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An experimental study of the oxygen consumption, growth, and metabolism of the COD (Gadus Morhua L.)
Jr. exp. mar. Biol. EcoL, 1972, Vol. 8, pp. 299-309; ~ North-Holland Publishing Company
AN EXPERIMENTAL STUDY OF THE OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD (GADUS MORHUA L.) R. R. C. EDWARDS,D. M. F!NLAYSONAND J. H. STEELE, Marine Laboratory, Aberdeen, Scotland
Abstract: The rate of oxygen consumption of cod in sea water at 12 °C containing MS222 (25 mg/l) can be expressed as: Qez = 0.245 W°.S2(mg/h), where W is the live weight of the fish (g). The maximum efficicncy of conversion of assimilated food into growth was 24 Yo during the feeding experiment. Digestion efficiencies were estimated at over 98 % using fillets of plaice as food. The effect of increasing the rate of food intake was to increase liver weight and condition factor. The relative proportions of protein and lipid in ~he body did not change over the range of feeding levels used. The conversion efficiency had a maximum value at an intermediate feeding rate.
INTRODUCTION
The experiments described in this paper are part of a marine food chain study being conducted in Loeh Ewe, Scotland. Previous investigations (Edwards & Steele, 1968) have shown that in this area at certain seasons the cod is an important predator on the populations of juvenile plaice (Pleuroneetesplatessa L.)so that further information on the food requirements of the cod becomes necessary. Earlier studies have been made on the respiration of the cod (Sundnes, 1957; Saunders, 1963) but they give no information on the effect of feeding level on meta.bolic rate. In the present study the dependence of oxygen consumption on body weight was ,.'nvestigated and this has provided the basis for a detailed analysis of the results of the feeding experiment. MATERIAL AND METHODS
Cod were caught with hand lines in shallow water at Stonehaven, Scotland. They were transported to Loch Ewe in W.nks supplied with gaseous oxygen diffusers. Mortality was negligible. The feeding experiments were conducted in large fib:'e glass tanks (1.8 x 3.7 x 1.2 m deep) connected to a fresh sea-water supply. Each tank was divided by small mesh netting into four compartments, and individual fish were placed in each compartment. A raised platform of rock allowed each fish to conceal itself and served to prevent unnecessary excitement as a result of disturbance. Weighed daily rations of plaice fillets were given to the cod and each fish was weighed monthly after anaesthetization by immersion in sea water containing MS222 (Sandoz) at 25 mg/I. Oxygen consumption was measured at 12 °C in a closed circuit respirometer incorporating a Beckman 777 oxygen electrode (Edwards, FinIayson & Steele, 1969). The use of anaesthetics to induce a 'constant' (resting) rate of oxygen consumption 299
300
R . R . C . EDWARDS, D. M. FINLAYSON AND J. H. STEELE
was demonstrated by McFtrland (19.59). The oxygen level which is critical for oxygen consumption in the cod is ~ 3 mg/l at 10 °C (Saunders, 1963) and, as Hughes (1964) has shown, oxygen uptake, is inhibited below this critical level. Care was taken, therefore, that the oxygen levels in the respirometer were well above this. Analyses for protein, carbohydrate, lipid and ash were made according to the methods given by Edwards, Finlayson & Steele (1969). The analyses of the fish were made e,fter homogenization of the whole body. To obtain faecal material, the fish were transferred for known periods to smaller tanks, .nd faeces collected by pipette. RESULTS RATE OF OXYGEN CONSUMPTION
The results obtained at 12 °C are shown in Fig. !. The oxygen uptake, Q,2 (mg/h) expressed as a function of the: live weight, W (g), is given by, Qoz - 0,245 W °'Sz with a S.E. for the exponent of 0.82_+0.035. The power constant 0.82 compares with the value of 0.80 proposed by W!aberg (1956) and is near the mean of the values I00
E
_.9. K
j"
I0
P
o U e.
I ..................
I
!0 Live
I00 W~lght
I
ICX:X:)
(g)
Fig. 1. Oxygen consumption as a function of live weight (log-log scales).
ranging I~etween 0.791 (starved) and 0.886 (fed) and given by Saunders (1963) for cod. Sun¢:nes (1957) gave values for cod and saithe of about 0.71. The rate of o×ygen consumption, i,gasured here at 12 °C, lies midway between the rates for starved and fed cod at 10 °C give,~ by Saunders (1963). The oxygen consumt'tion during anaesthetisation may be taken as a basal rate. Since, however, in the tank experiments the average temperature during the main
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
301
feeding period was ~ 16 °C, a correction may be applied using the Q1 o value of 2.48 found for 500 g cod at temperatures between 10 and 15 °C by Saunders (1963). After conversion to cal/h assuming that 1 mg of oxygen is equivalent to 3.38 g. cal (Winberg, 1956; Palohe~mo & Dickie, 1966) the standard metabolic rate is, Q = 1.00 W °'82 at 16 °C. BIOCHEMICAL ANALYSES
To convert the weight of fish, food, ~nd faecal materials in the feeding experiment into their caloric equivalents, analyses were made of protein, carbohydrate, lil:!d, and ash contents (Edwards, Finlayson & Steele, 1969). Mean values are given.i~: Table I. Two cod analysed at the start of the feeding experiments had an average T^BLv i Biochemical analyses: all values mg/100 mg dry weight. MeIin
Carbo.
Sample I, 2. 3. 4.
Cod (starting control) Cod (end of experiment) Plaice fillets Cod faece~
calorific
Protein
Lipid
hydrate
Ash
74.8 7~.2 85.6 31.5
5.8 5.3 7.6 4.1
1.1 0.8 0.8 2.5
18.5 18.8 5.9 62.00
value, kcal/g dry wt 4.82 4.82 5.63 3.09
calorific value of 4.82 k cal/g dry weight and this did not differ significantly from the experimental fish analysed at the end of the experiment. The higher calorific value of the plaice fillets was clue to their lower ash content since they contained little skeletal tissue. The dried faecal material averaged 2.3 % of the dry weight of the food, and had a caloric content of about 3.1 kcal/g dry weight. Thus the calorific content of the faeces produced was 1.3 % of the food intake. This indicates that the efficiency of absorption of the energy in the food was 98.7 %. This may be an over-estimate because the faecal material produced by the cod was of very fine texture, and although care was taken to collect all of this, some may have been lost as a fine suspension in the water. It should be noted, however, that Pandian (1967) estimated the efficiency of absorption of protein in the euryhatine fish Megalops cyprinoides to be as high as 98.3 %. Cod is assumed to be predominantly ammonotelic. Any significant excretion of urea would decrease the energy assimilated by the fish but increase the growth efficiency slightly. This would not affect the general conclusions. FEEDING EXPERIMENT
Fluctuations in water temperature during the 110 day~ of the feeding experiment are shown in Fig. 2. Apart from a brief increase during a period of warm weather in August when the temperature reached 19 °C, the temperatures were in the region of 14 to 16 °C, with a steady decline in October.
302
R. R, C. EDWARDS, D. M. FINLAYSON AND J. H, STEELE
The change in live weight of the 16 fish used in the experiment are shown in Table II, together with the fresh weight of plaice fillets consumed. (The tanks are numbered 5-8.) The results were converted into dry weights and thence into kcal, assuming that 1 g dry weight of protein is equivalent to 5.7 kcal, of lipid 9.5 kcal and of carbohydrate 4.2 kcal (Brody, 1945). Energy used for metabolism was esti~nated by subTABLE 11 Results of feeding experiment in large outdoor tanks: tanks numbered, 5-8; individual compartments, 1-4.
Fish no.
Live weights (g) lnit. Final
Fresh weight food
Growth
Food
Faeces
(kcal)
(kcal)
(kcal)
(kcal)
Metabolism
Conversion efficiency
(%)
(g)
0-33 Days 5)
6)
7)
~)
I 2 3 4
309,0 310,0 160.0 238,0
264.5 313,5 183,0 333,0
38,7 93.4 51.0 317.5
0 3.91 26,87 92.05
50,66 122.22 66.77 415.62
0.66 1,60 0.88 5.46
91,85 116.71 38,98 318.11
I 2 3 4
253.0 184.0 400,0 566.5
396.0 183.0 585.0 531,0
443.4 25.7 587.2 73.4
160.70 0 205.98 0
580.47 33.65 768.83 96.13
7.62 0.44 10.09 1.26
412.60 34.17 552.72 132.33
1 2l 3 4
457.3
466.0
129.9
13.70
170.18
2.39
154.08
8.17
610.5 512.0
572,0 679.0
76.4 650.5
0 182.08
98.31 851.64
1.29 11.18
139.96 658.37
21.66
~ 2 32 4
54.2.0 445.0 452.2 670.0
480.0 385.0 406.5 629.5
64.4 54.8 38.8 132. I
84.42 71.71 186.73 172.98
!.! ! 0.94 6.65 2.27
154.03 133.14 232.55 216.03
0 0 0 0
3,24 40.80 22.40 28.03 27.15
34-65 Days 5)
6)
7)
8)
I 2 3 4
264.5 313.5 183,0 333.0
252.0 378.7 190. I 439,5
43.5 145.0 58,0 245.4
0 72.08 8.29 103.19
59.95 197.20 79.94 575.14
0.75 2,49 ! ,00 7,17
70.96 122.63 70,65 464.77
I 2 3 4
396,0 183,0 585.0 531.0
546.0 172.5 741.2 525,0
328.1 22.4 363.0 83.9
168.56 0 173.90 0
769.02 30.87 850.79 114.10
9,59 0,38 10.60 !.44
790.87 40.47 666.29
I 2 3 4
466.0 596.0 572.0 679.0
541.6 525.5 577.0 773.6
217.5 68.0 I 16.0 296.4
81.41 0 5.58 103. ! 3
299.79 93.73 157.76 685.5
3,74 I.I 7 1.99 8.66
214.64 147,66 150.19 573,71
3.58 15.24
! 2 32
480.0 385.0
489.7 390.7
124.7 I 16.0
11.02 5.90
171.88 159.89
2.14 !.99
158.72 15t .99
6.49 3.74
4
629.5
756.5
348.0
142.10
479.67
5.98
331,59
29.99
37.02 10.50 18.17 22.19 20.70
118.99 27.50
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
303
TABI~ II (Contd.)
Fish no
Live weights (g) lnit. Final
Fresh weight food
Growth (kcal)
Food (kcal)
Faeces (kcal)
Metabolism (kcal)
Conversion efficiency (~)
(g) 66-96 Days 5)
1 2 3 4
252.0 378.7 190.1 439.5
264.0 423.5 213.5 490.5
62.5 ! 50.5 75.0 i 13.5
11.29 49.57 27.38 49.36
84.51 203.5 101.4 260.95
1.07 2.58 1.22 3.32
72.15 15 !.34 72.73 208.27
13.53 24.67 27.35 19.16
6)
I 2 3 4
546.0 172.5 741.2 525.0
612.0 171.5 744.0 525.0
155.2 37.5 100.6 87.5
73.97 0 3.13 0
356.82 50.71 231.33 118.31
4.53 0.66 2.94 1.50
278.31 51.01 225.26 116.81
20.99 1.37 -
7)
I 2 3 4
541.6 525.5 577.0 773.6
586.0 538.0 611.5 863.5
187.5 i 12.5 ! 25.0 225.0
47.82 11.63 38.47 98.43
253.53 152.12 169.02 517.44
3.22 1.93 2,15 6.57
202.48 138.55 128.40 412.43
19.10 7.74 23.05 19.27
8)
I 2 3 4
489.7 390.7 406.5 756.5
528.4 412.0 435.0 893.0
137.5 125.0 112.5 350.0
44.15 22.16 30.05 152.73
185.92 169.02 152.12 473.26
2.36 2.15 1.93 6.01
139,41 144.71 120.08 314.51
24.05 13.28 20.01 32.69
97-116 Days 5)
1 2 3 4
264.0 423.5 213.5 490.5
266.7 459.5 227.7 478.5
57.0 114.0 57.0 169.9
2.52 39.36 16.60 0
81.26 162.52 81.26 411.9
0.98 1.96 0.98 4.96
78.64 121.20 64.56 418.51
3.10 24.51 20.45 -
6)
I 2 3 4
612.0 171.5 744.0 525.0
708.5 168.5 824.0 517.5
210.9 38.0 218.6 95.0
158.64 0 89.08 0
511.5 54.17 538.94 i 35.44
6.16 0.65 6.39 1.63
346.07 56.38 443.47 141.00
31.39
1 2 3 4
586.0 538.0 611.5 863.5
604.5 543.5 606.5 953.3
! 52.0 95.0 76.0 249.0
19.92 5.12 0 97.8~
216.7 135.44 108.35 603.71
2.61 1.63 1.31 7.28
194.17 127.96 ! 12.61 498.55
9.30 3.85 16.41
I 2 3 4
528.4 412.0 435.0 893.0
544.5 416.0 440.0 952.8
104.5 ! 04.05 114.0 266.0
18.41 4.24 9.50 66.85
148.98 143.33 162.52 379.22
1.80 1.79 1.96 4.60
128.77 151.38 151.08 307.67
12.51 5.92 17.84
7)
8)
16.73
t D i e d at 22 days and was replaced. 2 Not weighed at 33 days; values are for 0-65 days.
tracting the calorie; utilized for growth and in the faecal material from the total food intake during a given period. The efficiency of cmwersion expresses the percentage of assimilated food laid down as growth. During the initial 33 days an attempt was made to feed 8 of the fish a maintenance diet, but the feeding level was below maintenance and the fish lost weight. In addition,
304
R.R.C. EDWARDS, D. M. F[NLAYSON AND J. H. STEELE ~
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Fig. 2. Average daily temperature in the experimental tanks. the fish numbered 5 (4), 6(1), 6(3) and 7 (4) in Table II were fed an excess diet throughout the course of the experiment. Uneaten food was collected, dried and weighed.
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~ood tntok. (~IO) Fig. 3. T h e relation o f food intake to growth (a) and m e t a b o l i s m (b). ( O , 18.?-18.8; C), 19.8-18.9; × , 19.9-13.10; A , 14.10-13.11).
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
305
The estimated efficiencies of conversion of assimilated food into growth for fish above maintenance averaged 21.63 % in the first period (0-33 days), 17.74 ~ in the second 04-65 days), 19.03 % in the third (66-96 days), and 14.73 ~o in the fourth (97-116 days). Juvenile fish normally show higher conversions than this (Pandian, 1967, 1970; Birkett, 1969): however conversion efficiency usually declines with age (Gerking, 1952; Pandian, 1967)and so these values for 2-3-year old cod are probably of the right order. The effect of feeding level on growth rate is shown in Fig. 3 .. Both growth rate and food intake, expressed as cal/h, were divided by Q, the standard metabolic requirement, to eliminate the effects of different fish sizes and hence intensities of metabolism. It may be seen that the relationship is not linear; but it can be fitted by the equation relation G/Q = (~'.106+0.534 log F/Q. The value F/Q = 1 corresponds to a feeding rate providing energy at the same rate as the metabolic rate determined from the respiration experiments. This feeding rate gives a small positive growth rate in the tanks, indicating that, as might be expected, the fish in the tanks do not respond in exactly the same way as those in the respirometer. As the feeding rate increases the growth rate also increases but at high feeding rates this increase is small. In consequence, the conversion, or gross growth efficiency expressed as G/F hasa" maximum value at an intermediate feeding rate. Similar results have been found in freshwater fish culture (Hastings, 1969). For the cod used here, this feeding rate has a value of F/Q of 2.2 and the maximum efficiency is 24 ~. Since growt~ accounts for less than a quarter of the food, this curvilinear relation between growth and food intake is not appaient when metabolic rate is plotted as a funcdon of food intake (Fig. 3b). Thus, within the limits of error of these results, metabolic rate appears proportional to food intake. THE EFFECT OF FEEDING LEVEL ON BIOCHEMICAL COMPOSITION
The analyses of the fish at the end of the feeding experiment were related to the mean feeding level. In Fig. 4 the total protein and lipid are expressed as percentages of the caloric content of the body and plotted against feeding level. It would appear
0
~ O ~ O ~
'if
6~ I
-
O~
gO
aJ?"
eo
J I
I<,
2
.
i
3
._
J
4
Food I~k= (.F/Q) Fig. 4. Lipid and protein content in relation to the food intake.
306
R.R.C.
E D W A R D S , D. M. F I N L A Y S O N A N D J. H. S T E E L E
that the body compositic ~ remained fairly constant over the observed feeding range and that protein comprised between 88 and 90 % and lipid about 10 % of the total caloric content. The remainder was carbohydrate. An analysis of the livers at the end of the experiment gave mean values of 47.7 % protein. 31.4 % lipid and 8.8 % carbohydrate. It was calculated that about 5.3 % of the total body lipid was stored in the liver. THE EFFECT OF FEEDING LEVEL ON CONDITION FACTOR AND LIVER WEIGHT
Conditon factor (K) is usually given as, wt(g)x 100/(length, cm) s. The condition factors of the fish ranged between 0 71 and 1.91 at the end of the feeding experiment and, as shown in Fig. 5a, varied with feeding level. When the feeding level was in |*3
"*
5
w
3
-
4J
.gy
I.I -
~
X
1,0 -
o
~e
X
v
! .x.
~o.~
-
G 0 U
0"8 -
X Xx
X .J
oo X
I "
/O0 • ~l~,e ql qlt
/°o
0.7 ..... X qt~'
I
--'2
' 3
, I 4
,I 5
, I 6 Food
0 Int o k e
:
_ a I
I 2
,
I,,, 3
I 4
(, F I Q )
Fig. 5. Condition factor as a function of food intake ( × , 18.9; O, 13.11) (a) and final liver weight as a function of food intake (b).
excess of three times the standard metabolic requirement, the fish developed a thickening o" the lateral musculature, particularly near the tail, which resulted in irregular and apparently difficult swimming. A series of length and weight measurements taken midway in the experiment ga.ve values of 0.70 to 1.25. Condition factors for a sample of 2-year old cod taken in July 1968 from the smae sea area as these fish had a mean of I. 17 (West, pers. comm.). The liver weight expressed as a percentage of the body weight increased with feeding level (Fig. 5b). THE EFFECT OF TEMPERATURE ON MAXIMUM GROWTH RATE
Since Tyler (1970) has ~hown that the gastric digestion of 2~year old cod proceeds most rapidly at 15 °C and declines at higher and lower temperatures. The rates of food intake observed in these experiments may be close to the maximum for this
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
307
species. A supplementary experiment during December when the water temperature was between 6 and 8 °C gave daily rates ofweight increase for four cod of!ess than 0.075 when fed excess rations; this is considerably less than those at the higher temperatures, so that temperature was probably limiting food intake and growth. DIscussION
There is good agreement between the values of oxygen consumption in these experiments and those of Sundnes (1957)and of Saunders (1963). The measurements of standard oxygen consumption made by Tytler (1969) on gadoid fish suggest that all these earlier values approximate to a routine rate. Our results demonstrate the dependence of metabolic rate on the rate of food intake. It is likely that ~he energy requirements for activity remained fairly low, since it was observe,t that most of the fish remained hidden during the daylight hours, though they emt-rged at night. The constancy of the calorific values of the fish at different feeding levels, together with constancy of protein and lipid content is of some interest. Apparently energy is not stored aslipid in the cod, as was found by Menzel (1960) for Bermuda reef fish. It would appear that any foo'~ consumed in excess of maintenance is laid down partl~ as liver growth but mainly as an increase in size of the lateral and tail muscles, which results in an increase in the condition factor: similar results have been obtained for other gadoids (Jones & Hislop, 1971). A condition factor of I. 17 for the natural population from which the experimental fish were taken suggests that their feeding level was at least twice the standard metabolic requirement estimated from this experiment. In addition, the activity necessary to secure food in t~e ~ a may result in some extra energy demand. Is is of interest that this intake level is approximately the same as that which gave maximum conversion efficiency in the feeding experiments, suggesting that the natural population could be operating close to this maximum. The observed, lower efficiency for lower experimental rates of feeding is according to expectation. The decrease at high levels of feeding may be related to the fact that the weight increase occurs as increased musculature rather than as an i: ~rease in length. The relation between rates of growth, metabolism and food intake derived from the results does not apply to starved fish; it is unlikely that any single mathematical relation would fit the whole range of metabolic effects from starvation to excessive food intake. The metabolic activity associated with food consumption (specific dynamic action) will be different below and above maintenance level (Warren & Davies, 1967). Since the food is primarily protein, energy loss will be due largely to deamination. In sockeye salmon Brett, Shelbourn & Shoop, (1969) observed a maximum gross growth efficiency at 15 ~C for an intermediate feeding rate. In this case there was increasing fat content with increased rate. Even so, the decreased conversion efficiency at high food intake for the fish used here cannot be due ~;olely to increased deamination resulting from fat
308
R . R . C . EDWARDS, D. M. FINLAYSON AND J. H. STEELE
deposition, since the extra weight is laid down as protein. As Jones & Hislop (1971) suggest, there may be an upper limit to the rate of linear growth of gadoid fish and this may be genetically determine,, i'or a particular species. Thus the optimum growth rate is pro0ably not the maximum rate of increase of weight but an intermediate rate which gives a maximum conversion efficiency of the food eaten.
ACKNOWLEDGEMENTS
Thanks are due to Mr M. H. Go:dlad and Mr J. Morrison for their assistance.
REFERENCES
BIRKETT, I,., 1969. The nitrogen balance in plaice, sole and perch. J. e:cp. I31oL, Vol. 50, pp. 375-386 BRE'rt, J. R., J. E. SHELnOtJRr~& C. T. SHOOP, 1969. Growth rate and body composition of fingerling sockeye salmon, Oncorhyncus nerka in relation to temperature and body Size. J. Fish. Res. lid Can., Vol. 26, pp. 2363-2394. BRODY, S., 1945. Bioenergetics and growth. Hafner, Publishing Company, New York, 1023 pp. EOWARDS, R. R. C., D. M. FINLAWON & J. H. S'r~V.LW,1969. The ecology of O-group plaice and ~ommon dabs in Loch Ewe. II. Experimental studies of metal~olism. J. exp. mar. Biol. EcoL, Vol. 3, pp. 1-17. EDW^aDS, R. R. C. & J. H. STEELE, 1968. The ecology of O-group plaice and common dabs at Loch Ewe. I. Population and food, J. exp. mar. 8hgl. Ecol., Vol. 2, pp. 215-238. GERK~NO, S. D., 1952. The protein metabolism of sunfish of different ages. Pi~y~iol. ZoiJl., Vol. 25, pp. 358-372. HASTINOS, W. H., 1969. Nutritional score. In, Fish in rese :rch, edited by O. W. Neuhaus and J. E. Halver, Academi,; Press New York and London, pp. 263-292. HUGHES, G. M., 1964. Fish respiratory homeostaais. Sytnp. Soc. exp. Bwl., Vol. 18, pp. 81-107. JoNr~S, R. & J. R. G. HISLOP, 1971. Investigations into the growth of haddock Melanoorammus aegl¢[inus (L.) and whiting Merlan.qius merlangus (L.) in aquaria. J. Cons. perm. int. Explor. Mer (in press). McFARLAND, W. N., 1959. A study of the effects of anaesthetics on the behaviour and physiology of fishes. Pubis Inst. mar. $ci. Univ. Tex., Vol. 6, pp. 23-55. MENZ~L, D. W., 1960. Utilisation of food by a Bermuda reef fish. J. Cons. perm. tnt. Explor. Mer, Vol. 25, pp. 216-222. PANDIAN, T. J., 1967. Intake, digestion, absorption and conversion of food in the fishes Megalops, Cyprinoides and Ophlocephalus strlatus. Mar. Biol., Vol. I, pp. 16-32. PANDIAN,J. jr., 1970. Intake and conversion of food in the fish exposed to different temperatures. Mar. Biol., Vol. 5, pp. 1-17. PALOHEIMO,J. E. & L. M. DICKIE, 1966. Food and growth of fishes. II. Effects of food and temperature on the relation between metaboEsm and body weight. J. Fish. Res. Bd Can., Vol. 23, pp. 869-908. SAt~ND~RS, R. L., 1963. Respiration of the Atlantic cod. J. Fish. Res. Bd Can., Vol. 20, pp. 373-386. SUNDNES,G., 1957. Notes on the energy metabolism of the cod (Gadus ca!!arias L.) and the coalfish (Gadus virens L.) in relation to body size. Fisk Dir. Skr. Serie Havundersokelser, Vol. 6, pp. 1-10. TYLER, A. V., 1970. Rates of gastric emptying in young cod. J. Fish. Res. Bd Can., ~/ol. 27, pp.
1177-1189.
TYTLER, P., 1969. Relationship between oxygen consumption arid swimming speed in the haddock, Melanogrammus aeglefinus. Nature, Lend., Vol. 221, pp. 274-275.
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
309
WARREN,C. E. & G. E. DAVIS, 1967. Laboratory studies on the feeding, bioenergetics, and growth of fish. In, The biolooieal basis of freshwater fish production, edited by S.D. Gerking, Blackwell, Oxford, pp. 175-214. Wn~mER~, G. G., 1956. Rate of metabolism and food requirements of fishes. [Translated from Russian of] Nauchyne Trud~ Belorusskovo Gosudarstvenrovo Universiteta imeni V. 1. Lenina Minsk, 253 pp. Fish Res. Bd. Can. Trans. Series, No. 194, 202 pp.
AN EXPERIMENTAL STUDY OF THE OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD (GADUS MORHUA L.) R. R. C. EDWARDS,D. M. F!NLAYSONAND J. H. STEELE, Marine Laboratory, Aberdeen, Scotland
Abstract: The rate of oxygen consumption of cod in sea water at 12 °C containing MS222 (25 mg/l) can be expressed as: Qez = 0.245 W°.S2(mg/h), where W is the live weight of the fish (g). The maximum efficicncy of conversion of assimilated food into growth was 24 Yo during the feeding experiment. Digestion efficiencies were estimated at over 98 % using fillets of plaice as food. The effect of increasing the rate of food intake was to increase liver weight and condition factor. The relative proportions of protein and lipid in ~he body did not change over the range of feeding levels used. The conversion efficiency had a maximum value at an intermediate feeding rate.
INTRODUCTION
The experiments described in this paper are part of a marine food chain study being conducted in Loeh Ewe, Scotland. Previous investigations (Edwards & Steele, 1968) have shown that in this area at certain seasons the cod is an important predator on the populations of juvenile plaice (Pleuroneetesplatessa L.)so that further information on the food requirements of the cod becomes necessary. Earlier studies have been made on the respiration of the cod (Sundnes, 1957; Saunders, 1963) but they give no information on the effect of feeding level on meta.bolic rate. In the present study the dependence of oxygen consumption on body weight was ,.'nvestigated and this has provided the basis for a detailed analysis of the results of the feeding experiment. MATERIAL AND METHODS
Cod were caught with hand lines in shallow water at Stonehaven, Scotland. They were transported to Loch Ewe in W.nks supplied with gaseous oxygen diffusers. Mortality was negligible. The feeding experiments were conducted in large fib:'e glass tanks (1.8 x 3.7 x 1.2 m deep) connected to a fresh sea-water supply. Each tank was divided by small mesh netting into four compartments, and individual fish were placed in each compartment. A raised platform of rock allowed each fish to conceal itself and served to prevent unnecessary excitement as a result of disturbance. Weighed daily rations of plaice fillets were given to the cod and each fish was weighed monthly after anaesthetization by immersion in sea water containing MS222 (Sandoz) at 25 mg/I. Oxygen consumption was measured at 12 °C in a closed circuit respirometer incorporating a Beckman 777 oxygen electrode (Edwards, FinIayson & Steele, 1969). The use of anaesthetics to induce a 'constant' (resting) rate of oxygen consumption 299
300
R . R . C . EDWARDS, D. M. FINLAYSON AND J. H. STEELE
was demonstrated by McFtrland (19.59). The oxygen level which is critical for oxygen consumption in the cod is ~ 3 mg/l at 10 °C (Saunders, 1963) and, as Hughes (1964) has shown, oxygen uptake, is inhibited below this critical level. Care was taken, therefore, that the oxygen levels in the respirometer were well above this. Analyses for protein, carbohydrate, lipid and ash were made according to the methods given by Edwards, Finlayson & Steele (1969). The analyses of the fish were made e,fter homogenization of the whole body. To obtain faecal material, the fish were transferred for known periods to smaller tanks, .nd faeces collected by pipette. RESULTS RATE OF OXYGEN CONSUMPTION
The results obtained at 12 °C are shown in Fig. !. The oxygen uptake, Q,2 (mg/h) expressed as a function of the: live weight, W (g), is given by, Qoz - 0,245 W °'Sz with a S.E. for the exponent of 0.82_+0.035. The power constant 0.82 compares with the value of 0.80 proposed by W!aberg (1956) and is near the mean of the values I00
E
_.9. K
j"
I0
P
o U e.
I ..................
I
!0 Live
I00 W~lght
I
ICX:X:)
(g)
Fig. 1. Oxygen consumption as a function of live weight (log-log scales).
ranging I~etween 0.791 (starved) and 0.886 (fed) and given by Saunders (1963) for cod. Sun¢:nes (1957) gave values for cod and saithe of about 0.71. The rate of o×ygen consumption, i,gasured here at 12 °C, lies midway between the rates for starved and fed cod at 10 °C give,~ by Saunders (1963). The oxygen consumt'tion during anaesthetisation may be taken as a basal rate. Since, however, in the tank experiments the average temperature during the main
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
301
feeding period was ~ 16 °C, a correction may be applied using the Q1 o value of 2.48 found for 500 g cod at temperatures between 10 and 15 °C by Saunders (1963). After conversion to cal/h assuming that 1 mg of oxygen is equivalent to 3.38 g. cal (Winberg, 1956; Palohe~mo & Dickie, 1966) the standard metabolic rate is, Q = 1.00 W °'82 at 16 °C. BIOCHEMICAL ANALYSES
To convert the weight of fish, food, ~nd faecal materials in the feeding experiment into their caloric equivalents, analyses were made of protein, carbohydrate, lil:!d, and ash contents (Edwards, Finlayson & Steele, 1969). Mean values are given.i~: Table I. Two cod analysed at the start of the feeding experiments had an average T^BLv i Biochemical analyses: all values mg/100 mg dry weight. MeIin
Carbo.
Sample I, 2. 3. 4.
Cod (starting control) Cod (end of experiment) Plaice fillets Cod faece~
calorific
Protein
Lipid
hydrate
Ash
74.8 7~.2 85.6 31.5
5.8 5.3 7.6 4.1
1.1 0.8 0.8 2.5
18.5 18.8 5.9 62.00
value, kcal/g dry wt 4.82 4.82 5.63 3.09
calorific value of 4.82 k cal/g dry weight and this did not differ significantly from the experimental fish analysed at the end of the experiment. The higher calorific value of the plaice fillets was clue to their lower ash content since they contained little skeletal tissue. The dried faecal material averaged 2.3 % of the dry weight of the food, and had a caloric content of about 3.1 kcal/g dry weight. Thus the calorific content of the faeces produced was 1.3 % of the food intake. This indicates that the efficiency of absorption of the energy in the food was 98.7 %. This may be an over-estimate because the faecal material produced by the cod was of very fine texture, and although care was taken to collect all of this, some may have been lost as a fine suspension in the water. It should be noted, however, that Pandian (1967) estimated the efficiency of absorption of protein in the euryhatine fish Megalops cyprinoides to be as high as 98.3 %. Cod is assumed to be predominantly ammonotelic. Any significant excretion of urea would decrease the energy assimilated by the fish but increase the growth efficiency slightly. This would not affect the general conclusions. FEEDING EXPERIMENT
Fluctuations in water temperature during the 110 day~ of the feeding experiment are shown in Fig. 2. Apart from a brief increase during a period of warm weather in August when the temperature reached 19 °C, the temperatures were in the region of 14 to 16 °C, with a steady decline in October.
302
R. R, C. EDWARDS, D. M. FINLAYSON AND J. H, STEELE
The change in live weight of the 16 fish used in the experiment are shown in Table II, together with the fresh weight of plaice fillets consumed. (The tanks are numbered 5-8.) The results were converted into dry weights and thence into kcal, assuming that 1 g dry weight of protein is equivalent to 5.7 kcal, of lipid 9.5 kcal and of carbohydrate 4.2 kcal (Brody, 1945). Energy used for metabolism was esti~nated by subTABLE 11 Results of feeding experiment in large outdoor tanks: tanks numbered, 5-8; individual compartments, 1-4.
Fish no.
Live weights (g) lnit. Final
Fresh weight food
Growth
Food
Faeces
(kcal)
(kcal)
(kcal)
(kcal)
Metabolism
Conversion efficiency
(%)
(g)
0-33 Days 5)
6)
7)
~)
I 2 3 4
309,0 310,0 160.0 238,0
264.5 313,5 183,0 333,0
38,7 93.4 51.0 317.5
0 3.91 26,87 92.05
50,66 122.22 66.77 415.62
0.66 1,60 0.88 5.46
91,85 116.71 38,98 318.11
I 2 3 4
253.0 184.0 400,0 566.5
396.0 183.0 585.0 531,0
443.4 25.7 587.2 73.4
160.70 0 205.98 0
580.47 33.65 768.83 96.13
7.62 0.44 10.09 1.26
412.60 34.17 552.72 132.33
1 2l 3 4
457.3
466.0
129.9
13.70
170.18
2.39
154.08
8.17
610.5 512.0
572,0 679.0
76.4 650.5
0 182.08
98.31 851.64
1.29 11.18
139.96 658.37
21.66
~ 2 32 4
54.2.0 445.0 452.2 670.0
480.0 385.0 406.5 629.5
64.4 54.8 38.8 132. I
84.42 71.71 186.73 172.98
!.! ! 0.94 6.65 2.27
154.03 133.14 232.55 216.03
0 0 0 0
3,24 40.80 22.40 28.03 27.15
34-65 Days 5)
6)
7)
8)
I 2 3 4
264.5 313.5 183,0 333.0
252.0 378.7 190. I 439,5
43.5 145.0 58,0 245.4
0 72.08 8.29 103.19
59.95 197.20 79.94 575.14
0.75 2,49 ! ,00 7,17
70.96 122.63 70,65 464.77
I 2 3 4
396,0 183,0 585.0 531.0
546.0 172.5 741.2 525,0
328.1 22.4 363.0 83.9
168.56 0 173.90 0
769.02 30.87 850.79 114.10
9,59 0,38 10.60 !.44
790.87 40.47 666.29
I 2 3 4
466.0 596.0 572.0 679.0
541.6 525.5 577.0 773.6
217.5 68.0 I 16.0 296.4
81.41 0 5.58 103. ! 3
299.79 93.73 157.76 685.5
3,74 I.I 7 1.99 8.66
214.64 147,66 150.19 573,71
3.58 15.24
! 2 32
480.0 385.0
489.7 390.7
124.7 I 16.0
11.02 5.90
171.88 159.89
2.14 !.99
158.72 15t .99
6.49 3.74
4
629.5
756.5
348.0
142.10
479.67
5.98
331,59
29.99
37.02 10.50 18.17 22.19 20.70
118.99 27.50
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
303
TABI~ II (Contd.)
Fish no
Live weights (g) lnit. Final
Fresh weight food
Growth (kcal)
Food (kcal)
Faeces (kcal)
Metabolism (kcal)
Conversion efficiency (~)
(g) 66-96 Days 5)
1 2 3 4
252.0 378.7 190.1 439.5
264.0 423.5 213.5 490.5
62.5 ! 50.5 75.0 i 13.5
11.29 49.57 27.38 49.36
84.51 203.5 101.4 260.95
1.07 2.58 1.22 3.32
72.15 15 !.34 72.73 208.27
13.53 24.67 27.35 19.16
6)
I 2 3 4
546.0 172.5 741.2 525.0
612.0 171.5 744.0 525.0
155.2 37.5 100.6 87.5
73.97 0 3.13 0
356.82 50.71 231.33 118.31
4.53 0.66 2.94 1.50
278.31 51.01 225.26 116.81
20.99 1.37 -
7)
I 2 3 4
541.6 525.5 577.0 773.6
586.0 538.0 611.5 863.5
187.5 i 12.5 ! 25.0 225.0
47.82 11.63 38.47 98.43
253.53 152.12 169.02 517.44
3.22 1.93 2,15 6.57
202.48 138.55 128.40 412.43
19.10 7.74 23.05 19.27
8)
I 2 3 4
489.7 390.7 406.5 756.5
528.4 412.0 435.0 893.0
137.5 125.0 112.5 350.0
44.15 22.16 30.05 152.73
185.92 169.02 152.12 473.26
2.36 2.15 1.93 6.01
139,41 144.71 120.08 314.51
24.05 13.28 20.01 32.69
97-116 Days 5)
1 2 3 4
264.0 423.5 213.5 490.5
266.7 459.5 227.7 478.5
57.0 114.0 57.0 169.9
2.52 39.36 16.60 0
81.26 162.52 81.26 411.9
0.98 1.96 0.98 4.96
78.64 121.20 64.56 418.51
3.10 24.51 20.45 -
6)
I 2 3 4
612.0 171.5 744.0 525.0
708.5 168.5 824.0 517.5
210.9 38.0 218.6 95.0
158.64 0 89.08 0
511.5 54.17 538.94 i 35.44
6.16 0.65 6.39 1.63
346.07 56.38 443.47 141.00
31.39
1 2 3 4
586.0 538.0 611.5 863.5
604.5 543.5 606.5 953.3
! 52.0 95.0 76.0 249.0
19.92 5.12 0 97.8~
216.7 135.44 108.35 603.71
2.61 1.63 1.31 7.28
194.17 127.96 ! 12.61 498.55
9.30 3.85 16.41
I 2 3 4
528.4 412.0 435.0 893.0
544.5 416.0 440.0 952.8
104.5 ! 04.05 114.0 266.0
18.41 4.24 9.50 66.85
148.98 143.33 162.52 379.22
1.80 1.79 1.96 4.60
128.77 151.38 151.08 307.67
12.51 5.92 17.84
7)
8)
16.73
t D i e d at 22 days and was replaced. 2 Not weighed at 33 days; values are for 0-65 days.
tracting the calorie; utilized for growth and in the faecal material from the total food intake during a given period. The efficiency of cmwersion expresses the percentage of assimilated food laid down as growth. During the initial 33 days an attempt was made to feed 8 of the fish a maintenance diet, but the feeding level was below maintenance and the fish lost weight. In addition,
304
R.R.C. EDWARDS, D. M. F[NLAYSON AND J. H. STEELE ~
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~ood tntok. (~IO) Fig. 3. T h e relation o f food intake to growth (a) and m e t a b o l i s m (b). ( O , 18.?-18.8; C), 19.8-18.9; × , 19.9-13.10; A , 14.10-13.11).
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
305
The estimated efficiencies of conversion of assimilated food into growth for fish above maintenance averaged 21.63 % in the first period (0-33 days), 17.74 ~ in the second 04-65 days), 19.03 % in the third (66-96 days), and 14.73 ~o in the fourth (97-116 days). Juvenile fish normally show higher conversions than this (Pandian, 1967, 1970; Birkett, 1969): however conversion efficiency usually declines with age (Gerking, 1952; Pandian, 1967)and so these values for 2-3-year old cod are probably of the right order. The effect of feeding level on growth rate is shown in Fig. 3 .. Both growth rate and food intake, expressed as cal/h, were divided by Q, the standard metabolic requirement, to eliminate the effects of different fish sizes and hence intensities of metabolism. It may be seen that the relationship is not linear; but it can be fitted by the equation relation G/Q = (~'.106+0.534 log F/Q. The value F/Q = 1 corresponds to a feeding rate providing energy at the same rate as the metabolic rate determined from the respiration experiments. This feeding rate gives a small positive growth rate in the tanks, indicating that, as might be expected, the fish in the tanks do not respond in exactly the same way as those in the respirometer. As the feeding rate increases the growth rate also increases but at high feeding rates this increase is small. In consequence, the conversion, or gross growth efficiency expressed as G/F hasa" maximum value at an intermediate feeding rate. Similar results have been found in freshwater fish culture (Hastings, 1969). For the cod used here, this feeding rate has a value of F/Q of 2.2 and the maximum efficiency is 24 ~. Since growt~ accounts for less than a quarter of the food, this curvilinear relation between growth and food intake is not appaient when metabolic rate is plotted as a funcdon of food intake (Fig. 3b). Thus, within the limits of error of these results, metabolic rate appears proportional to food intake. THE EFFECT OF FEEDING LEVEL ON BIOCHEMICAL COMPOSITION
The analyses of the fish at the end of the feeding experiment were related to the mean feeding level. In Fig. 4 the total protein and lipid are expressed as percentages of the caloric content of the body and plotted against feeding level. It would appear
0
~ O ~ O ~
'if
6~ I
-
O~
gO
aJ?"
eo
J I
I<,
2
.
i
3
._
J
4
Food I~k= (.F/Q) Fig. 4. Lipid and protein content in relation to the food intake.
306
R.R.C.
E D W A R D S , D. M. F I N L A Y S O N A N D J. H. S T E E L E
that the body compositic ~ remained fairly constant over the observed feeding range and that protein comprised between 88 and 90 % and lipid about 10 % of the total caloric content. The remainder was carbohydrate. An analysis of the livers at the end of the experiment gave mean values of 47.7 % protein. 31.4 % lipid and 8.8 % carbohydrate. It was calculated that about 5.3 % of the total body lipid was stored in the liver. THE EFFECT OF FEEDING LEVEL ON CONDITION FACTOR AND LIVER WEIGHT
Conditon factor (K) is usually given as, wt(g)x 100/(length, cm) s. The condition factors of the fish ranged between 0 71 and 1.91 at the end of the feeding experiment and, as shown in Fig. 5a, varied with feeding level. When the feeding level was in |*3
"*
5
w
3
-
4J
.gy
I.I -
~
X
1,0 -
o
~e
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v
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oo X
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' 3
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,I 5
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0 Int o k e
:
_ a I
I 2
,
I,,, 3
I 4
(, F I Q )
Fig. 5. Condition factor as a function of food intake ( × , 18.9; O, 13.11) (a) and final liver weight as a function of food intake (b).
excess of three times the standard metabolic requirement, the fish developed a thickening o" the lateral musculature, particularly near the tail, which resulted in irregular and apparently difficult swimming. A series of length and weight measurements taken midway in the experiment ga.ve values of 0.70 to 1.25. Condition factors for a sample of 2-year old cod taken in July 1968 from the smae sea area as these fish had a mean of I. 17 (West, pers. comm.). The liver weight expressed as a percentage of the body weight increased with feeding level (Fig. 5b). THE EFFECT OF TEMPERATURE ON MAXIMUM GROWTH RATE
Since Tyler (1970) has ~hown that the gastric digestion of 2~year old cod proceeds most rapidly at 15 °C and declines at higher and lower temperatures. The rates of food intake observed in these experiments may be close to the maximum for this
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
307
species. A supplementary experiment during December when the water temperature was between 6 and 8 °C gave daily rates ofweight increase for four cod of!ess than 0.075 when fed excess rations; this is considerably less than those at the higher temperatures, so that temperature was probably limiting food intake and growth. DIscussION
There is good agreement between the values of oxygen consumption in these experiments and those of Sundnes (1957)and of Saunders (1963). The measurements of standard oxygen consumption made by Tytler (1969) on gadoid fish suggest that all these earlier values approximate to a routine rate. Our results demonstrate the dependence of metabolic rate on the rate of food intake. It is likely that ~he energy requirements for activity remained fairly low, since it was observe,t that most of the fish remained hidden during the daylight hours, though they emt-rged at night. The constancy of the calorific values of the fish at different feeding levels, together with constancy of protein and lipid content is of some interest. Apparently energy is not stored aslipid in the cod, as was found by Menzel (1960) for Bermuda reef fish. It would appear that any foo'~ consumed in excess of maintenance is laid down partl~ as liver growth but mainly as an increase in size of the lateral and tail muscles, which results in an increase in the condition factor: similar results have been obtained for other gadoids (Jones & Hislop, 1971). A condition factor of I. 17 for the natural population from which the experimental fish were taken suggests that their feeding level was at least twice the standard metabolic requirement estimated from this experiment. In addition, the activity necessary to secure food in t~e ~ a may result in some extra energy demand. Is is of interest that this intake level is approximately the same as that which gave maximum conversion efficiency in the feeding experiments, suggesting that the natural population could be operating close to this maximum. The observed, lower efficiency for lower experimental rates of feeding is according to expectation. The decrease at high levels of feeding may be related to the fact that the weight increase occurs as increased musculature rather than as an i: ~rease in length. The relation between rates of growth, metabolism and food intake derived from the results does not apply to starved fish; it is unlikely that any single mathematical relation would fit the whole range of metabolic effects from starvation to excessive food intake. The metabolic activity associated with food consumption (specific dynamic action) will be different below and above maintenance level (Warren & Davies, 1967). Since the food is primarily protein, energy loss will be due largely to deamination. In sockeye salmon Brett, Shelbourn & Shoop, (1969) observed a maximum gross growth efficiency at 15 ~C for an intermediate feeding rate. In this case there was increasing fat content with increased rate. Even so, the decreased conversion efficiency at high food intake for the fish used here cannot be due ~;olely to increased deamination resulting from fat
308
R . R . C . EDWARDS, D. M. FINLAYSON AND J. H. STEELE
deposition, since the extra weight is laid down as protein. As Jones & Hislop (1971) suggest, there may be an upper limit to the rate of linear growth of gadoid fish and this may be genetically determine,, i'or a particular species. Thus the optimum growth rate is pro0ably not the maximum rate of increase of weight but an intermediate rate which gives a maximum conversion efficiency of the food eaten.
ACKNOWLEDGEMENTS
Thanks are due to Mr M. H. Go:dlad and Mr J. Morrison for their assistance.
REFERENCES
BIRKETT, I,., 1969. The nitrogen balance in plaice, sole and perch. J. e:cp. I31oL, Vol. 50, pp. 375-386 BRE'rt, J. R., J. E. SHELnOtJRr~& C. T. SHOOP, 1969. Growth rate and body composition of fingerling sockeye salmon, Oncorhyncus nerka in relation to temperature and body Size. J. Fish. Res. lid Can., Vol. 26, pp. 2363-2394. BRODY, S., 1945. Bioenergetics and growth. Hafner, Publishing Company, New York, 1023 pp. EOWARDS, R. R. C., D. M. FINLAWON & J. H. S'r~V.LW,1969. The ecology of O-group plaice and ~ommon dabs in Loch Ewe. II. Experimental studies of metal~olism. J. exp. mar. Biol. EcoL, Vol. 3, pp. 1-17. EDW^aDS, R. R. C. & J. H. STEELE, 1968. The ecology of O-group plaice and common dabs at Loch Ewe. I. Population and food, J. exp. mar. 8hgl. Ecol., Vol. 2, pp. 215-238. GERK~NO, S. D., 1952. The protein metabolism of sunfish of different ages. Pi~y~iol. ZoiJl., Vol. 25, pp. 358-372. HASTINOS, W. H., 1969. Nutritional score. In, Fish in rese :rch, edited by O. W. Neuhaus and J. E. Halver, Academi,; Press New York and London, pp. 263-292. HUGHES, G. M., 1964. Fish respiratory homeostaais. Sytnp. Soc. exp. Bwl., Vol. 18, pp. 81-107. JoNr~S, R. & J. R. G. HISLOP, 1971. Investigations into the growth of haddock Melanoorammus aegl¢[inus (L.) and whiting Merlan.qius merlangus (L.) in aquaria. J. Cons. perm. int. Explor. Mer (in press). McFARLAND, W. N., 1959. A study of the effects of anaesthetics on the behaviour and physiology of fishes. Pubis Inst. mar. $ci. Univ. Tex., Vol. 6, pp. 23-55. MENZ~L, D. W., 1960. Utilisation of food by a Bermuda reef fish. J. Cons. perm. tnt. Explor. Mer, Vol. 25, pp. 216-222. PANDIAN, T. J., 1967. Intake, digestion, absorption and conversion of food in the fishes Megalops, Cyprinoides and Ophlocephalus strlatus. Mar. Biol., Vol. I, pp. 16-32. PANDIAN,J. jr., 1970. Intake and conversion of food in the fish exposed to different temperatures. Mar. Biol., Vol. 5, pp. 1-17. PALOHEIMO,J. E. & L. M. DICKIE, 1966. Food and growth of fishes. II. Effects of food and temperature on the relation between metaboEsm and body weight. J. Fish. Res. Bd Can., Vol. 23, pp. 869-908. SAt~ND~RS, R. L., 1963. Respiration of the Atlantic cod. J. Fish. Res. Bd Can., Vol. 20, pp. 373-386. SUNDNES,G., 1957. Notes on the energy metabolism of the cod (Gadus ca!!arias L.) and the coalfish (Gadus virens L.) in relation to body size. Fisk Dir. Skr. Serie Havundersokelser, Vol. 6, pp. 1-10. TYLER, A. V., 1970. Rates of gastric emptying in young cod. J. Fish. Res. Bd Can., ~/ol. 27, pp.
1177-1189.
TYTLER, P., 1969. Relationship between oxygen consumption arid swimming speed in the haddock, Melanogrammus aeglefinus. Nature, Lend., Vol. 221, pp. 274-275.
OXYGEN CONSUMPTION, GROWTH, AND METABOLISM OF THE COD
309
WARREN,C. E. & G. E. DAVIS, 1967. Laboratory studies on the feeding, bioenergetics, and growth of fish. In, The biolooieal basis of freshwater fish production, edited by S.D. Gerking, Blackwell, Oxford, pp. 175-214. Wn~mER~, G. G., 1956. Rate of metabolism and food requirements of fishes. [Translated from Russian of] Nauchyne Trud~ Belorusskovo Gosudarstvenrovo Universiteta imeni V. 1. Lenina Minsk, 253 pp. Fish Res. Bd. Can. Trans. Series, No. 194, 202 pp.