The Energetics of Feeding, Metabolism and Growth of … · 923 the energetics of feeding, metabolism and growth of brown trout (salmo trutta l.) in relation to body weight, water

923

THE ENERGETICS OF FEEDING, METABOLISM AND GROWTH OF BROWN TROUT (SALMO TRUTTA L.) IN

RELATION TO BODY WEIGHT, WATER TEMPERATURE AND RATION SIZE

BY J. M. ELLIOTT

Freshwater Biological Association, Windermere Laboratory, Ambleside, Cumbria

INTRODUCTION

The study of energy budgets of fish was pioneered by Ivlev (1939) and grew rapidly after Winberg (1956) published his extensive review of the subject. An energy budget for a given period of time is described by the basic equation (from Ricker 1971):

C = F+ U+AB+R where R = Rs+ Ra+Rd

C is the total energy content of the food consumed by the fish, F is the energy value of the faeces, U is the energy value of the excretory products, AB is the total change in the energy value of body materials (growth or loss in energy content) and includes any reproductive products released by the fish, R is the total energy of metabolism which is subdivided into three components: R. is the energy equivalent to that released in the course of metabolism in unfed and resting fish (standard metabolism), Ra is the energy required for swimming and other activity, Rd is the energy required for the processes of digestion, movement and deposition of food materials (including specific dynamic action).

The extensive literature on energetics in fish has recently been reviewed by Beamish, Niimi & Lett (1975). Few workers have published complete energy budgets and have studied the effects of varying body size, temperature and ration size. The chief purpose of the present paper is to provide this information for brown trout and to develop equations to estimate the various components of the energy budget. Previous papers have dealt with various aspects of feeding and growth in brown trout (Elliott 1972, 1975a,b,c,d, 1976a,b) and the information in these papers is used extensively in the construction of the energy budgets. All the methods used in the experiments are described in detail in these previous papers. The methods used in the construction of the energy budgets are described in the appropriate part of the results.

RESULTS

The relationships between the components of the energy budget are summarised in Fig. 1. All symbols are defined in the introduction except the proportions of the daily energy intake lost in the faeces (PF), lost in the excretory products (Pu), absorbed by the trout (PA) and available for growth and metabolism (Pp). The latter quantity is often called the physiologically useful energy (Winberg 1956) or metabolizable energy (Beamish et al. 1975). Figure 1 includes the efficiencies of changes between the major components.

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924 Energetics of brown trout

Only the gross efficiency (AB/C) will be examined in the present paper, but the various efficiencies connected with energy losses in the waste products (PF, PU, PA, PP) were investigated in detail in a previous paper (Elliott 1976b).

Trout on maximum rations

The mean dry weight of Gammarus pulex L. (Dmax mg) eaten by a trout in a day was

Dolly energy intoke % g loss'i Foeces l C=F tU+AB+R _ reces (iOO PF) F CP

/% efficiency Absorbed materials%lossinExcretorycpro t 100 Pp J C_F CPA excretory products c pocts

-~~~~~~~~~~~~~~~~~~" 1- - -- --- - - -l - - -I

1 l efficiency' %/c gross efficiency

[ V 1~~~~00 PP/PA Io o 00 AB/C , / ~~~~~~~~

F LG 1. SummaryoftPhysiologicsaly useful o % efficieney i Growth or loss ctnhmocpesfhenergy bde And Bh C-F-eU-Rn

t b loss in metebol sm e IO iO RICPp J

Metabolism- -- Rio-F-U-Aw Stoendrd metobolism

=CPp-ZS , RS -R-R, +Rd

=Rs+ Ro +Rd

- t S

~~~~~~~~~~~~~Digestion, movement, Activity 6 deposftion of food

Ro = R- Rts- Rd Rd = R -Rs-R(]

FIG. 1. Summary of the losses and uses of the daily energy intake of a trout. The boxes contain the major components of the energy budget and the ovals contain the percentage efficiencies of changes between these major components. Direct pathways are shown as solid lines whilst broken lines indicate pathways which include more than one component.

measured in each experiment (Elliott 1975c) and was converted into energy units (using energy values given in Elliott 1976b) to give the energy content of the ration (Cnax cat day'1 in Table 1). Equations for the estimation of Cma, were easily derived from the product of the mean energy value of Gammarus (4-438 ea! mg-'1) and the equations used



Table 1. Water temperature (mean + range in 0 C), initial weight of fish (WI g live weight) and the major components (defined in the introduction) of the energy budget for trout on maximum rations (9500 confidence limits are given for all experiments in which

more than one trout was used)

To C W1 g Cmax cal F cal U cal AB cal R cal RS cal Ra+ Rd cal

3-8+0-3 50 09+0 07 280?1 82+1 12? <1 13+1 173?1 152? <1 21+1 5-6+0-5 11-57 198 53 10 49 86 76 10

50-27+0-27 607+8 164?3 32? <1 148?1 263?3 221?1 43+3 90 99 962 261 50 261 390 340 50

249-08 2124 589- 110 519 906 706 200 7q1+0-6 50 54+0 07 1051-5 270?2 63? <1 329?3 388?2 304? <1 85?2 9 5+0*7 1P62 532 126 38 166 202 135 67

05-69+0-27 1601?29 385?11 114?2 526+2 576+ 17 380? 1 196?17 91-24 2498 607 177 837 877 575 302

257-95 5552 1368 399 1848 1937 1213 724

12-8?0-7 11-75 1061 237 89 318 417 204 213 50-88?0-24 3055?13 695?5 257?1 976+20 1128?19 552?2 576?21 -

91P91 4722 1083 398 1398 1843 829 1014 248-47 10139 2381 840 2877 4041 1685 2356

15-0?0-6 11-78 1280 271 118 255 636 235 401 50.13+0417 3837+20 836?7 355?1 776+22 1870+25 641?2 1229+25 86-02 5885 1304 544 1053 2984 939 2045

255-30 13371 2970 1225 2613 6563 2044 4519 17-8?0-7 50-65+0-36 5141?32 1077?24 525?4 159+3 3380?19 801?4 2580?17 19-5?0-8 11-82 504 104 54 0 346 314 32

50-89+0-23 1550?18 322?9 167?2 - 1 _ 1 1062?9 911? 3 151? 8 83-42 2357 485 254 1 1617 1307 310

281-20 5412 1113 583 -50 3766 3176 590 21P7+1O0 50 90?0 39 344?47 69+9 39?5 -852?78 1088?88

tJt




to estimate Dmax (from Elliott 1975b, c). The new equations (eqn (1) in Table 2) indicate that both temperature (T? C) and the weight of the trout (W g live weight) affect the maximum energy intake. As comparisons in previous papers have shown that there was good agreement between actual and estimated values of Dmax, it is not surprising that the same was true for Cmax.

Energy losses in the faeces (F cal day- 1) and excretory products (U cal day-1) were not measured in the feeding experiments but were estimated from eqns (2) to (5) (Table 2). Equations (3) and (5) were developed from a series of detailed experiments on energy losses in the waste products (Elliott 1976b). As the weights of the trout and their energy content at the beginning and end of each experiment were known (Elliott 1976a), the total gain or loss in the energy content of each fish could be measured. This quantity was divided by the number of days in the experiment to give the mean change in the energy content of the fish (AB cal day-'). This component was positive in the temperature range

Table 2. Equations used to estimate the components of the energy budget for trout on maximum rations (eqns (3) and (5) are from Elliott (1976b))

Equation Temp. (T? C) a b ? 95?% C.L. b2 + 95%o C.L.

(1) Cma. = aWbleb2T 3.8-6-6 2-902 0-762?0-027 0.418?0-035 6*6-13*3 15-018 0-759?0-023 0-171 ?0-012

13-3-17.8 26-433 0-767?0-041 0-126+0-031 17-8-21P7 3.241 x 107 0-753 +0086 -0-662+0-054

(2) F= CPF 3-8-20.4 (3) PF = aTbleb2 (C/Cmax) 3-8-20-4 0-212 -0-222+0-0224 0-631 +00350 (4) U= CPU 3-8-20-4 (5) Pu = aTbleb2(c/Cmax) 3x8-20x4 0x0259 0x580?0x0110 -0-299+0-0162 (6) AB = CPP-R 3-8-20-4 (7) Pp = 1-PF-PU 3-8-20.4 (8) Rmax = aWb leb2 T 3-8-17-8 3 890 0-770+0-0254 0-204?0-00394

17.8-19 5 2-215 x 107 0-757?0-0208 -0-663+0-0175 19.5-21F7 28-833 0.756+0 0440 0*0325?0-0288

(9) RS = aWbleb2T 3-8-7-1 4-126 0-734?0-0257 0-192?0-0125 7-1-19-5 8-277 0-731+0-0220 0-0938?0 00407

(10) Ra+Rd = R-Rs 3-8-19-5

3-8-17-8' C and was therefore a measure of growth, but there was little change in the energy content at 19-5' C and a marked decrease in energy content at 21P7' C (Table 1).

The energy available for metabolism (Rmax cal day-') was found by difference (Rmax = Cmax -F- U- AB). Experiments with different sized fish were performed at five temperatures (Table 1) and when the values of Rmax from these experiments were plotted against the mean weight of the trout (WT g), a linear relationship was obtained on log/log scales (Fig. 2(a)). As values of Rmax for trout of initial weight close to 50 g were available for nine temperatures with four trout for each temperature, they were used instead of the intercepts from Fig. 2(a) to examine the relationship between Rma, and temperature (T?C). This was found to be exponential with three temperature ranges of 3 8-17-8' C, 17 8-19 5? C, 19-5-21P7' C (Fig. 2 (b)). Therefore the relationship between the three variables Rmax, J7V and T was defined by the multiple regression equation:

loge Rmax = logea+bl loge W+b2 T (8)

which is given in its exponential form in Table 2 together with values of the constants a, b1 and b2. Variance ratios were all highly significant (P <0 001) and the proportion of the



J. M. ELLIOTT 927

0 c

7000 150 - (Q)/

12-8

//X 19-5

.:. / *.... -7,~ ~ ~~~-

1000 xx(t*.

500 ,

x'

100 C; 80 I I ,

10 50 100 300 wg

4000 -

1000-

500 -

00

10 0 I I I I I , I , , , , I , I 3 5 10 15 20 22

T?C

FIG. 2. (a) Relationship between the energy required for metabolism (Rmax cal day 1) and the mean weight of the trout (W g) at different temperatures (0 C) (closed circles and crosses were used for 12-8? C and 19.50 C respectively because the values for these temperatures were similar). (b) Relationship between Rmax and temperature (T?C) for

trout of initial weight close to 50 g.




variance of loge Rniax attributable to its regression on loge Wand Twas over 99%0 for each temperature range. As both the physiologically useful energy (CPp) and the energy required for metabolism (Rmax) can be estimated, the change in the energy content of the fish (AB) can also be estimated from the difference between these two components (equations (6) and (7) in Table 2). If CPp is greater than R, AB is a measure of growth, but if CPp is less than R, then AB is the daily loss in the energy content of the trout.

3000- 3 19-5

(0) X 15*0

*12-8

1000 9

*5-6

500 :2

100 _ /

50 , , I I I I I 10 50_ 100 300

800 W .

(b)

500 -

100 1 I I I I I I I 3 5 10 15 20

To C

FIG. 3. (a) Relationship between the energy required for standard metabolism (R, cal day-') and the mean weight of the trout (W g) at different temperatures (0 C). (b) Relationship

between R, and temperature (T? C) for trout of initial weight close to 50 g.

The experiments with trout deprived of food (zero rations) were used to estimate the energy required for standard metabolism (R, cal day-1). As the weight and energy content of the trout at the beginning and end of each experiment were known (Elliott 1975d, 1976a), the mean daily loss in the energy content of each fish could be measured. Energy losses in the waste products (F+ U) were estimated from equations in Elliott (1976b) and subtracted from the daily loss to give the energy required for metabolism (R). As the fish were not fed and were fairly inactive, the values for R were assumed to be also esti-



J. M. ELLIOTT 929

mates of Rs. The data were analysed in the same way as those for Rmax. There was a

logarithmic relationship between Rs and mean weight (W g), and an exponential relation-

ship between Rs and temperature (T? C) with two temperature ranges of 3-8-7.1 C and

7.1-19 5o C (Fig. 3). Therefore the relationship between R., W and T was defined by an

equation similar to eqn (8). This equation is given in its exponential form as eqn (9) in

Table 2 together with values of the constants a, b, and b2 for the two temperature ranges.

Variance ratios were highly significant (P <0 001) and the proportion of the variance of

loge Rs attributable to its regression was over 99%0 for both temperature ranges. Equation

(9) was used to estimate Rs for the trout on maximum rations (Table 1) and the difference

between R and Rs provided an estimate of the energy required for activity and for the

digestion, movement and deposition of food materials (Ra+Rd cal day-'). These two

Table 3. Percentage of the daily energy intake requiredfor each component of the energy budget for trout on maximum rations (values for Rs and Ra + Rd

are expressed as percentages of R)

To C W1 g F+ U AB R Rs Ra+Rd 0/ 0/ 0/ 0/ 0/

3.8 50-09 33 5 62 88 12 5 6 11 58 32 25 43 88 12

50 27 32 24 43 84 16 90 99 32 27 41 87 13

247 08 33 24 43 78 22 741 50-54 32 31 37 78 22 9 5 11 62 31 31 38 67 33

50-69 31 33 36 66 34 91 24 31 34 35 66 34

257 95 32 33 35 63 37 12 8 11 75 30 30 39 49 51

50 88 31 32 37 49 51 91 91 31 30 39 45 55

248 47 31 28 40 42 58 15.0 11P78 30 20 50 37 63

50 13 31 20 49 34 66 86 02 31 18 51 31 69

255.30 31 20 49 31 69 17 8 50-65 31 3 66 24 76 19 5 11 82 32 0 69 91 9

50 89 31 0 69 86 14 83 42 32 0 69 81 19

281-20 31 0 70 84 16

components of the energy budget were the only components which could not be estimated

separately. As the trout were on maximum rations, body weight and temperature were the princi-

pal factors affecting the energy budget. Values of all components increased with the

weight of the trout at each temperature (Table 1), and the weight exponents for Cmax and

Rmax were very similar with slightly lower values for Rs (cf. b, in eqns (1), (8), (9) in

Table 2). Therefore, when each component was expressed as a percentage of the daily

energy intake, the values were very similar for trout of different weights at the same

temperature (Table 3). The effects of temperature were more complicated. Energy losses

in the waste products (F+ U) varied considerably with temperature (Table 1) but were

remarkably constant when expressed as a percentage of the daily energy intake (Table 3).




The effect of temperature on the change in the energy content of the fish (AB) was the same as that on mean specific growth rate (Elliott 1975c) with maximum values at 12.80 C and values decreasing with both decreasing temperatures below 12.80 C and increasing temperatures above 12.80 C (Table 1). When AB is positive and is expressed as a percentage of the daily energy intake, it is a measure of gross efficiency (Fig. 1) which will be discussed in detail later. Gross efficiency was similar for different weights of trout at the

1000 (o) 12-80C0

500.500 ,. 15.00 0

500 - X 7-10 /

x 5

3800CX 17800 C 56

-9-5 C 0 x-~~~~~

-500:0 X

-1000 I I l l I I l I

(b) 17800C x 3000

x 2000 2000 4000 60000 200 41500 0 200

Ccol

FIG. 4. (a) Relationship between the mean change in energy content (AR cal day-'1) and the daily energy intake (C cal day )1at different temperatures (0 C). (b) Relationship between the energy required for metabolism (R cal day-'1) and C at different temperatures (0 C).

same temperature but was markedly affected by temperature. It increased from a low value of 500 at 3.80 C to a maximum value of over 3000 at 9.50 C and then rapidly decreased to 000 at 19.50 C (Table 3). The effects of temperature on the energy required for metabolism (Rmax) and standard metabolism (Re) have already been examined and are illustrated in Figs 2(b) and 3(b). When Rma wa epsed as a percentage of the daily intake, its relationship with temperature was exactly the opposite to that shown by A\B with minimum values at 9 5? C and maximum values at high and low temperatures (Table 3).



J. M. ELLIOTT 931

The proportion of total metabolism required for standard metabolism decreased slightly with increasing body weight at the same temperature from 3.80 C to 17.80 C. As the daily energy intake and swimming activity both increased with increasing temperature from 3-8- C to 17.80 C, it is not surprising that there was a corresponding increase in the energy required for activity and the digestion, movement and deposition of food (Ra + Rd). These two components gradually increased from only 12% of total metabolism at 3.80 C to over 7000 at 17.80 C. The marked change in the relative proportions of R. and Ra+Rd at 19.50 C was probably related to the large decrease in both energy intake and metabolism whilst the energy requirements for standard metabolism remained high. Activity was limited to short bursts of rapid swimming at temperatures above 190 C and the trout were reluctant to feed.

1000 000

8 0 E < 1 2 5 2

1000

-500 750 C cal

500

250

-1000 , 1'1011 1 1 ,. 3 5 10 15 20

TO C

FIG. 5. Relationship between the mean change in energy content (AB cal day-') and temperature (T? C) at fixed levels of energy intake (C cal day- 1) for trout of initial weight

close to 50 g.

Therefore the relationships between the various components of the energy budget (Fig. 1) and the effects of temperature and body weight on these components can now be described in detail. Equations (1) to (10) (Table 2) can be used to estimate the five major components (C, F, U, AB, R) and the components of metabolism (R8, Ra +Rd) for trout in the weight range 10-300 g, in the temperature range 3.8-19.5' C, and on maximum rations.

Trout on reduced rations

Energy budgets were constructed in the same way as those for trout on maximum rations and are summarized in the Appendix. The major components of the budgets were affected by temperature, the weight of the fish and the daily energy intake. Values for




trout of initial weight close to 50 g illustrate the relationships between three of these components (Fig. 4). The relationship between the change in the energy content of the fish (AB cal day- ') and the daily energy intake (C cal day- 1) at each temperature was the the same as that between the mean rate of change in live weight and the mean dry weight of the ration (cf. Fig. 4(a) with Fig. 1 in Elliott 1975d). Although both temperature and energy intake also affected the energy of metabolism (R cal day- 1), the effects of variations in energy intake were relatively small at 19.50 C and temperatures below 12.80 C

(Fig. 4(b)). The complex relationships between AB, energy intake and temperature were clarified

by plotting AB against temperature at fixed levels of energy intake for trout of initial weight close to 50 g (Fig. 5). Values of AB at each level of energy intake were read off the curves in Fig. 4(a) and the maximum values of AB were calculated from eqn (6) in Table 2.

Table 4. Water temperature (T?C), initial weight of fish (W1 g live weight) and the major components of the energy budget for trout on maintenance

rations To C W1 g Cmain cal F cal U cal Rmain cal R. cal Ra+Rd cal

3-8 50 10 222 58 10 154 151 3 5-6 11-66 130 29 8 93 74 19

50-24 355 75 21 259 214 45 90-12 560 118 33 409 330 79

251P59 1142 235 68 839 698 141 7-1 50 55 462 85 33 344 283 61 9-5 11P72 222 38 19 165 122 43

50-68 555 90 48 417 355 62 90-68 957 159 81 717 543 174

254-45 2034 336 173 1525 1155 370 12-8 11 78 349 54 35 260 167 93

50-89 866 128 89 649 485 164 88-90 1433 215 147 1071 730 341

250-86 2905 429 299 2177 1557 620 15-0 11-75 411 60 46 305 205 100

50*11 1154 165 130 859 590 269 89-66 1662 227 192 1243 903 340

252-14 3645 511 415 2719 1921 798 17-8 50-68 1376 183 175 1018 774 244 19-5 11P81 577 128 60 389 313 76

50-89 1532 313 165 1054 910 144 86-32 2433 519 257 1657 1339 318

275-33 5956 1288 626 4042 3125 917

The level of energy intake affected the temperature range over which the total energy content of the fish increased (i.e. AB was positive) and there was a progressive decrease in this range from 3.8-16.5o C at 1250 cal day-' to only 3.8-4? C at 250 cal day-'. As the level of energy intake decreased, there was a corresponding decrease in the optimum temperature for the maximum increase in the energy content of the fish, and values ranged from about 16? C at an energy intake of 4000 cal day- to about 4? C at only 250 cal day-l

The maintenance energy intake (Cmain cal day- 1) is the energy intake that just main- tains a trout without any change in the energy content of the fish (AB = 0). Values of Cmain were read off enlarged versions of the curves in Fig. 4(a) and similar curves constructed from the data for other weights of trout (see Appendix). These values were used to construct energy budgets for trout on maintenance rations (Table 4). The products of



Table 5. Equations used to estimate the maintenance energy intake (Cmain calday 1), the energy requiredfor maintenance

metabolism (Rmai,, cal day-'), the optimum energy intake (C,p, cal day-1) and the energy intake within the 'scope for growth' (C cal day-')

Equation Temp. (T? C) a b, ? 95%, C.L. b2 ? 95%4 C.L.

(11) Cmain = aWbleb2T 3-8-66 6169 0716+0-107 0-224?0-102 6.6-19.5 12-031 0737+0-058 0 105?0.016

(12) Rmain = aWbleb2T 3.8-7-1 3.802 0-723+0-0998 0.245?0.08111 7K1-19-5 11P866 0-721 +00417 00915?0-0112

(13) C0,t = aWbleb2T 3-8-6 8 2-902 0-762+0-027 0-418+0-035 6.8-15-0 15-116 0-767+0-046 04138?0 0110

150.-19.5 753-852 0-767+0-017 -0*118?0 006

(14) C= a, Wb1ej2p+(a2+b3P)T a. a2 b3?95/O C.L.

3-8-6&8 6-126 0-219 0-757+0-079 -0-0067?0.0008 00017?0-0001 6-8-15-0 8-488 0-131 0-768+0-028 0-0076?0-0009 0-0000

150-19-5 29-755 0-0515 0-756+0-029 0-0353?+OOOO1 -0.0018?0.0001



Table 6. Comparison between the energy available for metabolism (Act. R cal) and the estimated w 4-pa values of the energy required for maintenance metabolism (Est. Rmain cal) for trout on reduced rations

(expressed as a proportion of the maximum ration: CICgax); 9500 confidence limits are given for Rmamn andfor R wheh more than one trout was used in the experiments; significant differences between R and

Rmain are indicated by asterisks: * P<0 05, ** P<0 -01

To C WI g CICma Act. R cal Est. Rmajn cal To C WJ g CICmax Act. R cal Est. Rmai, cal

3.8 50 09 0-82 160+ 2 163(131-202) 15 11-80 0-27 268 280(228-344) 5-6 11P72 0 42 84 89(65-121) 11-70 0-55 387 278(226-342)* 11P68 0-80 90 89(65-121) 11172 0 73 455 278(226-342)** 50 19 0-43 258+6 254(200-323) 50-11 0-28 875?49 793(655-960) 50 33 0-79 273+ 1 255(201-324) 50-11 0'50 1065? 30 793(655-960) * 88-22 0-42 387 382(301-485) 50*10 0'73 1293 ?15 793(655-960)** 90 34 0 80 422 389(306-494) 90 21 0-27 1305 1212(1002-1467) 252 36 0-42 879 818(644-1039) 91-46 0-48 1559 1224(1012-1481)*

256'67 0 79 956 828(647-1060) 91'73 0-72 2165 1226(1013-1483)** 7*1 50 50 0-46 355? 1 369(269-506) 252 31 0-31 3335 2544(2085-3104)* 50 58 0*90 343+ 1 369(269-506) 248-28 0-54 3864 2514(2061-3067)** 9 5 11 70 0-35 139 168(137-207) 254-67 0-76 5006 2561(2099-3124)** 11 83 0-65 147 169(137-208) 17-8 50-74 0.19 1035?5 1036(849-1264) 50 58 0 35 422+4 482(395-588) 50 76 0-36 1267?4 1036(849-1264)* 50179 0-63 425+6 483(399-584) 50 77 0-68 2419?6 1036(849-1264)** 89-36 0 35 647 726(595-886) 19*5 11179 0 70 400 423(341-525) 90-87 0 65 659 734(602-895) 50 90 0-56 1097?12 1214(995-1481) 249-52 0-33 1571 1521(1237-1871) 86-21 0*61 1655 1774(1454-2164)

257*93 0-68 1522 1558(1267-1916) 278-23 0-59 3999 4129(3357-5079) 12-8 11-76 0-34 212 228(185-280) 11P75 0Q64 243 228(185-280) 1182 0-91 372 229(183-286)* 50 84 0 35 665? 12 655(541-793) 50-94 0-62 663? 8 656(542-794) 51'02 0-89 964+26 656(542-794)* 86-24 0-36 1008 958(792-1159) 88&36 0-63 1021 975(806-1180) 87-63 0-95 1617 969(801-1172)**

250 2l 0-38 2382 2065(1693-2519) 246-36 0-66 2470 2042(1674-2491) 258 63 0-92 3419 2115(1734-2580)**



J. M. ELLIOTT 935

the mean energy value of Gammarus and the equations used to estimate the maintenance ration (from Elliott 1975d) provided new equations for estimating Cmain (eqn (11) in Table 5). Previous comparisons have shown that there was good agreement between actual and estimated values of the maintenance ration (Elliott 1975d), and the same was true for Cm in. Energy losses in the waste products were estimated from eqns (2) to (5), AB was zero and the energy required for maintenance metabolism (Rmain cal day- 1) was estimated by difference. The energy required for standard metabolism was estimated from eqn (9) and was always less than the maintenance metabolism (Table 4). Values of Rmain were analysed in the same way as those for R and the relationship between Rmain, mean weight (0k g) and temperature (T? C) was defined by an equation similar to eqn (8) but with two temperature ranges of 3.8-7-lo C and 7.1-19-5' C. This equation is given in

900 - ( a) 3000

900~ ~~~ 0 (0)

'1 00

300

750 20%\

5QQ N IN

o

08 (b)

100~ ~~~~0

o 3 5 10 15 20

T0 C

FIG. 6. (a) Gross efficiency measured in terms of energy values for trout of initial weight close to 50 g. Percentage efficiencies are drawn as isopleths over the curves relating AB to temperature at fixed levels of energy intake (from Fig. 5). (b) Gross efficiency measured in

terms of wet weight (from Fig. 8 in Elliott 1975d).

its exponential form as eqn (12) in Table 5 together with values of the constants a, b1, b2. Variance ratios were highly significant (P <OOO1) and the proportion of the variance of loge Rmain attributable to its regression was over 9800 for both temperature ranges.

Equation (12) was used to estimate R .i for the trout on reduced rations and these values were compared with values for the total energy of metabolism (Table 6). In spite of large variations in temperature, body weight and energy intake, the values of R and Rmain were often very similar, especially at temperatures below 12.80 C and at the highest




temperature of 19-5' C. The energy of metabolism was never significantly lower than the maintenance metabolism, and significantly higher values occurred when the ratio of energy intake to maximum energy intake was greater than about 090 at 12.80 C, 045 at 15? C and 0 30 at 17-80 C. Therefore, as temperature increased from 12-8 to 17.80 C, the level of the energy intake at which R was significantly higher than Rmajn progressively decreased.

It is clear, however, that the metabolic requirements of trout on a reduced energy intake of less than 90%0 of the maximum intake were remarkably close to maintenance metabolism in the temperature range 3-8-12-80 C. These trout always met their requirements for maintenance metabolism and if these requirements were not fulfilled by the daily energy intake, then the extra energy was obtained from body tissues. Although no general equation was developed to estimate the metabolic requirements of trout on reduced rations, the equations for estimating maintenance metabolism provide close estimates of these requirements for trout on reduced rations at temperatures below about 130 C.

Gross efficiency, optimum energy intake and the scope for growth Gross efficiency (KG) is the ratio of the increase in the total energy content of the fish

5000 -

,,100 /

200 I 3 5 10 15 20 22

TO C

FIG. 7. Relationship between the maximum, optimum and maintenance energy intake (C cal day- 1) for trout of 50 g initial weight.

(positive AB) to the daily energy intake (C) and is usually expressed as a percentage. The gross efficiency for trout on maximum rations was unaffected by variations in body weight (Table 3) and the same was true for trout on reduced rations. Therefore the extensive data for trout of initial weight close to 50 g were used to illustrate the effects of temperature and energy intake on the gross efficiency. Isopleths of gross efficiency were drawn over the curves (from Fig. 5) relating AB to temperature at fixed levels of energy intake (Fig. 6 (a) ). Gross efficiency exceeded 33%0 in a zone within 8-11? C, and then decreased with both increasing and decreasing temperature, energy intake and AB. A comparison was made with isopleths of gross efficiency calculated in terms of wet weight (Fig. 6 (b) from Fig. 8 in Elliott 1975d). The zone of maximum efficiency and the general pattern of the isopleths were very similar in both units, but the actual levels of efficiency were much higher when measured in terms of energy values rather than wet weight. These



J. M. ELLIOTT 937

differences in gross efficiency were chiefly due to differences in the energy content of the trout and their food, rather than differences in water content: mean values for trout and Gammarus were 75.600 and 76 10% for water content, 5787 cal g'- 1 and 4438 cal g- 1 (dry weight) for energy content. Therefore, when gross efficiency was maximal, the weight of Gammarus eaten by the trout was about five times the increase in the weight of the fish (KG = 20%), but the energy content of the food was only about three times the increase in the total energy content of the fish (KG = 330O).

The optimum energy intake (C0p, cal day- 1) is the energy intake which produces the greatest increase in the energy content of the fish for the least energy intake, and is

Table 7. Comparison between the daily energy intake (C cal day 1) of trout on reduced rations and values estimated from eqn (14); T? C is the water temperature, W1 g is the initial weight of the trout, Pg?/ is the growth rate expressed as a percentage of the maximum growth rate (Pg = l00ABIABmax), and 9500 confidence limits for est. C were calculated from equations given

in Elliott (1975d)

TO C W1 g Pg% Act. C cal. Est. C cal. (95%, C.L.) 3.8 50 09?0 03 0 231?2 273 (196-379) 5 6 11 68 40 159 152 (110-210)

5033+?008 41 479?1 463 (351-611) 90 34 44 750 720 (545-950)

256 67 40 1645 1571 (1190-2074) 7*1 50 58?0 03 89 941?1 912 (691-1204) 9*5 11V83 61 350 338 (291-392)

50-79?0-17 61 1005+ 8 1008 (869-1169) 90 87 63 1572 1566 (1350-1817)

257-93 68 3627 3619 (3093-4234) 12*8 11-76 4 295 314 (268-367)

11 75 80 665 665 (568-778) 50 84?0 09 4 933? 17 963 (830-1117) 50'94?0.11 81 1808+9 1889 (1628-2191) 86 24 4 1411 1442 (1243-1673) 88 36 82 2778 2902 (2502-3366)

250 21 6 3407 3318 (2860-3849) 246 36 79 6200 6077 (5239-7049)

15.0 11 70 39 677 606 (522-703) 11 72 81 976 934 (805-1083) 50 11?0 03 38 1857?44 1794 (1547-2081) 50 10?0 04 86 2761?24 2725 (2349-3161) 91 46 39 2778 2790 (2405-3236) 91 73 74 4342 3885 (3349-4507)

248 28 40 6704 5993 (5122-7012) 254 67 74 9840 8231 (7035-9630)

17 8 50 76?0 05 44 1874?4 1716 (1479-1991) 50-77?0 03 53 3573? 1 1777 (1532-2061)

therefore the energy intake at which gross efficiency is maximal. The optimum ration (Dopt mg dry weight, day -1) can be estimated from equations developed in Elliott (1975d), and therefore the products of these equations and the mean energy value of Gammarus provided new equations for estimating C.pt (eqn (13) in Table 5). The relationship between the maximum, maintenance and optimum energy intakes for trout of similar weight is illustrated in Fig. 7. Optimum and maximum energy intakes were not significantly different in the range 3 8-6 8? C, they diverged markedly at temperatures above 6 8? C and then converged to a similar value at 19.50 C.

The range between the maintenance and maximum energy intakes defines the 'scope




for growth', i.e. the range within which the total energy content of the trout increases. As Cmax and Cmain can be estimated from eqns (1) and (11), the scope for growth can be estimated for trout in the weight range 10-300 g and the temperature range 3-8-19-5' C. The energy intake within the scope for growth can be estimated from the product of the energy value of Gammarus and the equation developed to estimate the mean weight of food eaten in a day (eqn (2) in Elliott 1975d). The new equation (eqn (14) in Table 5) describes the relationship between the daily energy intake (C cal day-') and the body weight (W g), water temperature (T? C) and growth rate expressed as a percentage of the maximum growth rate (Pg0 %). Growth rates were expressed in terms of wet weight in the original equation, but the increases in total energy content were used to calculate Pg in eqn (14), i.e. Pg = 100 AB/ABmax where ABmax was calculated from eqn (6), using Cmax and Rmax.

The adequacy of eqn (14) for the trout on reduced rations was tested empirically by comparing estimated values of C with actual values obtained in the experiments (Table 7).

Table 8. Comparison between the actual and estimated values of the major components of the energy budget for trout feeding on different food organisms at 12-2 + 0.80 C; W1 g is

the initial weight of the trout and D mg is the mean dry weight of the daily ration

W1 g D mg Ccal F+Ucal ABcal KG% R cal Maximum rations Baetis rhodani (Pictet) Act. 247-12 1632 9629 2985 2275 24 4369

Est. 1924 8540 2647 2374 28 3519 Chironomidae Act. 11-31 178 962 299 273 28 390

Est. 207 919 285 267 29 367 Hydrop,yche spp. Act. 248&23 1501 8553 2654 2195 26 3704

Est. 1916 8504 2636 2364 28 3504 Tenebrio molitor L. Act. 50-71 389 2634 817 899 34 918 (mealworms) Est. 604 2692 835 771 29 1086

Reduced rations Baetis Act. 250-31 1087 6413 1825 1526 24 3062

Est. 1248 5039 1360 1526 30 2153 Chironomidae Act. 11-42 73 394 103 55 14 236

Est. 81 343 90 55 16 198 Hydropsyche Act. 249-08 798 4547 1209 942 21 2396

Est. 1011 4112 1110 942 23 2060 Mealworms Act. 50-66 141 955 243 0 712

Est. 211 865 182 0 683

There was good agreement between the actual and estimated values in most of the comparisons, and the actual values lay within the estimated 9500 confidence limits. Actual values were higher than the upper estimated limit in only two of the comparisons (W1 = 254-67 g at 15.00 C, W1 = 50 77 g at 17-8' C). In several experiments, the value of Pg was greater than 9500, but the values of C (not included in Table 7) were very close to the maximum energy intake estimated from eqn (1). It was therefore concluded that eqn (14) was a good equation for describing the relationship between the daily energy intake and the increase in the total energy content of trout feeding on reduced rations.

Trout feeding on different food organisms

A small number of experiments were performed with the food organisms listed in Table 8. The experimental procedure and the construction of the energy budgets were the same as those used in the experiments with Gammarus as the food organism. Energy



J. M. ELLIOTT 939

values used to convert the dry weight of each food organism into energy units are given in Elliott (1976b). The mean dry weights of the rations (D mg day-') were compared with values estimated from equations developed for trout feeding on Gammarus, and there was good agreement between the actual and estimated values of D for Baetis and Chiro- nomidae with actual values always within the 9500 confidence limits of the estimated values (see also Elliott 1975c,d). No similar agreement was found for Hydropsyche and mealworms, and actual values were much smaller than estimated values. The estimated values of C, AB and R for trout on maximum rations were determined from eqns (1), (6) and (8) respectively, and the estimated values of F+ U were determined from eqns (2) to (5) for all trout. Before C for trout on reduced rations could be estimated from eqn (14),

Table 9. Comparison between the actual and estimated values of the mean dry weight (Dmax mg day -) and the mean energy content (Cmax cal day- 1) of meals of different food organisms eaten by trout on maximum rations; T? C is the water temperature, WI g is the initial weight of the trout, estimated values of Dmax were calculated from equations given in Elliott

(1975c) and estimated values of Cmax were calculatedfrom eqn (1)

Dmax mg Cma. cal To C W1 g Act. Est. Act. Est.

Baetis 3.8 ?0.3 50410 51 63 302 280 741?0-6 90410 302 364 1788 1615

15 1?07 50415 722 889 4274 3945 17 8?0 7 11 68 378 393 2238 1744

Chironomidae 3 8?0 3 11 49 18 21 97 93 7 1?0 6 50 23 201 235 1086 1043

15 1?07 9023 1163 1376 6283 6107 17 8?0 7 11V26 321 383 1734 1700

Oligochaetes 3 8?0 3 248&20 193 215 967 954 (Lumbricidae) 741?0 6 50-12 210 234 1052 1038

12.2+0.8 93-21 834 939 4177 4167 15*1?0+7 11-44 276 305 1382 1354 17*8?0*7 250-20 3532 3969 17688 17614

Protonemura meyeri 741+0.3 11-42 68 78 358 346 (Pictet) 12.2?0 8 50 34 516 599 2716 2658

1541?07 9025 1162 1367 6116 6067 Hydropsyche 3 8? 03 50-22 47 64 268 284

741?0 6 90 38 288 362 1641 1607 15 1?07 50-36 681 890 3880 3950 17-8?0-7 251-26 3082 3979 17561 17659

Mealworms 38 ? 03 90 42 65 99 440 439 741?0 6 250 83 512 775 3467 3439

15 1?07 11 46 188 302 1273 1340 17 8?0-7 50 32 779 1176 5275 5219

it was necessary to assume that AB was the same for both actual and estimated energy budgets.

There was generally good agreement between the actual and estimated values of the major components of the energy budgets (Table 8). Differences between the values of the daily energy intake (C cal) for trout feeding on Hydropsyche or mealworms were much smaller than differences between corresponding values for the weight of the ration (D mg). The only marked discrepancies were in the energy butdgets with Baetis as the food organism. Although the actual and estimated values of AB were similar, the values of C, F+ U and R were consistently higher for Baetis in both comparisons. There was therefore




a suggestion that Baitis was a less efficient food than Gammarus. As only two comparisons are available, this conclusion can only be regarded as tentative.

Although no more complete energy budgets were constructed, it was possible to compare the daily energy intakes of trout feeding on different food organisms (Table 9). The growth rates of these trout were very similar to rates estimated from equations developed from extensive data for trout feeding on Gammarus (Elliott 1975c). This similarity between actual and estimated growth rates occurred even when the food was Hydropsyche or mealworms and the weight of the ration was much lower than the corresponding value for Gammarus (cf. values of Dmax in Table 9). When the daily food intake was expressed in terms of energy units, there was no corresponding difference between actual and estimated values (cf. values of Cmax). Therefore the daily energy intake was similar in spite of differences in the weight of different food organisms eaten in a day. This similarity suggests that there is a feedback system which regulates the energy intake with different foods. It has already been shown that the proportion of the daily energy intake lost in the waste products (F+ U) is very similar for different food organisms and therefore the proportion available for growth and metabolism remain fairly constant (Elliott 1976b). Therefore, it is possible to explain why the growth rates were similar even when the weight of the ration was much lower than the expected value. Once again, the comparisons suggest that Baetis was an exception with actual values of Cmax consistently higher than estimated values. Although some food organisms such as Baetis may be possible exceptions, it can generally be concluded from these limited comparisons that the equations developed in the present study are applicable to trout feeding on different food organisms.

DISCUSSION

Although there are no comparable energy budgets for salmonids, different components of the energy budgets of fishes have been studied and this work has been recently reviewed by Beamish et al. (1975). A detailed comparison of all this work with the present study would not lead to any general conclusions and therefore this discussion is confined to an examination of some of the quantitative aspects.

The metabolic requirements of the trout were estimated indirectly and not by measur- ing rates of oxygen consumption. Paloheimo & Dickie (1965, 1966a,b) concluded that the estimation of metabolism from food intake and growth studies is preferable to its estimation from oxygen consumption because the former can be recorded over extended periods whereas the latter is experimentally exacting, necessitates the confinement of the fish in special apparatus and is usually recorded only over short periods of time. Beamish (1964a,b) has shown that the problems in obtaining reliable data on metabolism, especially standard metabolism, can be formidable, particularly because of the complex relationship between metabolism and factors such as oxygen tension and the activity of the fish. There are therefore several good reasons for estimating metabolism indirectly from feeding experiments and one major advantage of this method is that it allows the measure- ment of the effects of different foods and ration sizes on metabolism and growth.

In their extensive review of the literature on the relationship between metabolism and body weight in fish, Paloheimo & Dickie (1966a) concluded that values of the weight exponent were very similar in oxygen consumption experiments and feeding experiments in which metabolism was measured indirectly. Most values were in the range 07-09 and a mean value of about 0 8 provided an adequate general description of the relationship



J. M. ELLIOTT 941

between metabolism and body weight for a majority of species under more or less constant, non-stress conditions. Winberg (1956) analysed the results of thirty studies relating oxygen consumption to body weight for different species of salmonids, and he found that the mean value of the weight exponent was 0 76 + 0 032. Ricker (1973) proposed that the geometric mean estimate of the functional regression (GM regression coefficient) was more appropriate than the predictive regression coefficient used by Winberg, and he calculated new values of 0 778 and 0 795 for the predictive and GM coefficients respec-

5000 (a) Ccol (b)

4000 - Cc)/ \ ,W

1000 10 1

500-

T?C

FIG. 8. (a) Comparison between estimates of the maintenance ration (CB-cal day-'1) from Brown (1946), the maximum energy intake in one meal (CM cal day-'1) from Elliott (1975a) and the maximum and maintenance energy intakes (estimated from eqns (1) and (11)). (b) Comparison between Winberg's estimates of the daily energy intake required for resting metabolism (W1 cal day-'), twice resting metabolism (W2 cal day-') and the maximum and maintenance energy intakes. (c) Comparison between Winberg's estimates of the energy required for resting metabolism (WR cal day-') and th~e energy required for standard, maintenance and maximum metabolism (estimated from eqns (9), (12) and (8) ). (d) Comparison between new estimates of W, and W2 and the maximum, optimum and

maintenance energy intakes. All values are calculated for trout of 50 g live weight.

tively. Unfortunately, Ricker's calculations do not appear to be correct and the actual values for the salmonid data are O 761 for the predictive regression (i.e. the same as that given by Winberg but to more significant figures) and O 779 for the functional regression. The predictive regression coefficient was used to estimate the weight exponent in the present study. Values ranged from O 716 to 0 770 and appeared to be lower at lower metabolic levels with ranges of OS756-OS77O for Rmax, 0x721-0x723 for Rmain and 0n731- 0 734 for Rs (Tables 2 and 5). All these values are close to Winberg's mean value of 0*76.




Therefore the values of the weight exponent in the present study were very close to values obtained by other workers in studies of oxygen consumption in salmonids (cf. also Graham 1949; Job 1955).

In her detailed work on growth of brown trout, Brown (1946) determined the maintenance ration for 50 g trout fed on a mixture of minced meat and liver at different temperatures. Assuming that the energy content of the food was 1 56 cal mg 1, her values have been converted into energy units (CB cal day 1) and compared with estimates of the maximum and maintenance energy intakes (Fig. 8(a)). Brown's estimates of the maintenance energy intake were much higher than those obtained in the present study, but were very close to the energy intake obtained in one satiation meal (CM cal day-1). One possible explanation for this discrepancy between the two estimates of the maintenance energy intake is that the experimental approach was very different in the two studies. Brown measured the maintenance ration directly by adjusting the daily ration until the trout were neither gaining nor losing weight, whereas the values for maintenance in the present study were obtained by interpolation from the curves relating AB to the daily energy intake at each temperature (Fig. 4(a)).

Winberg (1956) developed a basic equation relating oxygen consumption to body weight: Q = aWb where Q ml h-' is the oxygen consumed by a fish at a standard temperature and Wg is the live weight of the fish. He further demonstrated that the values of the level of metabolism (a) and weight exponent (b) were fairly constant for different taxonomic groupings with values for Salmonidae of b = 0-76 and a = 0-498 at a body weight of 1 g and a standard temperature of 200 C. The value of the constant a, and hence the level of metabolism, at various temperatures follows the curve of Krogh (1916) and therefore it is possible to estimate the resting metabolic rate of a trout at any combination of body size and temperature. Winberg assumed that the energy equivalent (Qox) for converting rate of oxygen consumption into energy units was 5 cal ml-' oxygen consumed, that the energy losses in the waste products formed 20% of the energy intake, and that the metabolic rate of a fish in nature is about twice the resting level. Therefore two estimates of the daily energy intake required for metabolism can be made, one based on resting metabolism (W1 cal day- 1) and the other based on twice that value (W2 cal day-1). A comparison of these values with estimates of the maintenance and maximum energy intakes shows that W1 lies very close to the maintenance value in the temperature range 3.8-19.50 C (Fig. 8(b)).

It has already been shown that Winberg's value for Qox is too high for a carnivorous fish that utilizes ammonia as its chief excretory product and a value of 4-63 cal ml-' oxygen consumed is more appropriate (Elliott & Davison 1975). This value was applied to Winberg's equation for salmonids and a reanalysis of the original data provided slightly different estimates of the two constants with b = 0-761 and a = 0A491. These new values were used to estimate the energy required for resting metabolism (WR cal day-1). A comparison of WR with estimates of the energy required for standard, maintenance and maximum metabolism shows that WR lies between the standard and maintenance values within most of the temperature range 3-8-19-50 C (Fig. 8(c)). It has already been shown that Winberg's estimate of energy losses in the waste products is too low for trout and that a mean value of 28% is more appropriate (Elliott 1976b). Therefore this higher percentage was used to calculate new values of W1 and W2. As the new Q,x value is lower and the percentage for energy losses is higher than Winberg's values, the new estimates of W1 and W2 are very simiiar to those provided by Winberg's original equation (cf. Fig. 8(b) and (d)). However, it is thought that the assumptions inherent in the new calcula-



J. M. ELLIOTT 943

tions are more realistic than those proposed by Winberg. A comparison of the new values of W1 and W2 with various levels of energy intake shows that W1 is very close to the mainte&nance value in the range 3-8-19-5? C and W2 is fairly close to the optimum energy intake in the range 6-5-16-5' C (Fig. 8(d)). Therefore, if the new values of Q.. and

5000

o 100 , I,,,, I ,., I ' I ' / -I ' --'

4000

2000

3 5 10 15 20 22 T?C

FIG. 9. Division of the major components of the energy budget for trout of 50 g live weight: (a) energy values on logarithmic scale; (b) energy values on arithmetic scale.

energy losses are used in the calculations, Winberg's basic equation for salmonids provides approximate estimates of the maintenance and optimum energy intakes of brown trout in the temperature ranges 3i8-l9*5? C and 6*5-16*5o C respectively.

The equations developed in the present study have been used to construct a figure that illustrates the relative changes in the major components of the energy budget (Fig. 9).




Although the energy values are usually shown on logarithmic scales in this study, this presentation can be misleading and therefore these values are also shown on arithmetic scales in the figure. For example, the energy losses in the waste products appear to be fairly constant on a log scale in the range 3.8-17.80 C, but actually increased with increasing temperature in this range. It is almost impossible to assess changes in AB on a log scale but the arithmetic scale shows the usual relationship between growth and temperature with maximum values at 12-13? C.

The 'scope for activity' (i.e. R-Rj) increased markedly with temperature from almost zero at 3.80 C to a maximum at 17 80 C and then decreased to almost zero at 19.50 C (Fig. 9). The scope for activity also increased with temperature in rainbow trout (Salmo gairdneri Richardson) and was highest at 150 C and 200 C for hatchery trout and wild trout respectively (Dickson & Kramer 1971). As the experiments were performed at intervals of 50 C, these values are comparable to that of 17.80 C for brown trout. Other workers have found that the metabolic requirements of fish kept on maximum rations may be three to five times higher than those of fish on maintenance rations (references in Paloheimo & Dickie 1966a; Warren & Davis 1967).

The increase in the scope for activity is obviously due to an increase in both the energy required for activity, including swimming (Rj), and the energy required for the processes of digestion, movement and deposition of food materials, including specific dynamic action (Rd). Unfortunately, these two components could not be estimated separately in the present study, but it was obvious in the feeding experiments that the activity of the trout increased with temperature up to about 190 C and then was limited to short bursts of swimming at temperatures above 190 C. The activity of fish has proved difficult to measure and workers have often disagreed on the appropriate terms in which to discuss activity (see review of Beamish & Dickie 1967). The energetic costs of moderate levels of swimming activity are relatively low (Brett 1964; Brett & Sutherland 1965), and Warren & Davis (1967) concluded that it is unlikely that swimming activity for feeding accounts for a large part of the total metabolic rate of growing fish. Therefore the increase in the scope for activity in the brown trout was probably due chiefly to an increase in Rd.

Energy requirements for absorption, digestion, transportation and deposition of food materials are distinct from those for specific dynamic action but experimentally difficult to separate. Therefore the term 'apparent specific dynamic action' can be used to cover all these energy requirements (Beamish 1974) and this term is equivalent to Rd. Very little is known about this component of the energy budget in fish and no information is available in the present study. Some information is urgently needed on the separate energy requirements of activity and apparent specific dynamic action in brown trout.

Finally, it is worth noting that the time taken to complete the work described in this series of papers on feeding and growth in brown trout is equivalent to about twenty-one man-woman years. In spite of this effort, many questions remain unanswered.

ACKNOWLEDGMENTS

I wish to thank all those who have helped me with this work, especially Dr H. Decamps for performing many laborious calculations and Mrs P. A. Tullett for all her assistance in the analysis of the data and the preparation of this paper.

SUMMARY

(1) Energy budgets were calculated for brown trout (live weight 5-281 g) fed on various



J. M. ELLIOTT 945

ration sizes ranging from zero to maximum rations at different water temperatures (range 3-8-21P70 C).

(2) Both the weight of the trout and the water temperature affected the five components of the energy budget: daily intake (C cal day- 1), losses in faeces (F cal dayf -) and excretory products (U cal day-'), change in total energy content of the fish (AB cal day-'), metabolism (R cal day-'). Equations were developed to estimate these components for trout on maximum rations. Of the three components of metabolism, the energy required for activity (Ra cal day-'), and for the apparent specific dynamic action (Rd cal day') could not be separated, but the energy required for standard metabolism (R. cal day ) was estimated from equations developed from the data for trout on zero rations.

(3) Energy budgets were also constructed for trout on reduced rations. As energy intake decreased, the optimum temperature for maximum values of AB also decreased, and the temperature range over which growth occurred (i.e. AB was positive) also decreased. Equations were developed to estimate the maintenance energy intake (Cmain cal day-1) and the energy required for maintenance metabolism (Rm.i cal day-'). Estimates of Rmain provided close estimates of the metabolic requirements of trout on reduced rations at temperatures below 130 C. All these equations were applicable to trout feeding on a variety of food organisms.

(4) The gross efficiency of energy utilization exceeded 33%O in a narrow zone of energy intake and a temperature range of 8-11 'C. It then decreased with both increasing and decreasing temperature, energy intake and change in the total energy content of the trout. Equations were developed to estimate the optimum energy intake, i.e. the most efficient energy intake which produces the greatest increase in AB for the least energy intake, and the 'scope for growth' between the maintenance and maximum energy intakes.

REFERENCES

Beamish, F. W. H. (1964a). Respiration of fishes with special emphasis on standard oxygen consumption. II. Influence of weight and temperature on respiration of several species. Can. J. Zool. 42, 177-88.

Beamish, F. W. H. (1964b). Respiration of fishes with special emphasis on standard oxygen consumption. III. Influence of oxygen. Can. J. Zool. 42, 355-66.

Beamish, F. W. H. (1974). Apparent specific dynamic action of largemouth bass, Micropterus salmoides. J. Fish. Res. Bd Can. 31, 1763-9.

Beamish, F. W. H. & Dickie, L. M. (1967). Metabolism and biological production in fish. The Biological Basis of Freshwater Fish Production (Ed. by S. D. Gerking), pp. 215-42. Blackwell Scientific Publica- tions, Oxford.

Beamish, F. W. H., Niimi, A. J. & Lett, P. F. K. P. (1975). Bioenergetics of teleost fishes: environmental influences. Comparative Physiology-Functional Aspects of Structural Materials (Ed. by L. Bolis, H. P. Maddrell & K. Schmidt-Nielsen), pp. 187-209. North-Holland, Amsterdam.

Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. J. Fish. Res. Bd Can. 21, 1183-226.

Brett, J. R. & Sutherland, D. B. (1965). Respiratory metabolism of pumpkinseed (Lepomis gibbosus) in relation to swimming speed. J. Fish Res. Bd Can. 22, 405-9.

Brown, M. E. (1946). The growth of brown trout (Salmo trutta L.). III. The effect of temperature on the growth of two-year-old trout. J. exp. Biol. 22, 145-55.

Dickson, W. & Kramer, R. H. (1971). Factors influencing scope for activity and active and standard metabolism of rainbow trout (Salmo gairdneri). J. Fish. Res. Bd Can. 28, 587-96.

Elliott, J. M. (1972). Rates of gastric evacuation in brown trout, Salmo trutta L. Freshwat. Biol. 2, 1-18.

Elliott, J. M. (1975a). Weight of food and time required to satiate brown trout, Salmo trutta L. Fresh- wat. Biol. 5, 51-64.

Elliott, J. M. (1975b). Number of meals in a day, maximum weight of food consumed in a day and maximum rate of feeding of brown trout, Salmo trutta L. Freshwat. Biol. 5, 287-303.

Elliott, J. M. (1975c). The growth rate of brown trout (Salmo trutta L.) fed on maximum rations. J. Anim. Ecol. 44, 805-21.



946 Energetics of brown trout Elliott, J. M. (1975d). The growth rate of brown trout (Salmo trutta L.) fed on reduced rations. J.

Anim. Ecol. 44, 823-42. Elliott, J. M. (1976a). Body composition of brown trout (Salmo trutta L.) in relation to temperature and

ration size. J. Anim. Ecol. 45, 273-89. Elliott, J. M. (1976b). Energy losses in the waste products of brown trout (Salmo trutta L.). J. Anim.

Ecol. 45, 561-80. Elliott, J. M. & Davison, W. (1975). Energy equivalents of oxygen consumption in animal energetics.

Oecologia (Berl.), 19,195-201. Graham, J. M. (1949). Some effects of temperature and oxygen pressure in the metabolism and activity

of the speckled trout, Salvelinus fontinalis. Can. J. Res. Sect. D, 27, 207-88. Ivlev, V. S. (1939). Balance of energy in carps. Zool. Zh. 18, 303-18. (In Russian with English summary.) Job, S. V. (1955). The oxygen consumption of Salvelinusfontinalis. Univ. Toronto Bio. Ser. No. 61. Publ.

Ontario Fish. Res. Lab., No. 73, pp. 39. Krogh, A. (1916). Respiratory Exchange of Animals and Man. Longmans, Green, London. Paloheimo, J. E. & Dickie, L. M. (1965). Food and growth of fishes. I. A growth curve derived from

experimental data. J. Fish. Res. Bd Can. 22, 521-42. Paloheimo, J. E. & Dickie, L. M. (1966a). Food and growth of fishes. II. Effects of food and temperature

on the relation between metabolism and body weight. J. Fish. Res. Bd Can. 23, 869-908. Paloheimo, J. E. & Dickie, L. M. (1966b). Food and growth of fishes. III. Relations among food, body

size, and growth efficiency. J. Fish. Res. Bd Can. 23, 1209-48. Ricker, W. E. (Ed.) (1971). Methods for Assessment of Fish Production in Fresh Waters, 2nd edn. IBP

Handbook No. 3. Blackwell Scientific Publications, Oxford. Ricker, W. E. (1973). Linear regressions in fishery research. J. Fish. Res. Bd Can. 30, 409-34. Warren, C. E. & Davis, G. E. (1967). Laboratory studies on the feeding, bioenergetics, and growth of fish.

The Biological Basis of Freshwater Fish Production (Ed. by S. D. Gerking), pp. 175-214. Blackwell Scientific Publications, Oxford.

Winberg, G. G. (1956). Rate of Metabolism and Food Requirements of Fishes. Belorussian State University, Minsk. (Translated from Russian by Fish. Res. Bd Can. Transl. Ser. No. 194, 1960.)

(Received 9 March 1976)



APPENDIX

Water temperature (T? C), initial weight of fish (W1 g live weight) and the major components of the energy budget for trout on reduced rations; 95% confidence limits are given for all experiments in which more than one trout was used

To C W1 g C cal F cal U cal AB cal R cal R, cal Ra+ Rd cal

3-8 50 09?0 03 231+2 61?1 10i<1 0+1 160?2 152+<1 9+2 5-6 11-72 80 15 5 -24 84 72 12

11-68 159 38 9 22 90 74 16 50-19?0-05 249+ 6 47?1 16? <1 -72?1 258 6 211+ <1 47+6 50-33?0-08 479+1 114?1 27? <1 66?1 273?1 218?3 55+3 88-22 381 72 23 -101 387 320 67 90 34 750 179 42 107 422 332 90

252-36 858^ 162 53 -236 879 696 183 256-67 1645 391 91 207 956 716 240 .4

7-1 50-50?0 04 461?4 85+1 32? <1 -11?1 355?1 283? <1 72+1 50 58+0 03 941+1 227+<1 58+<1 313+1 343?1 299+<1 44+<1

9 5 11-70 172 28 15 -10 139 121 18 11-83 350 68 28 107 147 132 15 50-58+0-08 525? 6 84?1 45? <1 -26+1 422?4 354+ < 1 68+3 o 50-79+0-17 1005?8 193?2 80?1 308+ <1 425+6 374?1 51?6 H 89-36 800 128 69 -44 647 536 111 90-87 1572 304 124 485 659 560 99

249-52 1962 322 170 -101 1571 1139 432 257-93 3627 717 283 1105 1522 1199 323

12-8 11-76 295 44 30 9 212 168 44 11-75 665 119 62 241 243 198 45 11-82 983 210 85 316 372 204 168 50-84?0 09 933 ?17 140? 3 95+ 2 32? 3 665?12 488?1 177?12 50-94+0-11 1808?9 322?2 171?1 653?2 663?8 531+1 132?9 51-02?0-12 2672+13 562?13 234?2 912+2 964?26 550?1 415?26 86-24 1411 213 144 46 1008 726 282 88-36 2778 497 262 998 1021 793 228 87-63 4210 921 360 1312 1617 798 819

250-21 3407 521 346 158 2382 1562 820 246-36 6200 1130 579 2021 2470 1638 832 258-63 9011 1935 778 2879 3419 1715 1704



00

Appendix (cont.)

TO C W1 g C cal Fcal U cal AB cal R cal R. cal Ra+Rd cal

15.0 11-80 302 42 38 -46 268 198 70 11-70 677 111 72 107 387 216 171 11-72 976 180 98 243 455 234 221 50-11+0-02 978?5 136?1 112?1 -145?49 875?49 583?5 292?54 50-1+0-03 1857?44 295?9 199?4 297?2 1065?30 620? <1 444?30 50-10?0-04 2761?24 507?6 277?2 684?2 1293?15 632? <1 660?15 90-21 1470 202 169 -206 1305 891 414 91-46 2778 437 300 482 1559 943 616 91-73 4342 795 436 946 2165 981 1184

252*31 3692 521 419 -583 3335 1902 1433 24828 6704 1094 711 1035 3864 1959 1905 254-67 9840 1850 977 2007 5006 2027 2979

17-8 50 74?0 03 905+3 114? <1 118? <1 -362+4 1035?5 746? <1 289?5 50-76?0-05 1874?4 263?1 232_ <1 113+1 1267?4 794+ <1 473?4 50-77?0-03 3573?1 614?1 401_ <1 138+6 2419?6 798?1 1621?8

19-5 11-79 319 54 38 -173 400 278 122 50x90+0-13 870?5 136?1 107? <1 -470?9 1097?12 878?3 220?15 86-21 1319 212 160 -708 1655 1263 392

278-23 3152 500 383 -1730 3999 3042 957



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