the respiratory metabolism of temperature-adapted … · bolic costs to traverse a unit distance...
TRANSCRIPT
J. exp. Biol. (1982), 97, 359-373 3 5 9JWith 6 figures
Wrinted in Great Britain
THE RESPIRATORY METABOLISM OFTEMPERATURE-ADAPTED FLATFISH AT REST ANDDURING SWIMMING ACTIVITY AND THE USE OF
ANAEROBIC METABOLISM AT MODERATESWIMMING SPEEDS
BY GARRY G. DUTHIE*
Department of Zoology, University of Aberdeen, Scotland, United Kingdom
{Received 24 June 1981)
SUMMARY
(1) The standard oxygen consumption and the oxygen consumptionduring measured swimming activity have been determined in three flatfishspecies at 5, 10 and 15 °C.
(2) The relationship between weight and standard oxygen consumptionfor flatfish conform to the general relationship Y = aWb. On an interspeciesbasis, standard oxygen consumption of flatfish is significantly lower than thatof roundfish.
(3) A semilogarithmic model describes the relationship between oxygenconsumption and swimming speed for the three species. Values for maximumoxygen consumption, metabolic scopes and critical swimming speeds are lowin comparison to salmonids.
(4) The optimum swimming speeds and critical swimming speeds offlatfish are similar. It is suggested that, over long distances, flatfish adopta strategy of swimming at supercritical speeds with periods of intermittentrest to repay the accrued oxygen debt.
(5) Elevated lactic acid levels in flounder white muscle after moderateswimming indicate an additional 15 % anaerobic contribution to the cost oflocomotion as calculated from aerobic considerations.
INTRODUCTION
This study has examined the metabolism of three flatfish species at rest and whileswimming in a tunnel respirometer, and has considered the results in terms of meta-bolic scopes (Fry, 1947) and energetic costs of locomotion. Except for feeding andescape, or during migration, flatfish rest on bottom substrates for prolonged periods.It is likely that there are differences in metabolic costs and swimming strategiesbetween flatfish and more active, well studied, roundfish species.
Priede & Holliday (1980) established oxygen consumption-swimming speedrelationships for the flatfish plaice, Pleuronectes platessa, at three temperatures andrelated their results to those of sonic tracking experiments in the North Sea. (Greer-Walker, Harden-Jones & Arnold, 1978). The species used in the present study were
Present address: Research Unit for Comparative Animal Respiration, University of Bristol,Road, Bristol BS8 iUG, England.
360 G. G. DUTHIE
the flounder, Platichthys flesus (L), the common dab, Limanda limanda (L) and trfllemon sole, Microstomus kitt (Walbaum). The standard metabolism (Fry, 1947) ora wide weight range of fish exposed to constant temperatures for prolonged periodswas measured. Using a narrow weight range, the effects of adaptation temperature(Alderdice, 1976) on the respiratory metabolism during swimming activity wasassessed. Estimates of maximum levels of oxygen consumption (active metabolicrates), maximum sustained swimming speeds (critical swimming speeds) and meta-bolic costs to traverse a unit distance (Weihs, 1974; Webb, 1975; Priede & Holliday,1980) have been made and the results discussed in terms of swimming strategiesflatfish may adopt.
Further, the assessment of exercise capability in terms of metabolic costs assumesnegligible anaerobic contribution (Jones & Randall, 1978). It was observed that theflatfish invariably showed a gradual decline in oxygen consumption subsequent toswimming at moderate speeds, suggesting that an oxygen debt was incurred. Anattempt was made to assess the relative contributions of aerobic and anaerobic meta-bolism to the total energy expenditure during swimming in the flounder. Lactic acidproduction was used as an index of anaerobic energy expenditure.
MATERIALS AND METHODS
(1) Collection and maintenance of fish
Large individuals (100-800 g) were trawled off the coast of Aberdeen, Scotland.Smaller specimens (1-50 g) were obtained by beach seine. The fish were maintainedin aerated constant temperature tanks for two months prior to experimentation toensure thermal adaptation. All three species were maintained at 5 ± 0-2 and 15 + c-2 °C.In addition, a 10 + 0-2 °C regime was introduced for dabs and lemon sole. The fishwere fed daily to satiation and starved for 48 hours prior to metabolic determina-tions. A 12 h L:D photoperiod was maintained.
(2) Measurement of oxygen consumption
Two types of respirometer were used. That for measuring standard oxygen con-sumption consisted of a closed system with a flush capacity. Three sizes of perspexboxes were used as respiration chambers, total volumes being 12-4, 7-1, and 0-5 1.This allowed the use of a wide weight range of fish. A full description of the apparatusand experimental procedures used can be found in Duthie (1980).
The respirometer used in the swimming trials is described in Priede & Holliday(1980). It is essentially a Brett-type respirometer mounted on gimballs so that thewhole apparatus can be tilted at 0-900 from the horizontal. Tilting the respirometerovercomes the flatfishes' rheotactic behaviour to a water current (Arnold, 1969).The volume of the respirometer was 40 1.
The fish were left overnight in the respirometer in a flow of 5 cm/s before the firstswimming trials were conducted. The water velocity was then increased and thetunnel tilted (30-500 from horizontal) until swimming began. In the assessment offish swimming performance the usual technique involves stepwise increases in watervelocity. It was found that a uniformly swimming flatfish became disorientated ifspeed was changed. After each run, the water flow was reduced and the fish
Respiratory metabolism of temperature-adapted flatfish 361
20
10
eo
1 1-0
0 1
Flounders
10 10 100
Live weight (g)
1000
20 Lemon sole
10 100
Live weight (g)
500 10 10 100
Live weight (g)
500
Fig. 1. The relationship between standard oxygen consumption and body weight for the threespecies of flatfish at various adaptation temperatures. O = S °C, • = 10 °C, # = 15 °C.
to settle on the bottom of the chamber. Swimming was reinduced after 2 h at a highertest velocity (8 cm s- 1 increases). Each discrete run lasted 30 min. Critical swimmingspeeds were taken as the maximum speeds that could be sustained over a 30 minperiod. The oxygen consumption at these speeds were used as estimates of activemetabolic rates.
(3) Determination of lactic acid
Immediately on termination of a swimming trial the fish was removed from therespirometer and killed by a blow to the head. Muscle blocks (0-5 g) were cut fromthe eyed surface and frozen in liquid nitrogen. 0-5 ml of blood were sampled via thecaudal vein and precipitated in chilled 08 N perchloric acid. Lactic acid in muscleand blood was analysed using the procedures of Horhorst (1963) and Wardle (1978).Controls were resting flounders which had been undisturbed for 2 days.
RESULTS
(1) Standard oxygen consumption - weight relationships
i In Fig. 1, standard oxygen consumption values determined at various adaptationtemperatures are plotted against body weight for the three flatfish species. Regression
362 G. G. DUTHIE
Table 1. Standard oxygen consumption (Y) in relation to weight (W) at differentadaptation temperatures for the three flatfish species
(The weight range of each population can be seen from Fig. 1. Y is mg O2 h"1 and W is g.)
Species
Platichthys flesus
Limanda limanda
Microstomus kitt
Adaptationtemperature (°C)
5IS
510
IS
5IO
IS
logloglogloglog
logloglog
Regressions
Y = 0827 log W-1 -261Y = 0-812 log W— 0-941Y = 0-772 log W— 0-787y = 0-782 log w—1-014y = 0634 log w- 0-859y = 0680 log W-0-975y = 0-717 log w—0804y = 0783 log PF-0-774
r values
09880-990
09360-9650-9730-97509680-981
Level ofsignificance
P < o-oo 1P < o-ooiP < o-ooiP < o-ooiP < o-ooi
P < o-oorP < o-ooiP < o-ooi
Table 2. Mea« lengths and weights (± S.E.) 0/ the fish usedin the swimming respirometry experiments
(Each group consists of 4 individuals except for 10 °C dabs where only one individual was used.All fish were adapted to their respective temperatures for at least 2 months prior to theswimming trials.)
AdaptationSpecies
Platichthys flesus
Limanda limanda
Microstomus kitt
temperature (°C)
5IS
510
IS
510
15
Length (cm)
34-7 ±0-5829-5 ±1-3833'O±o-3327-731-310-7629-410-7929-6 + 0-2128-510-79
Weight (g)
433-S±i6'97395O + 53II
3999± 0'9°236-2395-8 + 23-4O229-4+18-31248-7! 0-78221-3117-80
lines have been fitted to the data. The equations, correlation coefficients and signifi-cance levels are given in Table 1. Interspecific comparison of regressions (Snedecor &Cochran, 1972) between equivalent temperatures in no case show significant dif-ferences in slopes or elevations (P > 0-05).
(2) Oxygen consumption - swimming speed relationships
Mean lengths and weights of the fish used in the swimming trials are given inTable 2. Fig. 2(a)-(c) shows the relationships between oxygen consumption andswimming speed for flounders adapted to 5 and 15 °C, and dabs and lemon soleadapted to 5, 10 and 15 °C. Regression equations are given in Table 3.
Included in Fig. 2 are standard rates of oxygen consumption calculated for fish ofequivalent weight to those used in the swimming trials from the weight-oxygenconsumption regressions (Fig. 1). A discrepancy exists between the extrapolatedintercepts and the calculated standard rates.
Intraspecific comparison between slopes and elevations of pairs of regressionsshow that there are no significant differences in slopes at the different adaptation^
Respiratory metabolism of temperature-adapted flatfish
w300 15°C
200
3 100
I 50a
10
(ft)
0-5 10Specific speed (Bis"1)
1-5
200
100
50
a
10
15 °C
0 0-4 0-8 1-2
200
100
50
10
10 °C
300 r 5 °C
200
2 100
I 50aE
100 0-5 10
Specific speed (Bis"1)
0 0-4 0-8 1-2Specific speed (Bl s"1)
200
100
50
5°C
" " ' I
10
363
1-5
0-4 0-8 1-2
(c)
200
T 10000
50
10
15°C
0-4 0-8 1-2
200
100
50
10
10 °C
0 0-4 0-8 1-2
Specific speed (Bis"1)
200
100
50
10
5°C
0-4 0-8 1-2
Fig. 2. The relationships between oxygen consumption and swimming speed for the threespecies of flatfish at various adaptation temperatures. In each graph the points representdeterminations on a number of individuals tested for different speeds. The dashed horizontallines are standard rates calculated from the standard oxygen consumption-weight regressions(Table 1), for fish of equivalent weight, (a) flounders, (6) dabs, (c) lemon sole.
Tab
le 3
. Res
ults
from
the
sw
imm
ing
resp
irom
etry
exp
erim
ents
(Sw
imm
ing
spee
d (X
) is
spe
cifi
c sp
eed
(bod
y le
ngth
s s-
I).
Sta
ndar
d ox
ygen
con
sum
ptio
n w
as c
alcu
late
d fr
om p
revi
ousl
y es
tabl
ishe
d w
eigh
t-ox
ygen
co
nsum
ptio
n re
gres
sion
s fo
r eq
uiva
lent
wei
ghts
of
fish
(F
ig.
I).
Sco
pe is
the
dif
fere
nce
betw
een
stan
dard
an
d a
ctiv
e ox
ygen
con
sum
ptio
n (F
ry, 1
947)
. In
terc
ept
is t
he
valu
e de
rive
d fr
om e
xtra
pola
tion
of
the
oxyg
en c
onsu
mpt
ion-
swim
min
g sp
eed
regr
essi
on (
i.e.
anti
log
of t
he
regr
essi
on c
onst
ant)
. 'P
ostu
re e
ffec
t' is
the
int
erce
pt m
inus
sta
ndar
d ox
ygen
con
sum
ptio
n (P
ried
e &
Hol
lida
y, 1
980)
.)
Tem
pera
- tu
re (T
)
5 1.5 5
I0
15
5
I0
1.5
Cri
tica
l S
tand
ard
Act
ive
swim
min
g 'P
ostu
re
rate
ra
te
spee
d S
cope
In
terc
ept
effe
ct'
(mg
kg-'
h-')
(mg
kg-'
h-')
(B 1
s-')
(mg
kg-'
h-')
(mg
kg-'
h-')
(mg
kg-
' h-
') S
wim
min
g re
gres
sion
r
P
Pla
ticht
hys f
lew
s 61
.57
92'9
1
Lim
anda
lim
anda
58
.88
68.7
4
91'7
1
Mic
rost
omrr
s kit
t 5 3
'46
66.7
8
85'2
7
log
Y =
0.2
02 X+ I
~7
89
log Y =
0.2
40 x+ I
~9
68
log Y =
0.2
1 I X+ I
.770
log
Y =
0.2
68 X+ 1
.837
log Y =
0.2
09 X+ 1
-962
log Y =
0.2
93 X+ 1
.728
log Y =
0.3
42 x+ 1
.825
log Y =
0.3
01 X
+ 1
.931
Respiratory metabolism of temperature-adapted flatfish
250
•T 200
g 150
o•a
I 100(A
8O 50
Flounders
5 10 15
Temperature (°C)
2-5
2-0
1-5 £
10 £
0-5
250
V 200
I 15°jI 100
O 50
Lemon sole 2-5 250
20
1-5
10
0-5
0
200
150
100
50
0
Dabs
20
1-5
10 %8.
0-5
05 10 15 5 10 15
Temperature (°C)
Fig. 3. Effect of adaptation temperature on the active metabolic rate # , critical swimmingspeed O, intercept of the oxygen consumption-swimming speed regression A, and thestandard oxygen consumption • , for the three species of flatfish.
temperatures (P > 0-05). The elevations between compared pairs differ significantly(P < c-05). Interspecific comparisons of the regressions between equivalent adapta-tion temperatures show no significant differences in slopes or elevations (P > 0-05).
Values for critical swimming speeds and active metabolic rates are presented inTable 3. These values are plotted against temperature in Fig. 3. along with thecalculated standard rates and the intercepts of the oxygen consumption-swimmingspeed regressions. The maximum levels of oxygen consumption for the three speciesincrease with temperature. For dabs and lemon sole there is a relative reduction in
^his value at 15 °C. The maximum sustained speed for lemon sole declines at 15 °C.
366 G. G. DUTHIE
500 r . Flounder
400
o" 300
o 200
o100
^ , 15 °C
„ - . 5°C
500
~ 4006
O 300
&
8 200
100
Dab
0-5 10 1-5 20 2-5Specific speed (Bl s"1)
500
400
O 300
30
^ - 10 °C.T - " 15 °c
J"_~J" - 5°C
8 200
100
0
Lemon sole
10 °C' 1 5 ° C
5°C
0 0-5 10 1-5 20 2-5 0-5 10 1-5 2-0 2-5 3030 0Specific speed (Bl s"1)
Fig. 4. The total cost of swimming per kilometre for different swimming speeds for the threeflatfish species at the adaptation temperatures. Cost was calculated from oxygen consumptionvalues obtained from the oxygen consumption-swimming speed regressions (Table 3). Thedashed lines indicate where cost has been calculated from extrapolation of the regressions.The arrows indicate the maximum sustained swimming speeds observed in the respirometer.
(3) The cost of locomotion
Fig. 4. shows the total aerobic cost of swimming (including standard costs) perkilometer at different swimming velocities for the three species. Total cost per unitdistance was calculated using the oxygen consumption-swimming speed relationships(Table 3) using the formula:
Y(x)C(x) =
Xwhere Y(x) is the rate of oxygen consumption at velocity X. Specific speed wasconverted to km h"1 using the mean lengths of the fish in each group (Table 2).
Fig. 4 shows that the aerobic cost of swimming remains low over a range of swim-ming speeds. By extrapolating the oxygen consumption-swimming speed regressionsbeyond the maximum observed speeds, the lowest costs are incurred at speedyaround or in excess of the maximum recorded speeds in the respirometer.
Respiratory metabolism of temperature-adapted flatfish 367
100
80
Mo22 60I•a•32 403
20
Muscle
0-5 0-75 10
Specific speed (Bl s"1)
1-25
—0 Blood
1-5
Fig. 5. Changes in lactic acid in flounder muscle and blood in relation to swimming speed.Trials were conducted at 15 °C. Each point represents the mean + s.E. from samples from sixindividuals. Samples were taken immediately on conclusion of a swimming trial.
(4) Lactic acid accumulation
Initial experiments showed that blood and muscle lactic acid levels in the flounderrose after handling. Within 5-8 h values returned to resting levels. In practice, fishwere left overnight in the respirometer before swimming trials were conducted.
The results of the swimming experiments are shown in Fig. 5. Each point on thegraph represents the mean + S.E. of six individuals. Blood lactic acid levels remainsmall relative to the increase in muscle lactic acid. The relationship between musclelactic acid and swimming speed can be described by:
log L — 0-151 X+ 1-650 (r = 0-916, P < o-oi),
where L is concentration of lactic acid in mg/100 g tissue and X is swimming speedin body lengths s-1.
Assuming that 45 % of the total weight of a flatfish is white muscle, (I. G. Priede,pers. comm.), and that the difference between resting lactic acid levels and levels atany particular swimming speed are a consequence of activity alone, the contributionof aerobic and anaerobic factors to the total energetic mobilisation during activity canbe estimated by converting oxygen consumption and lactic acid production to theirequivalent of ATP produced. The conversion factors given in Bennett & Licht (1972)were used. Details of calculations are in Duthie (1980). The aerobic and anaerobicexpenditure for a standard 250 g flounder at a variety of swimming speeds is given inTable 4. For all speeds considered, the anaerobic contribution to the total energyfcpenditure is relatively constant.
368 G. G. DUTHIE
Table 4. ATP production (mmol ATP 250 £ animal*1 h~l)from aerobicand anaerobic sources for flounder at selected swimming speeds at 15 °C
Swimmingspeed (B 1 s"1)
o-so-75I'001-251'40
Aerobic ATPproduction
3-844695666797'54
Anaerobic ATPproduction
0-650841-031-25i-39
DISCUSSION
Total ATPproduction
4'49S'S2670803892
Anaerobiccontribution (%)
1461 5 115-4•15-5IS-S
(1) Standard oxygen consumption of flatfish and roundfish
Flatfish metabolic rates have been found to be low in comparison to more activespecies (Wood et al. 1979; Priede & Holliday, 1980). The standard oxygen consump-tion values of the three species in the present study have been plotted against tempera-ture, along with measurements reported in the literature for other flatfish and roundfishspecies, in Fig. 6. In view of the number of records available, only data for salmonidsand marine pelagic species have been used as representative of active roundfish.All data have been adjusted to a standard 250 g animal using an exponent of o-8(Winberg 1956), unless values were given in the studies.
Assuming a semilogarithmic transformation comes closest to linearising such data(Brett 8c Groves, 1979), the regression equations are
Flatfish: log Y = 0-036 T + o-6oo (r = 0-777, P < o-ooi)Roundfish: log Y = 0-038 T +0-743 (r = °'&5h P < 0001)
where Y is mg 02 h"1 and T is temperature in °C.In Fig. 6, values for two species of tropical flatfish (nos 16 & 17) were excluded
from the line-fitting procedure. They may show a marked metabolic compensation totemperature (Edwards et al. 1970) in a manner analogous to the reputed phenomenonof cold-adaptation observed in certain high latitude ectotherms (Holeton, 1974).
There is no significant difference in slopes of the above regressions (P > 0-05).A significant difference exists between the elevations (P < o-oi). Flatfish havea significantly lower standard metabolism over the temperature range considered.This may reflect the relatively inactive lifestyle of flatfish. During sedentary periodson the sea bottom, a low standard metabolism would allow a saving in basic main-tenance costs.
(2) Oxygen consumption-swimming speed relationships
The range of coefficients describing the rate of increase in the logarithm of oxygenconsumption with specific swimming speed for the flatfish in the present study(Table 3) fall within that for other fish species (see Beamish, 1978). Comparisonbetween the coefficients for each flatfish species at different adaptation temperaturesand also interspecific comparison between equivalent thermal regimes show qfl
Respiratory metabolism of temperature-adapted flatfish 369
40
30
Ico
••§. 1 0E
(a) Flatfish species
14 i /
0 5 10 15 20 25 30
Temperature (°C)
5040
30
20
10
2
1
• (b)
•
10
t /
/
u
9
Roundfish species
V i
; /
j / *
Ai I
. / i
/
121
- 5 0 5 10 15 20
Temperature (°C)
25 30
Fig. 6. The standard oxygen consumption of a number of fish species in relation to tempera-ture, (a) flatfish, (6) roundfish. All values are for a 250 g standard animal. Flatfish:(1) Platichthys flesus (present study), (2) Limanda limanda (present study), (3) Microstomuskitt (present study), (4) Platichthys stellatus (Hickman, 1959), (5) Parophrys vetulus (Hickman,1959), (6) Citharichthys stigmaeus (Hickman, 1959), (7) Pleuronectes platessa (Priede &Holliday, 1980), (8) Platichthys stellatus (Wood et al. 1979), (9) Pseudopleuronectes americanus(Cech et al. 1975), (10) Platichthys stellatus (Watters & Smith, 1973), (11) Pseudopleuronectesamericanus (Voyer & Morrison, 1971), (12) Pleuronectes platessa (Edwards et al. 1969),(13) Pseudopleuronectes americanus (Rowell et al. 1975), (14) Pleuronectes platessa (Edwardset al. 1970), (15) Pleuronectes platessa (Edwards, 1971), (16) Cynoglossus sp. (Edwards et al.I97i)» ('7) Brachirus sp. (Edwards et al. 1971), Note, numbers 16 and 17 are marked • toindicate exclusion from the line fitting exercise. Roundfish: (1) Oncorhynchus nerka (Brett,1964)1 (2) Salmo trutta (Beamish, 1964), (3) Salvelinus fontinalis (Beamish, 1964), (4) Salmogairdneri (Stevens & Randall, 1967), (5) Salmo gairdneri (Webb, 1971), (6) Pollachius virens(Tytler, 1978), (7) Melanogrammus aeglefinus (Tytler, 1978), (8) F. Cottidae (Holeton, 1974),(9) F. Cyclopteridae (Holeton, 1974), (10) Boreogadus saida (Holeton, 1974), (11) F. Zoarcidae(Holeton, 1974), (12) Oncorhynchus kisutch (Averett, 1969), (13) Gadus morhua (Edwards et al.1972).
significant differences. The overall oxygen consumption-swimming speed relation-ships for flatfish are similar and independent of adaptation temperature. The elevationsof the regressions are significantly altered. It is energetically more expensive to swimat the higher temperatures.
Both standard and active metabolic rates of the flounder approximately double forthe 10 °C increase in temperature (Table 3). Relatively, the increase in active meta-bolism is greater and thus scope increases with increase in adaptation temperature.The relative reduction in active metabolic rate in dabs and lemon sole at 15 °C(Fig. 3) may indicate the critical temperature for these species, whereby the energydemands of ventilation and associated circulation become excessive, restricting in-
370 G. G. DUTHIE
creased supply of oxygen to tissues (Jones, 1971) and/or oxygen itself becomes Ia respiratory limiting factor (Brett, 1964; Fry, 1971). The relative reduction incritical speed at 15 °C may also be due to this.
A discrepancy exists between the extrapolated intercepts and standard rates for allthree species. Priede & Holliday (1980) found a similar discrepancy for plaice andsuggest that it represents the power requirement for lift-off which they term the'posture effect'. The situation is analogous to that observed in a number of mammalswhen running is initiated from a resting position (Schmidt-Nielsen, 1972). Baudinette(1978) suggested that such differences also include an 'excitement factor' as well as anincrement due to increased power requirements. An excitement component wouldhave a relatively greater effect at the lower swimming speeds, causing a correspondingreduction in the slopes of the oxygen consumption-swimming speed regressions.Although it is not possible to state exactly how the difference between intercept andstandard rate is partitioned into the power requirement for lift-off and ' excitement',the data in Fig. 2 (a)-(c) demonstrate that the common method of assessing thestandard metabolism of fish, that is the extrapolation of the oxygen consumption-swimming speed relationship to zero swimming speed (Fry & Hochachka, 1970)does not apply to flatfish.
(3) The cost of locomotion -possible swimming strategies
The cost of locomotion calculations (Fig. 4) indicate that the optimum swimmingspeeds and the maximum sustainable swimming speeds for the three species correlateclosely. By calculating the costs beyond the range of the original oxygen consumption-swimming speed regressions it appears that the most economical speeds may occur atspeeds greater than the critical speeds. This implies that the aerobic scope of theseflatfish may be insufficient to allow them to swim at what is theoretically their mostoptimum swimming velocity. To attain these speeds may involve the use of anaerobicmetabolism. Plaice have been observed to swim continuously at 0-9-2-0 body lengthss-1 for 05 h with long periods of rest between swimming phases (Greer-Walker et al.1978). If anaerobic metabolism was being employed, these rest periods would allowthe repayment of the oxygen debt.
A flounder, for example, swimming at 2-0 body lengths s - 1 at 15 °C would theoreti-cally consume 28067 m g 0 2 • kg"1 h"1 (from extrapolation of the oxygen consumption-swimming speed relationship). The maximum rate of oxygen consumption that wasobserved was 214 mg O2.kg-1 h"1, leaving a deficit of 65-69 mg 02.kg"1 h-1.Anaerobic swimming involves the metabolism of muscle glycogen to lactic acid,which releases 558 Jg"1 glycogen (Priede & Holliday, 1980). Fish white musclecontains about 1 g glycogen 100 g"1 muscle (Wardle, 1975). Approximately 45 % ofthe weight of a flounder is myotomal muscle giving a total glycogen store of 4-5 g kg"1,or 2511 J energy store. Aerobic metabolism releases 22-5 J mg 0 2
- 1 consumed(Priede & Holliday, 1980), so the deficit represents a power requirement of 1478 Jkg"1 h-1. If the anaerobic metabolism of muscle glycogen was used for this deficit,the fish could swim for 2511/1478 = 17 h at 2 body lengths s"1 before all theglycogen reserve was exhausted. This calculation assumes that the animal in its naturalenvironment cannot increase its oxygen consumption above the maximum recorded^
Respiratory metabolism of temperature-adapted flatfish 371
fin the respirometer. However, it does indicate that glycogen stores are sufficient tomaintain a low level of anaerobic metabolism for a prolonged period. A similarcalculation for the plaice indicates that this fish could swim at 2 body lengths s"1 for1-23 h before exhaustion (Priede & Holliday, 1980). It is not unreasonable to assumethat as well as the plaice, other flatfish species have movements characterised byalternating swimming and resting phases. Therefore, the use of 'supercritical'swimming speeds with associated build up of oxygen debts is a plausible strategy.
(4) Anaerobic metabolism at moderate swimming speeds
Priede & Holliday (1980) consider that the white muscle of the plaice works onlyat high speeds. The elevated lactic acid levels in flounder white muscle (Fig. 6) indicateit is operating anaerobically at moderate speeds. The white muscle of a number offish species is utilized at swimming velocities other than burst activity (Black et al.1962; Greer-Walker & Pull, 1973; Hudson, 1973; Johnson & Goldspink, 1973;Wokoma & Johnson, 1981).
When the total energy contributions of aerobic and anaerobic processes in theflounder are assessed as ATP produced, the anaerobic contribution is 15% of thetotal energy expenditure for all speeds examined (Table 4). Comparable data forother fish species is lacking although rainbow trout swimming at 3-5 body lengths s- 1
may initially employ at least a 38% anaerobic contribution (Wokoma & Johnston,1981). The cost of swimming calculations (Fig. 4), which are based on aerobic con-siderations alone, would appear to be inadequate indicators of the energy requirementsof sustained locomotion in the respirometer.
It should be noted that the assessment of aerobic and anaerobic metabolism in theflounder during swimming is based on a number of assumptions: (a) that lactic acidis the only end-product of anaerobic metabolism; (b) that phosphocreatine is notutilized or synthesised during swimming; (c) that the P/O ratio is 3; (d) that lacticacid formed during exercise is neither excreted nor re-utilized during swimming.
The first three assumptions have been discussed elsewhere (e.g. Wood et al. 1977;Bennett, 1978; Carey, 1979; Hochachka, 1980; Duthie, 1980). Concerning the lastassumption, Wardle (1978) provides evidence for the retention of lactic acid accumu-lated during strenuous activity by the white muscle of the plaice. The low bloodlactic acid levels in the flounder immediately after exercise (Fig. 5) suggests a similarphenomenon.
It is difficult to extrapolate the results of this laboratory study to what may occurunder natural conditions. The increase in lactic acid as speed increases may be anartifact of the experimental apparatus. White muscle may be employed to provideorientation as turbulence increases in the water tunnel. On the other hand, movementover short distances with accumulation of anaerobic end-products would be of littleinconvenience to a flounder which spends a large percentage of its time on the sub-stratum, and thus could easily pay off any accrued oxygen debt. Movement overgreater distances, e.g. during migration, may be achieved by very rapid burst swim-ming, with long rest periods to restore depleted glycogen reserves. The use of selectivetidal transport may also aid migration (Priede & Holliday, 1980). Periods of restJ^ould occur when the tidal currents are in an adverse direction.
372 G. G. DUTHIE
In comparison to salmonids the active metabolic rates and critical swimmingspeeds of flatfish are low. Thus despite the relatively low standard metabolic rates offlatfish (Fig. 5), the aerobic scopes are small, e.g. less than 20% of the sockeyesalmon in Brett's (1964) study. Thus the total amount of oxygen available to thelocomotory muscles of flatfish is relatively small. It is, perhaps, not surprising thatduring swimming, the aerobic metabolism of flatfish is supplemented by anaerobicmetabolism. It may even increase the range of speeds at which the fish is able toswim (Wokoma & Johnston, 1981).
My thanks to Dr D. F. Houlihan and Dr I. G. Priede for valuable support and forcriticism of the manuscript. This work has been accepted in partial fulfilment forthe degree of Ph.D. at the University of Aberdeen. Financial assistance was from theS.R.C. whilst in receipt of a studentship. Professor G. M. Hughes made helpfulcomments.
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