होम Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and... Energy conversion efficiency in fish: The influence of food intake and temperature on K-lines at...
Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 1977 Vol. 114; Iss. 2
J. comp. Physiol. 114, 191-202 (1977) Journal of Comparative Physiology. B 9 by Springer-Verlag 1977 Energy Conversion Efficiency in Fish: The Influence of Food Intake and Temperature on K-Lines at Rations Close to Maintenance P.M.C. Davies and Susan M. Massey Department of Zoology, University of Nottingham, Nottingham NG7 2RD, England Received November 2, 1976 Summary. Data relating to growth in goldfish at ration levels very close to maintenance are used to calculate maintenance rations and food conversion efficiencies (K) in energetic terms. The relationship between maintenance metabolism and temperature is logarithmic, with a Q10 of 2.2 (12-28 ~ A significant positive relationship is apparent between I n K and ration on which the influence of temperature is equivocal. The meaning of this in relation to the findings of other workers is discussed. Introduction In the decade since Paloheimo and Dickie's (1966) extensive re-analysis of experimental fish growth data, doubt has grown about the general validity and ecological applicability of the 'K-line' growth model they proposed (Warren and Davis, 1967; Rafail, 1968; Brett etal., 1969; Kerr, 1971a, b; Kelso, 1972; Elliott, 1975; Staples, 1975). Their examination of the results of several independent laboratory studies of fish growth revealed, in almost all cases over a wide range of species, that gross growth efficiency (K), expressed logarithmically, was linearly and negatively related to ration size, and that temperature, while influencing levels of gross metabolic turnover, changed neither the slope nor the position of this relationship (termed by Paloheimo and Dickie the 'K-line'). Diet structure, on the other h a n d - i n particular, food particle size - and salinity had a pronounced effect on both parameters of the K-line (Paloheimo and Dickie, 1966). Subsequent work has tended either to confirm this relationship (LeBrasseur, 1969), to qualify it in some way (Warren and Davis, 1967; Pandian, 1967; Rafail, 1968; Brett etal., 1969; Kerr, 1971a, b; K; elso, 1972; Elliott, 1975), or to suggest reasons for questioning its general validity and predictive value when applied to natural fish populations (Staples, 1975). One of the principal limitations of the K-line appears to be that it relates to growth sustained by relatively high levels of food consumption, and takes Abbreviation." dbw~ dry body weight 192 P.M.C. Davies and S.M. Massey no a c c o u n t o f c o n v e r s i o n u n d e r c o n d i t i o n s o f severely restricted f o o d s u p p l y (Rafail, 1968; Brett et al., 1969; K e r r , 1971a; Elliott, 1975). Since K at m a i n t e n ance m u s t be zero, t h e o r e t i c a l analysis p r e d i c t s the existence o f a positive p h a s e o f the K - l i n e i m m e d i a t e l y a b o v e m a i n t e n a n c e ( K e r r , 1971 a), rising to a n inflection at the c o m m e n c e m e n t o f the negative phase. This inflection c o r r e s p o n d s to the r a t i o n at which g r o w t h efficiency is m a x i m a l (' o p t i m u m r a t i o n ' ) . M a x i m a o f this k i n d have o n l y very rarely been d e t e c t e d in fish g r o w t h studies (Brett et al., 1969; Elliott, 1975). T h e d a t a p r e s e n t e d here are d e r i v e d f r o m an e x p e r i m e n t a l study o f ' d i g e s t i v e ' o r ' energy a b s o r p t i o n ' efficiency over the p e r i - m a i n t e n a n c e range, as c o n d i t i o n e d by r a t i o n size, t e m p e r a t u r e a n d c r o w d i n g (reports in p r e p a r a t i o n ) . Since m a n y o f o u r fish grew d u r i n g the course o f these experiments, the a c c u m u l a t i n g d a t a p r o v i d e d a u n i q u e o p p o r t u n i t y for e x a m i n i n g the i n t e r a c t i o n of K, r a t i o n size a n d t e m p e r a t u r e at feeding levels very close to m a i n t e n a n c e . I n the hope, therefore, o f s h e d d i n g s o m e light on the q u e s t i o n o f low i n t a k e energy c o n v e r s i o n efficiency, the results o f this e x a m i n a t i o n are s u m m a r i s e d below. Materials and Methods The basic experimental and pre-experimental procedures used in this investigation were modelled on methods developed in an earlier study of goldfish energetics (Davies, 1964), and will be described in detail elsewhere. Briefly, they consisted in providing small groups of acclimatised, size-controlled goldfish (Carassius aurqtus L., 10-20 g body weight, 4 fish per group) weight-specific peri-maintenance rations (0.5-3.5% dry body weight per day) under regulated photothermal conditions at five different temperatures (12, 16, 20, 24 and 28 ~ and measuring the faecal output and weight change (final weight-initial weight) of each group over relatively short periods of time (maximum 21 days). Each group of four fish was maintained in a 280 x 410 mm Dexion plastic bin holding approximately 5 1 of water. A total of 137 groups were treated in this way. Energy values of food consumed, growth achieved and faeces produced were obtained using a Parr semi-micro bomb calorimeter. A sample of 39 fish from the experimental population was used to prepare standard curves relating wet to dry weight, and dry weight to total energy content, from which the energy values of observed growth increments could be calculated. Variables such as age, sex, colour, condition factor and inheritance, which could not easily be controlled directly, were controlled by randomisation. The fish were fed on a commercially prepared, granulated trout food ('Beta Trout Food', Cooper Nutrition Products Ltd., Witham, Essex, England), designed by the manufacturer to float on water. To reduce still further the risk of premature disintegration, the granules (mean diameter 3-5 mm) were coated with flexible collodion in the way described by Rozin and Mayer (1964). Observational checks on the fate of food pellets confirmed that no significant wastage of food occurred during the feeding experiments. The results were examined statistically by analysis of variance (ANOVAR) with the aid of a computer, using the GLIM package (Nelder, 1975). Results 1. Growth and Maintenance Scatter d i a g r a m s were p r e p a r e d relating g r o w t h rate ( % wet b o d y weight g a i n or loss p e r day) to r a t i o n at each e x p e r i m e n t a l t e m p e r a t u r e (Fig. 1), a n d to Energy Conversion Efficiency in Fish 193 4" A , 12~ 0., C. 2 0 ~ 9 0. 0"2 0 0"2 B. 16~ D. 2 4 ~ C 9 0-~ 0.' ; ~ 'i I I , I i 9 I ._~ I 0.; 0.2 u J= I ' s r I 0-4 I 1 "2 I I I 2 l I" 2 "8 0"4 1.2 I I 2 2"8 4. 0.4i E. 28 ~ C o 0-2 ! o ol L I L t ! 0"2 | 0-4 i u 0'4 Ration (~dry body weight.day i 1.2 I L 2 I i 2"8 -I ) Fig. l. The relationship between growth rate (weight change per cent per day') and ration (per cent dry body weight per day) at five experimental temperatures. The x-intercepts represent the maintenance ration (Rm) at each temperature. Each point represents the mean growth rate of four fish I 194 P.M.C. Davies and S.M. Massey Temperature (~ Fig. 2. The relationship between growth rate (weight change per cent per day) and temperature at three ration levels (R1, R2, R3 per cent dry body weight per day). The x-intercepts represent the maintenance temperature for each ration Table 1. Regression equations, x-intercepts (maintenance ration, R~) and A N O V A R results for the growth data represented in Figure 1 Experimental temp. (~ C) y = a + bx Rm (y=growth rate; x = r a t i o n ) (% dbw per day) 12 16 20 24 28 y= y= y= y= y= 1.02 1.70 1.60 2.19 3.39 - 0.0970 + 0.0946x -0.1281 + 0,075 lx -0.1624+0,1012x -0.2461 +0,1121x - 0.2530 + 0.0746x A N O V A R results: SS df M Sq. F p 1. Ration Residual 1.340000 2.408000 1 135 1.340000 0.017837 75.0 <0.01 2. Temperature Residual 0.575000 1.833000 4 131 0.143750 0.013992 10.3 <0.01 3. Ration• Residual 0.014000 1.819000 4 127 0.003500 0.014322 0.2 N.S. Energy Conversion Efficiency in Fish 195 Table2. Regression equations and ANOVAR results for the growth-temperature lines in Figure2 Ration (% dbw per day) R1 R2 R3 y = a + bx (y=growth rate; x = t e m p . ) 0.87 1.75 3.48 y=O.0914-O.0073x y=0.2457-0.0135x y=0.5471 - 0.0253x A N O V A R results SS df M Sq. 1. Temperature Residual 0.560 1.133 4 74 0.140 0.015 9.1 <0.01 2. 0.383 0,750 2 72 0.190 0.010 18.4 <0.01 0.220 0.530 8 64 0.028 0.008 3.3 <0.01 Ration Residual 3. Temperature x ration Residual F p 3 i 2 Y=0"12+ 0.67x ~ e " X 0 I 1 ] 2 t 3 Ration (e/odbw. day-I) Fig. 3. The influence of ration (per cent dry body weight per day) on the temperature sensitivity of growth (as measured by the slopes, AG/A T. 100, of the lines in Fig. 2) temperature at three ration levels (R=0.87, 1.75 and 3.48% dbw per d a y Fig. 2). Regression lines were fitted by the method of least squares, and the data subjected to a two-way analysis of variance. Regression equations and ANOVAR results are shown in Tables 1 and 2 respectively. Growth rate is influenced by both ration and temperature, but the relationship between growth and ration is independent of temperature (Fig. 1, Table 1). On the other hand, the relationship between growth and temperature is ration dependent (Fig. 2, Table 2). The slopes of the three lines in Figure 2, being measures of the influence 196 P.M.C. Davies and S.M. Massey 45 log y = 0.6947+0"0346x o ~ e p < 0"005 -- 35 E ~ 25 E~ ~ ~ 15 j o I 12 I I I 16 l 20 I I 24 I I 28 Temperature (~ Fig. 4. The influence of temperature on maintenance metabolism (cal/g fish- day -logarithmic scale). Qlo=2.2. Closed circles derived from the x-intercepts of Figure 1; open circles derived from the x-intercepts of Figure 2 of temperature on weight change, are related to ration in Figure 3. The relationship is linear o.*er the range studied. Since the observed growth rates were, in all cases, very small, the logarithmic transformation of weight change data was not necessary. Where the data are grouped (as in Fig. 1 A and B), ' grouped' and conventional regression analysis were found to give identical lines. Maintenance (M cal/g wet wt. d a y ) - the energy required to sustain routine physiological needs under conditions of zero growth-was calculated for each temperature from the maintenance ration (Rm % dbw per day) according to the relation M= p.Rm. C 100. W~ cal/g wet wt.day where p is the mean coefficient of energy absorption at each temperature (from unpublished daia: 0.8103, 0.8056, 0.8269, 0.8157, 0.8078, 0.8134, 0.8134 and 0.8134 respectively-see Fig. 4, in ascending order of temperatures), C is the energy value of the food (4195 cal/g), and W~ the wet weight equivalent of 1 dry g of fish~(i.e, the slope of the wet weight/dry weight standard curve, in this case 2.7108). Rmfor each of the experimental temperatures is given by the x-intercept of the corresponding growth line in Figure 1. The temperatures at which R1, Rz End R 3 become maintenance rations are given by the x-intercepts in Figure 2. Using these eight values of Rm, corresponding values of M and Log M were calculated and compared with temperature to establish the nature of the influence of temperature on maintenance metabolism. Lines were fitted by the method of least squares. The regression coefficient of the logarithmic relationship (Fig. 4) was found to be more highly significant (p < 0.005) than Energy Conversion Efficiency in Fish 197 Table 3. Regression equations and A N O V A R results for the K-lines in Figure 6 Experimental temp. (~ C) n y = a + bx (y = conversion efficiency; x = ration) 12 8 16 20 24 28 12 19 11 6 K= - 3.1422 + 0.3884R K= K= K= K= --4.1272+0.4994R -- 3.0155 + 0.2684R --2.7953 +0.0855R -- 4.4343 + 0.6430R A N O V A R results SS df M Sq. F p 1. Ration Residual 4.20 27.76 1 54 4.20 0.50 8.2 <0.01 2. Temperature Residual 3.35 24.41 4 50 0.84 0.49 1.7 N.S. 3. Ration x temperature Residual 0.77 23.64 4 46 0.19 0.51 0.4 N.S. ~0 y = - 10"3703 + 2.1195 x 50 iJ -g .:c v c~ =. 6 30 4 F- 10 I t I i I 5 10 15 20 25 Wet weight (g) Fig. 5. The relationship between total energy (kcai), wet weight and dry weight of goldfish. The equation shown describes the total energy/wet weight relationship P.M.C. Davies and S.M. Massey 198 1,0 (D D 0 i r --2 .~ 0.1 ~- --3 O ta =~ ua --4 0.01 I [ J 1 2 3 Ration (~ dbw. day - I ) Fig. 6. The relationship between gross energy conversion efficiency (K on a logarithmic scale or In K) and ration (per cent dry body weight per day) at five experimental temperatures ('K-lines') that of the linear relationship (0.005 < p < 0.01). The Qlo of maintenance expenditure is 2.2 over the temperature range 12-28 ~ 2. Energy Conversion Efficiency (K) Energy conversion (or growth) efficiency values were calculated for all groups of fish showing a weight gain at the end of the experimental period, in this case 56 groups spread unevenly over the five experimental temperatures (Table 3). Gross conversion efficiencies (K or Kt) were calculated according to the formulation (Ivlev, 1945; Paloheimo and Dickie, 1966); AW K = - R .At where A W is the energy equivalent of the total weight increment during the experimental period t (in days), and R is the energy value of the daily ration. Highly significant (p < 0.001) standard curves relating wet body weight to dry body weight, and dry body weight to total energy content, made it possible to derive algebraically a single composite equation relating wet weight directly to total energy content (Fig. 5). This equation was used to transform initial and final weights into initial and final energies, from which the energy value of Energy Conversion Efficiencyin Fish 199 the weight increment was obtained by difference. Following the analytical procedures developed by Paloheimo and Dickie (1966), in K was plotted against ration for each temperature, and regression lines were fitted by the method of least squares ('K-lines'-Fig. 6). Regression equations and ANOVAR results are shown in Table 3. A significant positive relationship exists between energy conversion efficiency and ration which appears to be independent of temperature. Similarly, temperature appears to have no direct effect on conversion efficiency over the ration range used in these experiments. Discussion The data summarised in Figure 6 and Table 3 indicate that, despite considerable inter-group variation in K, a significant positive relationship exists between conversion efficiency and ration at rations immediately above maintenance, and that this relationship holds good over a wide temperature range, thus lending support to the view-founded largely on theoretical expectations (Kerr, 1971a) - that an inflected, biphasic K-line is a more appropriate model of food utilisation for growth in fish than the simple negative relationship originally proposed by Paloheimo and Dickie (1966). Brett et al. (1969), Rafail (1968) and more recently, Elliott (1975), have found evidence of a similar kind for the existence of a positive phase of the K-line in young sockeye salmon, plaice, and trout respectively. Taken alongside our own data from goldfish, this suggests that the biphasic pattern is perhaps more common than has hitherto been apparent, at least in laboratory-reared fish. The complete absence of any evidence of an inflection in the negative K-lines of the various fish growth studies reviewed and re-analysed by Paloheimo and Dickie (1966) has been explained by Rafail (1968), Brett et al. (1969), and Kerr (1971a) as being a consequence of the relatively high ration levels used in the studies concerned. It is certainly the case that the ration levels used in these investigations rarely if ever approached the 'peri-maintenance' range. Since K-line inflections appear to occur only at ration levels close to maintenance, their failure to appear in growth studies which do not extend down to maintenance is hardly surprising. But other factors may also be important in determining whether or not an inflection appears, in particular the way in which the experimental fish are fed. Rations can be 'restricted' in at least two ways: by reducing the frequency of exposure to 'excess rations'; or by reducing directly the prescribed ration on a weight-specific basis. Although there is yet little in the way of hard empirical evidence to guide speculation in this area, it is theoretically possible at least that these different methods of administering food might, by inducing different patterns of foraging and feeding behaviour, produce corresponding differences in feeding costs, and thereby in gross growth efficiencies as well.Particular laboratory and experimental conditions, in other words, could, in certain cases, be eliminating the positive limb of the K-line by altering the cost-benefit parameters of feeding. Nothing is currently known about the relative energetic costs of different foraging and ingesting strategies in fish, but both Paloheimo and Dickie (1966) and Kerr 200 P.M.C. Daviesand S.M. Massey (1971 a) have postulated the importance of cost-benefit functions as determinants of the K-line phenomenon. The precise nature of the influence of temperature on conversion efficiency is at present unclear. A fall in gross K with increasing temperature, among fish maintained on severely restricted rations, is to be expected on thermodynamic grounds. As temperature increases, the energy required for maintenance increases logarithmically (Fig. 4; see also Brown, 1957, and Kelso, 1972). At the same time the SDA (Specific Dynamic Action) component of the energy budget increases (Warren and Davis, 1967), leaving a progressively smaller amount of energy available for growth. Gross conversion efficiency will therefore tend to decline as temperature increases because temperature induces higher 'living costs' which cannot, in the case of restricted feeding (but not necessarily in the case of 'excess' feeding), be met by increasing ingestion rates. This reduction in the 'scope for growth' (Warren and Davis, 1967) with increasing temperature (represented by the progressive shift to the right of the lines in Figure 1, and by the negative character of the relationships depicted in Fig. 2) appears to be ration dependent, with rising temperatures reducing growth rates more severely on higher than on lower rations (Fig. 2). The regularity of this increase in the severity of the temperature effect with ration (Fig. 3) (measured in terms of the slopes of the lines in Fig. 2) is remarkable, and suggests an equally regular, ration dependent increase in feeding and assimilation costs, most probably (though much more empirical data is needed in this area) those associated with foraging behaviour and SDA. On several grounds, therefore, the K-lines offish on restricted rations can be expected to separate with temperature, the separation tending to increase with ration, and the value of K tending to fall with rising temperature. Nothing definite can at present be said about the influence of temperature on the points of inflection themselves, though the work of both Brett et al. (1969) on Sockeye Salmon and Elliott (1975) on trout suggests that the optimum ration for conversion declines with temperature. In the light of these theoretical considerations, it is perhaps suprising that unequivocal empirical evidence confirming the expected temperature-induced separation of K-lines has proved difficult to find. In their survey of several fish growth studies, Paloheimo and Dickie (1966) found little convincing evidence of a significant temperature influence on the K-line, though evidence of a kind was apparent in the work of Baldwin (1956), Kinne (1960) and Menzel (1960). Winberg (1956) also reached the conclusion that temperature had little or no effect on conversion efficiency. In contrast, Brett et al. (1969) conclude that temperature probably exerts as much influence on conversion efficiency as ration when the full ranges of both are taken into consideration, Staples (1975) reports evidence of marked seasonal changes in gross growth efficiency correlated with changes in water temperature, and Elliott (1975) provides clear evidence of a temperature effect on at least the negative phase of the K-line. Once again the apparent conflict of evidence may be due in part to differences of experimental method, differences which could enable 'excess feeders' and 'restricted feeders' to respond differently, in terms of growth and growth efficiency, to the same average ration. Our own data are suggestive rather than Energy Conversion Efficiency in Fish 201 clear cut, derived as they are from experiments not designed primarily to measure growth rates. Statistically, K appears not to be influenced by temperature at rations close to maintenance. Nevertheless, a comparison by eye of the 12, 20 and 24 ~ K-lines (Fig. 6), which diverge as ration increases, tends to bear out the general expectation discussed above that K falls with temperature, and that the magnitude of this fall is ration-dependent. If this is in fact the true pattern of interaction between K, ration, and temperature-and the results of Brett et al. (1969) and Elliott (1975) give support to the view that it i s - t h e n the failure of the statistical analysis to detect a temperature induced separation of the K-lines in the present case, where rations are sub-optimal and close to maintenance, could be explained by a corollary of this pattern of interaction, namely that temperature-separated K-lines converge as rations are reduced. If 'optimum ration' also changes with temperature, as the work of Brett et al. and Elliott suggests, then a situation might very well arise in which the ascending limbs of ostensibly different K-lines became statistically indistinguishable. This seems to be the most likely explanation of the lack of clear separation in our own data. Tentatively, therefore, it would seem reasonable to suppose that while the K-line, viewed in its entirety, is both inflected and temperature dependent, its dependence on temperature is much less marked in the positive than in the negative phase. The separation of the three ration lines in Figure 2 corresponds closely to a similar separation observed in Sockeye salmon by Brett et al. (1969), and may reasonably be interpreted in the same way. Though we did not ourselves conduct experiments at temperatures below 12 ~ it seems probable that the lines in Figure 2 are rising to points on inflection corresponding to optimum temperatures for growth, and that these optima decrease with ration. This work was supported by a research grant from the Natural Environment Research Council (U.K.). We are grateful to Mr. David Chadwick for technical assistance, to the staff of the Animal House for constant help and advice, and to Dr. David Parkin for statistical advice. References Baldwin, N.S.: Food consumption and growth of brook trout at different temperatures. Trans. Amer. Fish. Soc. 86, 323-328 (1956) Brett, J.R., Shelbourne, J.E., Shoop, C.T. : Growth rate and body composition of fingerling sockeye salmon, Oncorhynchus nerka, in relation to temperature and ration size. J. Fish. Res. Bd. Can. 26, 2364 2394 (1969) Brown, M.E.: Experimental studies on growth. In: The physiology of fishes, Vol. 1 (ed. M.E. Brown), pp. 361-400. New York: Academic Press i957 Davies, P.M.C. : The energy relations of Carassius auratus L. I. Food input and energy extraction efficiency at two experimental temperatures. Comp. Biochem. Physiol. 12, 67-79 (1964) Elliot, J.M.: The growth of brown trout (Salmo trutta L.) fed on reduced rations. J. anita. Ecol. 44, 823-842 (1975) Ivlev, V.S. : The biological productivity of waters. Usp. sovrem. Biol. 19, 98-120 (1945) (cf. Trans. Fish. Res. Bd. Can. No. 394) Kelso, J.R.M. : Conversion, maintenance and assimilation for walleye, Stizostedion vitreum vitreum, as affected by size, diet and temperature. J. Fish. Res. Bd. Can. 29, 1181-1192 (1972) Kerr, S.R.: Analysis of laboratory experiments on growth efficiency of fishes. J. Fish. Res. Bd. Can. 28, 801-808 (1971a) 202 P.M.C. Davies and S.M. Massey Kerr, S.R.: Prediction of fish growth efficiency in nature. J. Fish. Res. Bd. Can. 28, 809-814 (1971 b) Kinne, O.: Growth, food intake and food conversion in a euryplastic fish exposed to different temperatures and salinities. Physiol. Zool. 33, 288 317 (1960) LeBrasseur, R.J.: Growth of juvenile chum salmon (Oneorhynchus keta) under different feeding regimes. J. Fish. Res. Bd. Can. 26, 1631-1645 (1969) Menzel, D.W.: Utilisation of food by a Bermuda reef fish, Epinephelus guttatus. J. Cons. perm. int. Explor. Mer. 25, 216 222 (1960) Nelder, J.A.: General linear interactive modelling. Numerical Algorithms Group, Oxford (1975) Paloheimo, J.E., Dickie, L.M.: Food and growth of fishes. III. Relations among food, body size and growth efficiency. J. Fish. Res. Bd. Can. 23, 1209-1248 (1966) Pandian, T.J. : Intake, digestion, absorption and conversion of food in the fishes Megalops cyprinoides and Ophiocephalus striatus. Marine Biol. 1, 16 32 (1967) Rafail, S.Z. : A statistical analysis of ration and growth relationship of plaice (Pleuronectes platessa). J. Fish. Res. Bd. Can. 25, 717-732 (1968) Rozin, P., Mayer, J.: Some factors influencing short-term food intake of the goldfish. Amer. J. Physiol. 206, 1430 1436 (1964) Staptes, D.J.: Production biology of the upland bully Philypnodon breviceps StokelI in a small New Zealand lake. III. Production, food consumption and efficiency of food utilisation. J. Fish. Biol. 7, 47-69 (1975) Warren, C.E., Davis, G.E.: Laboratory studies on the feeding, bioenergetics and growth of fish. In: The biological basis of fieshwater fish production (ed. S.D. Gerking), pp. 175 214. Oxford: Blackwell 1967 Winberg, G.G.: Rate of metabolism and food requirements of fishes. Fish. Res. Bd. Can. Transl. Ser. No. 194 (1956)