the respirometers, rarely touching the
electrified grid, until current speed became too high for them to maintain a
stable position. When this occurred, current speed was reduced to 15 cm
s-1, and fish were left in the respirometers overnight. The
following morning, fish were killed with an overdose of MS-222, weighed
(M) to the nearest 0.01 g, and measured to the nearest 0.05 mm for
the following morphological characters: standard length
(Ls), maximum width (Wmax) and depth
(Dmax), length of pectoral fin (Lp),
depth of caudal peduncle (Dp), length
(Lc) and depth (Dc) of caudal fin. For
each individual, maximum cross-sectional surface area (SA, in
cm2), assuming an ellipsoid shape, was calculated as:
![]() | (1) |
To avoid using individuals that used anaerobic metabolism to a significant
extent, only data from individuals that swam consistently at at least three
swimming speeds, for 2 h at each swimming speed, and for which the
log10O2
increased linearly with swimming speed, were kept for further analysis;
approximately 10 % of individuals were rejected because they did not meet
these criteria. Furthermore, few DBC individuals and no WYP individuals were
able to swim consistently at 8 °C. To maintain consistency between species
and to avoid large variation in sample size between experimental water
temperatures, only data obtained at 12 °C and higher were kept for further
analyses, leaving a sample size of 10 WBC, 53 DBC and 57 WYP
(Table 1).
|
Analyses
All morphological characters were significantly and linearly related to
standard length (P<0.05). Accordingly, size-adjusted morphological
characters (Wmax', Dmax',
Lp', Dp',
Lc' and Dc') were
calculated as the residuals of the linear regression of each character as a
function of Ls
(Packard and Boardman, 1987).
The aspect ratio of the caudal fin (ARc) was calculated by
dividing Dc by Lc. A body shape index
(BSI) was calculated as the residuals of the following model:
![]() | (2) |
For each individual, standard metabolic rate (SMR) was estimated using the
following model:
![]() | (3) |
Measurements of
O2 and of
CSWnet were obtained at multiple current speeds for each
individual. To eliminate pseudoreplication, an absolute swimming cost index
(SWCI) was calculated, for each individual, as the average of the
residuals of Equation 3 applied separately to each group at each water
temperature. A net swimming cost index (SWCInet) was
calculated in a similar manner, by replacing
log10
O2
with log10CSWnet in Equation 3. These
regressions were significant for all groups at all experimental temperatures
(P<0.05). Individuals with positive values for these indices have
on average higher
O2 or
CSWnet than predicted from current speed at a given
water temperature, and therefore have higher swimming costs than individuals
with negative values. The difference between SWCI and
SWCInet is that SWCInet is
independent of SMR. Analyses of variance indicated that both indices differed
significantly among individuals, and individual repeatability values,
calculated from the results of these analyses of variance
(Lessells and Boag, 1987
),
were high (0.87 for SWCI and 0.75 for
SWCInet), indicating that these indices reliably reflect
individual variation in swimming costs rather than random noise. Residuals
were calculated at each water temperature separately, instead of including
water temperature as a variable in the models, because the effects of current
speed changed according to water temperature (P. Boily, D. Boisclair and P.
Magnan, unpublished data). Similarly, an SMR index (SMRI) was calculated at
each water temperature as the difference between the group mean and the
individual's value of log10SMR. These calculations were done
separately at each water temperature, and logarithmic values of SMR were used
for consistency with the calculations of swimming cost indices. None of the
indices (SWCI, SWCInet, SMRI) changed
significantly according to water temperature and nearly identical results were
obtained if water temperature was included as an independent variable for the
calculation of indices.
For each group of fish, stepwise multiple linear regression analyses (forward selection, P<0.05 to be included) were performed to test the significance of the effects of BSI and size-adjusted morphological characters on SWCI, SWCInet and SMRI. In addition, standard length and water temperature were included as independent variables, to eliminate their potentially confounding effects. Standard length was used as a measure of body size, for consistency with size adjustments of morphological characters and calculations of BSI; nearly identical results were obtained if body mass was used instead. Furthermore, Dmax', Wmax' and Dp' were excluded from these analyses because they were highly correlated to BSI (r>0.69, P<0.001). All statistical analyses were performed using SYSTAT version 8.03 with a 5 % level of significance.
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Results |
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Discussion |
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Our method to calculate a body shape index is very similar to methods
commonly used to estimate condition in salmonids and other fish species
(Chellappa et al., 1995;
Simpson et al., 1992
;
Wootton and Mills, 1979
).
Therefore, the positive relationship between SMRI and the body shape index may
reflect a trade-off between two opposing selective forces. On the one hand,
high levels of energy reserves could increase the fitness of individuals
through higher reproductive investments; it is known that surplus energy is
invested in growth and reproduction, and that higher fecundity and larger eggs
increase survivorship rates (Moyle and
Cech, 1996
). On the other hand a higher body shape index could be
disadvantageous because of the associated increase in maintenance costs (SMR),
which also results in an increase in absolute swimming costs. This
relationship between the SMR index and the body shape index could be the
expression of a reaction norm (Stearns,
1992
), allowing different individuals to use different habitats
(i.e. stout individuals, the littoral zone, and slender individuals, the
pelagic zone) (see Dynes et al.,
1999
; Proulx and Magnan, 2001). This reaction norm could still be
present in the genetic expression of domestic brook charr because they have
been reared in Québec hatcheries for less than a century. In this
context, the trade off between higher reproductive investment and higher SMR
could be balanced by the differential costs of foraging in these habitats,
which are presumed to be lower in the littoral zone (lower swimming costs and
higher habitat profitability;
Héroux, 1998
).
Trade-offs between the accumulation of energy reserves and locomotor
efficiency are well documented in small birds, where an increase in storage of
energy reserves increases the cost of flight because of the excess weight
(Chai and Millard, 1997
), and
may even lead to larger mortality rates due to predation
(Gosler et al., 1995
). The main
difference with our results is that a better condition is not directly related
to an increase in locomotion costs per se, but rather to an indirect
increase in swimming costs because of higher SMR. This explanation of the
mechanism involved in increasing SMR as the body shape index increases is
speculative, however, because body shape indices can be poor predictors of
body composition (Chellappa et al.,
1995
).
Similar to brook charr, the absolute swimming cost index of yellow perch
was positively related to the body shape index. However, in contrast to brook
charr, the net swimming cost index was also positively related to the body
shape index, while the SMR index was not. Furthermore, both absolute and net
swimming cost indices significantly increased as the aspect ratio of the
caudal fin decreased. Taken together, these results suggest that, in yellow
perch, the relationship between morphological characters and swimming costs is
the result of variation in drag and thrust forces rather than variation in
SMR. While the effect of subtle variation in morphology on drag and thrust
forces can be hard to predict (Vogel,
1994), our results suggest that slender yellow perch individuals
produce less turbulence and therefore less drag, and that yellow perch with
high-aspect caudal fins produce thrust more efficiently, both of which would
lead to lower swimming costs. Such relationships between body shape, caudal
fin shape and swimming efficiency are well documented at the interspecies
level (Webb, 1984b
,
1988
).
In conclusion, our results indicate that absolute swimming costs increase in stout individuals for all three fish groups investigated. While a similar trade-off between the accumulation of energy reserves and locomotion efficiency may be present in both species, the mechanism generating it appears to differ. In brook charr, the increase in swimming costs associated with a stout body shape is related to an increase in SMR, while this is not the case for yellow perch, where the increase in swimming cost may be the result of increased drag forces.
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Acknowledgments |
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