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Body composition changes and energy retention in milk-fed lambs undergoing energy restriction
Small Ruminant Research 31 (1999) 127±133
Body composition changes and energy retention in milk-fed lambs undergoing energy restriction F.J. GiraÂldez*, P. Frutos, P. LavõÂn, A.R. MantecoÂn EstacioÂn AgrõÂcola Experimental de LeoÂn, CSIC. Apdo 788, 24080 LeoÂn, Spain Accepted 10 April 1998
Abstract Eighteen milk-fed Churra lambs were used to study the effect of three levels of energy intake below maintenance requirements (293, 377 and 460 kJ GE/kg body weight (BW)0.75) at different BW (LW: 5 kg; HW: 8 kg) on energy retention (ER) and mobilisation of body components. Losses of fat and energy were related to energy intake (linear orthogonal contrast; p<0.05). Energy and fat mobilisation were greater for HW (linear contrast, p<0.05). There was also a signi®cant effect of energy intake on protein retention, with increased protein deposition at higher energy intakes (linear contrast, p<0.05). Crude protein retention for the LW group ranged from negative (for the lowest level of energy intake) to positive mean values, while the mean values for the HW group were always greater and positive. No evidence of maintenance energy requirements changing quantitatively during the milk-fed phase was found in this study. Daily NE requirements for maintenance were not signi®cantly different (p>0.05) for LW and HW groups either, the overall value being 494 kJ/kg BW0.75 (SE 74.4). # 1999 Elsevier Science B.V. All rights reserved. Keywords: Milk-fed lambs; Undernutrition; Body composition; Energy maintenance requirements
1. Introduction In calculating feed requirements for lambs given liquid diets, the Agriculture Research Council recommends a constant value for energy maintenance requirements until weaning (ARC, 1980). Nevertheless, it has been reported that the fasting metabolism of lambs could change quantitatively throughout the milk-fed period (Graham et al., 1974). Additionally, maintenance requirement estimates from different energy evaluation schemes do not agree well (NRC, *Corresponding author. Tel.: 0034 987 31 71 56; fax: 0034 987 31 71 61
1975; ARC, 1980; Wallach et al., 1984). These differences are of little signi®cance when lambs are slaughtered at high body weight (BW) and the milk feeding period comprising only a small part of the animal's life. However, under some traditional farming systems, lambs are slaughtered unweaned at approximately 10 kg BW (e.g. Churra lambs in Spain; LavõÂn, 1996). Therefore, the milk feeding period is an important phase of the productive cycle and detailed knowledge of metabolism and nutritive requirements in the preruminant stage is basic to reliable prediction of animal performance. Therefore, the present experiment was designed to: (a) study the body composition changes and energy retention of
0921-4488/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S0921-4488(98)00129-1
128
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
milk-fed lambs of different BW during short periods of energy restriction and (b) estimate the energy maintenance requirement of milk-fed lambs at different BW. 2. Material and methods 2.1. Animals and experimental design Eighteen male Churra lambs were randomly allocated to six groups of three animals according to a 23 factorial design, with factors consisting of two BWs at the beginning of the feed restriction period (LW: 5 kg; HW: 8 kg) and three levels of GE intake below theoretical maintenance allowances (ARC, 1980), (LI: 293 kJ GE/kg BW0.75; MI: 377 kJ GE/ kg BW0.75; HI: 460 kJ GE/kg BW0.75). 2.2. Management and feeding The lambs were removed from the ewes within 3 h of birth, identi®ed and housed individually in metabolic cages. The air temperature in the building was kept between 15 and 208C over the preliminary (from birth until lambs achieved the experimental BW) and experimental periods. Animals were weighed (ca. 5 g) for the ®rst time after 6 h of fasting and then once daily, before morning feeding, until the day of slaughter. They were individually placed on the experiment when their BWs were between 4.9 and 5.1 kg for LW and between 7.9 and 8.1 for HW. During the ®rst 2 days animals received colostrum at the rate of approximately 40% of BW. After those 2 days and until the end of the experiment, they were fed in two equal meals per day (9 and 17 h) with reconstituted cow's milk (18.6% of total solids, 23.14 mJ/kg of GE, 290 g/kg of CP, 245 g/kg of fat and 69 g/kg of ash). Milk was prepared twice daily immediately before its distribution and supplemented with NaCl (0.5 g/kg), Ca2PO4 (1 g/kg) and vitamins A (500 mg/ g), D3 (7.5 mg/g) and E (600 mg/kg). The level of milk offered was ®xed at 1255 kJ GE/kg BW0.75 during the preliminary period and at one of the three planned levels during the 10 days of the experimental period. Daily allowance was adjusted three times a week, according to BW. Feed refusals were weighed daily to determine the actual intake.
2.3. Slaughter procedure Lambs were weighed on the morning of the 11th day of the experimental period and anaesthetised with sodium pentobarbitone. Then, they were shorn and slaughtered by exsanguination from the jugular vein. The whole body of each lamb was dissected into carcass and `non-carcass' components which were minced, mixed and homogenised in a commercial blender. Samples from each component were taken for chemical analysis and determination of their energy content. 2.4. Analytical methods Dry matter content of milk replacer was determined by drying samples to constant weight in an oven at 100±1058C. Crude Protein content (N6.38) was determined by macro-Kjeldahl technique and lipid content according to the method of Gerber (Bateman, 1970). Ash was determined by burning in a muf¯e furnace at 5508C and the GE by adiabatic bomb calorimetry. Dry matter of body components was determined by freeze-drying samples to constant weight. CP (N6.25), ash and GE were determined by the same techniques as for milk replacer. Lipid content was estimated by difference. Initial body composition of the experimental animals was calculated using the following equations obtained by MantecoÂn (1986) in milk-fed Churra lambs ranging from 3.5 to 9 kg of BW (n108) Water (g) Nitrogen (g) Fat (g) Ash (g) Energy (kJ)
259.6 (SE 50.76)0.61 (SE 0.008)BW (g) 12.6 (SE 3.92)0.02 (SE 0.001)BW (g) ÿ568 (SE 39.96)0.17 (SE 0.006)BW (g) 41.5 (SE 11.20)0.03 (SE 0.002)BW (g) ÿ20375.9 (SE 1455.7)9.95 (SE 0.226)BW (g)
r0.9911 r0.9701 r0.9331 r0.8534 r0.9736
In order to estimate the NE requirements for maintenance (NEm) and the ef®ciency of utilisation of metabolisable energy (Km), a regression of energy
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
retention (ER) vs. ME intake (ME), with both ER and ME scaled up to BW0.75, was determined for each BW group. ME intake was estimated from GE milk replacer assuming a constant value of 0.92 for the metabolisability (MantecoÂn, 1986). 2.5. Statistical analysis Analysis of variance was used to determine the effect of BW and energy intake on body composition and energy content. Orthogonal contrasts were used to test for linear and quadratic effects of energy intake level, and also for interactions between these linear and quadratic energy level effects and BW treatment. A LSD test was used to compare mean values within factors, except for estimated values of NEm and Km, where a t-test was used. Analyses were performed according to Steel and Torrie (1980) procedures. 3. Results Fig. 1 shows mean values of chemical composition and energy content of the empty body weight (EBW) at the beginning of the experimental period, for LW (493826.4 g) and HW (801371.4 g) groups.
129
Mean values of the changes (g/day) in BW, EBW, water, CP, fat and ash during feed restriction for the two BW groups and for the three levels of energy intake are shown in Table 1. There were no signi®cant BW and energy intake interactions and, thus, only results for the two main effects are presented. The differences (p>0.05) between LW and HW groups in the changes in BW, EBW, water and ash were not signi®cant. However, the HW group mobilised more fat and accreted more protein than did the LW group (p<0.05). These differences were also observed when daily retentions were expressed relative to BW0.75 (Table 2). Live weight, EBW, water and crude protein changes (g/day) were signi®cantly affected by level of energy intake (linear contrast, p<0.05). Fat mobilisation was also affected by energy intake (linear contrast, p<0.05) when daily variation was related to W0.75. However, whereas at the lowest level of energy intake lambs lost BW, EBW, fat and water, at the highest level intake only BW and fat showed negative changes. Crude protein retention (g/kg W0.75/day) was also related to energy intake (linear contrast, p<0.05). Crude protein retention for the LW group ranged from negative mean values for the lowest level of energy intake, to positive ones, while the mean values of protein retention for the HW group were always higher and posi-
Fig. 1. Chemical composition (g/kg) and energy content (kJ/100 g) of the empty body weight at the beginning of the experimental period, for the two live body weight groups (LW, &; HW, &).
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
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Table 1 Mean values of the changes (g/day) of BW, empty BW (EBW), and water, CP, fat and ash contents in the EBW BW groups LW BW EBW Water CP Fat Ash
ÿ42.48 ÿ14.68 2.35 ÿ0.22a ÿ15.85a ÿ0.96
Level of GE intake HW
LI a
ÿ35.03 ÿ9.49 13.41 11.38b ÿ34.57b 1.00
RSD
MI a
ÿ68.25 ÿ39.73a ÿ12.09a 1.26a ÿ28.57 ÿ0.33
HI b
ÿ40.08 ÿ13.30b 6.98b 5.91b ÿ25.50 ÿ0.59
c
ÿ7.93 16.78c 28.84c 9.57c ÿ21.56 ÿ0.07
21.903 18.189 13.526 2.652 4.950 1.606
Analysis of variance W
GE
GElin
GEquad
ns ns ns ** **
** ** ** ** ns
** *** *** *** ns
ns ns ns ns ns ns
ns: not significant (p>0.10); : p<0.10; *: p<0.05; **: p<0.01; ***: p<0.001. within each source of variation values in the same line followed by different letters are significantly different by LSD test (p<0.05). GElinlinear effect of GE intake level (orthogonal contrast). GEquadquadratic effect of GE intake level (orthogonal contrast). No interaction was significant (p>0.10). a,b,c
Table 2 Mean values of the changes (g/kg W0.75/day) of BW, empty body weight (EBW), and water, CP, fat and ash contents in the EBW BW groups LW W EBW Water CP Fat Ash
ÿ13.41 ÿ4.71 0.64 ÿ0.09a ÿ4.96a ÿ0.30
Level of GE intake HW ÿ7.53 ÿ2.06 2.84 2.43b ÿ7.38b 0.06
LI
RSD
MI a
ÿ18.24 ÿ10.60a ÿ3.39a ÿ0.02a ÿ7.10a ÿ0.13
HI b
ÿ10.85 ÿ3.63b 1.54b 1.27b ÿ6.27ab ÿ0.18
c
ÿ2.32 4.09c 7.07c 2.21b ÿ5.14b ÿ0.04
5.367 4.268 3.103 0.749 1.111 0.446
Analysis of variance W
GE
GElin
GEquad
ns ns ** **
** ** ** ** * ns
*** *** *** ** * ns
ns ns ns ns ns ns
ns: not significant (p>0.10); : p<0.10; *: p<0.05; **: p<0.01; ***: p<0.001. within each source of variation values in the same line followed by different letters are significantly different by LSD test (p<0.05). GElinlinear effect of GE intake level (orthogonal contrast). GEquadquadratic effect of GE intake level (orthogonal contrast). No interaction was significant (p>0.10). a,b,c
tive. In no case was a signi®cant quadratic contrast found. Mean values of ER are shown in Table 3. ER values were negative for all the treatments and there were signi®cant differences (p<0.05) between LW and HW groups and among levels of energy intake, but the interaction was not signi®cant (p>0.10). Energy retention was lower for the LH than for the HW group although there were not signi®cant differences (p>0.10) when ER was expressed in relation to BW0.75. Body energy losses were inversely related to energy intake, decreasing more than 30% from the lowest to the highest level of energy intake (linear contrast, p<0.05; quadratic contrast, p>0.05). Estimated values for NEm and km are presented in Table 4. There were no signi®cant differences
(p>0.05) between BW groups for NEm or for km estimations. Overall mean values were 494 kJ/kg W0.75/day (SE 74.4) for NEm and 0.79 (SE 0.211) for km. 4. Discussion Lambs remained healthy during the preliminary and experimental periods, although some of them showed losses of more than 10% of initial BW. There were no refusals of the offered milk throughout the experimental period and hence the planned levels of energy intake were achieved. As was expected, lambs from both LW and HW groups lost fat at all three levels of energy intake, the
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Table 3 Mean values of energy retention BW groups LW kJ/day kJ/kg W0.75/day kJ/100 kJ of GE in the initial EBW
Level of GE intake HW
a
ÿ659.40 ÿ206.91 ÿ22.93a
LI b
ÿ1103.78 ÿ235.89 ÿ18.53b
RSD
MI a
ÿ1105.75 ÿ282.41a ÿ26.08a
HI ab
ÿ874.98 ÿ220.46ab ÿ20.85ab
b
ÿ663.98 ÿ161.33b ÿ15.26b
272.845 61.800 5.177
Analysis of variance W
GE
GRlin
GEquad
*** ns
** ** ***
** ** **
ns ns ns
ns: not significant (p>0.10); : p<0.10; *: p<0.05; **: p<0.01; ***: p<0.001. within each source of variation values in the same line followed by different letters are significantly different by LSD test (p<0.05). GElinlinear effect of GE intake level (orthogonal contrast). GEquadquadratic effect of GE intake level (orthogonal contrast). No interaction was significant (p>0.10). a,b,c
Table 4 Maintenance energy requirements (NEm; kJ/Kg W0.75) and efficiency of utilisation of metabolisable energy for maintenance (km) BW groups
NEm
km
r
Level of significance
LW HW Overalla
503 (SE 72.5) 484 (SE 134.2) 494 (SE 74.4)
0.85 (SE 0.206) 0.72 (SE 0.301) 0.79 (SE 0.211)
0.84 0.58 0.68
p<0.05 p<0.10 p<0.05
a
Overall value estimated considering all the experimental animals.
rate being inversely related to energy intake. These observations are consistent with the notion that in underfed animals, fatty acid catabolism increases progressively as the supply of oxidisable alimentary nutrients declines (Pethick et al., 1984). An interesting aspect concerning fat mobilisation was the difference observed between experimental BW groups when fat losses were expressed in relation to metabolic BW. There is evidence from ewes in different physiological states that the capacity to mobilise body fat reserves is positively related to the level of body fat (Gibb and Treacher, 1980; Buratovich, 1995). Differences in fat mobilisation between lambs of different BW detected in this experiment could be related to the development of the adipose tissue. Lambs from the HW group had almost double body fat than the lambs from the LW group (102 vs. 55 g of fat/kg EBW). When fat losses were expressed in relation to the initial body fat reserves, the LW group showed a larger daily rate (p<0.05) than the HW group (6.3 vs. 4.5%) which suggests that the higher body fat losses in the HW group were simply due to a higher amount of body fat rather than to differences in the rate of the metabolic processes involved in lipolysis and fatty acid catabolism.
Studies of different animal species, including lambs, have demonstrated that fat mobilisation can provide energy to sustain positive N balance in animals with inadequate energy-yielding nutrition but with an adequate protein supply (Fowler et al., 1983; Hovell et al., 1983; érskov et al., 1983; Vipond et al., 1989; Chawdury et al., 1990). Low intake after weaning of lambs can also cause fat losses while protein gain continues (Graham, 1982). The present results support these ®ndings, although the HW group showed a larger protein accretion than LW group. Since N supply (g/kg BW0.75) within the same level of energy intake was similar for LW and HW lambs but fat losses were higher for HW lambs, fat mobilisation seems to be the main factor explaining the differences observed between BW groups in protein retention. Although more energy was used for protein synthesis by the HW group, neither total energy losses (relative to metabolic BW) nor fasting metabolism and ef®ciency with which dietary ME replaces body fat and protein as a source of energy for maintenance differed between BW groups. In contrast and as a consequence of the different levels of fat mobilisation, N balance occurred at lower energy input for the HW (17942.7 kJ ME/kg
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Table 5 Estimates of the net energy requirements for maintenance (kJ NEm/kg metabolic weight) of milk-fed lambs Source
Method of estimation
NEm requirements
Walker and Faichney, 1964 Kielanowski, 1965 Chiou and Jordan, 1973 Graham et al., 1974 ARC, 1980 Degen and Young, 1982 MantecoÂn, 1986 Present studya
Calorimetric Serial slaughter Serial slaughter Calorimetric Calorimetric Calorimetric Serial slaughter Serial slaughter
438 kJ/kg W0.73 372 kJ/kg W0.73 444 kJ/kg W0.75 539 kJ/kg W0.75 350 kJ/(kg W/1.05)0.75 536 kJ/kg W0.75 506 kJ/kg W0.75 494 kJ/kg W0.75
a
Overall value estimated considering all the experimental animals.
BW0.75) than for the LW group (34913.3 kJ ME/kg BW0.75) which implies a better ability to mobilise extra energy from body fat reserves for the HW group. Fattet et al. (1984) suggest that protein accretion in animals with negative energy balance may depend on the overall energy status of the animals, which is in agreement with the present results. As shown in Table 5, values of NEm obtained here are comparable to other published data, although present estimates seem consistently higher than NEm values proposed by the Agricultural Research Council (ARC, 1980). The ARC estimates of maintenance energy requirements are based on calorimetric studies and it is known that fasting metabolism declines during starvation periods (Alexander, 1962; ARC, 1980). Additionally and in contrast to mature sheep, heat production of milk-fed lambs is not constant after fasting for 72 h, although at this time metabolism can decrease to more than 50% of initial heat production (Graham et al., 1974). Therefore, these features could explain the higher values found in the present study compared with ARC (1980), even though it might also be expected that fasting metabolism decreases in underfed animals. However, our estimates of NEm are comparable to NEm values obtained by MantecoÂn (1986) with Churra milk-fed lambs fed above maintenance. In summarising the above results, it may be concluded ®rstly that fatty acid catabolism from body fat reserves can supply extra energy to sustain positive N balances in lambs fed below maintenance energy requirements provided that protein is supplied above the level needed to replace the endogenous losses. It is concluded that the rate of fat mobilisation per kg of metabolic BW is directly related to total body fat
reserves. However, under severe energy restrictions the level of adipose tissue may not be suf®cient to avoid the catabolism of body protein reserves. In contrast to earlier studies, there is no evidence in this study that maintenance energy requirements changed quantitatively during the milk-fed phase, although the limited range of BW tested must be considered before getting de®nitive conclusions.
Acknowledgements The authors wish to thank I.A. Wright for revision of the manuscript and A. GoÂmez for technical assistance. This research was supported by the project GAN 90-0906.
References ARC, 1980. The Nutrient Requirements of Ruminant Livestock. CAB, London. Alexander, G., 1962. Energy metabolism in the starved new-born lamb. Aust. J. Agric. Res. 13, 144±164. Bateman, J.V., 1970. NutricioÂn Animal. Manual de meÂtodos analõÂticos (Animal Nutrition. Analytical methods). Herrero Hermanos Sucesores, S.A. MeÂxico. Buratovich, O., 1995. Respuesta a la suplementacioÂn durante la gestacioÂn del ganado ovino en pastoreo (Response to supplementation during pregnancy by grazing sheep). M.Sc. Thesis. CIHEAM, Zaragoza. Chawdury, S.A., érskov, E.R., MacLeod, N.A., 1990. Protein utilisation during energy undernutrition in steers. Proc. Nutr. Soc. 49, 208A. Chiou, P.W.S., Jordan, R.M., 1973. Ewe milk replacer diets for young lambs. IV. Protein and energy requirements of young lambs. J. Anim. Sci. 37, 581±587.
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133 Degen, A.A., Young, B.A., 1982. Intake energy: Energy retention and heat production in lambs from birth to 24 weeks of age. J. Anim. Sci. 54, 353±362. Fattet, I., Hovell, F.D. Deb, érskov, E.R., Kyle, D.J., Pennie, K., Smart, R.I., 1984. Undernutrition in sheep. The effect of supplementation with protein on protein accretion. Br. J. Nutr. 52, 561±574. Fowler, V.R., McWilliam, R., Pennie, K., Ross, L., 1983. Compositional changes in growing pigs when fed at maintenance. Anim. Prod. 36, 517. Gibb, M.J., Treacher, T.T., 1980. The effect of ewe body condition at lambing on the performance of ewes and their lambs at pasture. J. Agric. Sci., Camb. 95, 631±640. Graham, N.McC., Searle, T.W., Griffiths, D.A., 1974. Basal metabolic rate in lambs and young sheep. Aust. J. Agric. Res. 25, 957±971. Graham, N.McC., 1982. Maintenance and growth. In: Coop, I.E. (Ed.), Sheep and Goat Production, Elsevier, Amsterdam, pp. 81±101. Hovell, F.D. Deb, érskov, E.R., MacLeod, N.A., McDonald, I., 1983. The effect of changes in the amount of energy infused as volatile fatty acids on the nitrogen retention and creatinine excretion of lambs wholly nourished by intragastric infusion. Br. J. Nutr. 50, 331±343. Kielanowski, J., 1965. Estimates of the energy cost of protein deposition in growing animals. In: Blaxter, K.L. (Ed.), Energy Metabolism, EAAP Publication No. II, Academic Press, London, pp. 13±20. LavõÂn, P., 1996. Los sistemas de produccioÂn animal en la provincia de LeoÂn: Factores condicionantes de su distribucioÂn y
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estructura (Animal production systems in LeoÂn: factors affecting distribution and structure). Ph.D. thesis. University of LeoÂn. MantecoÂn, A.R., 1986. Lactancia Artificial de Corderos de Raza Churra. Necesidades Nutritivas (Milk feeding of Churra lambs. Nutritive requirements). Ph.D. thesis. University of LeoÂn. NRC, 1975. Nutrient Requirements of Sheep. National Academic Press, Washington, DC. érskov, E.R., MacLeod, N.A., Fahmy, S.T.M., Istasse, L., Hovell, F.D. Deb, 1983. Investigation of nitrogen balance in dairy cows and steers nourished by intragastric infusion. Effects of submaintenance energy input with or without protein. Br. J. Nutr. 50, 99±107. Pethick, D.W., Bell, A.W., Annison, E.F., 1984. Fats as energy sources in animal tissues. In: Wiseman, J. (Ed.), Fats in Animal Nutrition, Butterworths, London, pp. 225±248. Steel, R.G.D., Torrie, J.H. 1980. Principles and Procedures of Statistics. A Biometrical Approach. McGraw-Hill, New York. Vipond, J.E., King, M.E., érskov, E.R., Wetherill, G.Z., 1989. Effect of fish-meal supplementation on performance of overfat lambs fed on barley straw to reduce carcass fatness. Anim. Prod. 48, 131±138. Walker, D.M., Faichney, G.J., 1964. Nitrogen balance studies with the milk-fed lamb. I. Endogenous urinary nitrogen, metabolic faecal nitrogen and basal heat production. Br. J. Nutr. 18, 187± 200. Wallach, D., Elsen, J.M., Charpentau, J.L., 1984. Maintenance energy requirements of grazing sheep: A detailed comparisons between models. Agric. Systems 15, 1±22.
Body composition changes and energy retention in milk-fed lambs undergoing energy restriction F.J. GiraÂldez*, P. Frutos, P. LavõÂn, A.R. MantecoÂn EstacioÂn AgrõÂcola Experimental de LeoÂn, CSIC. Apdo 788, 24080 LeoÂn, Spain Accepted 10 April 1998
Abstract Eighteen milk-fed Churra lambs were used to study the effect of three levels of energy intake below maintenance requirements (293, 377 and 460 kJ GE/kg body weight (BW)0.75) at different BW (LW: 5 kg; HW: 8 kg) on energy retention (ER) and mobilisation of body components. Losses of fat and energy were related to energy intake (linear orthogonal contrast; p<0.05). Energy and fat mobilisation were greater for HW (linear contrast, p<0.05). There was also a signi®cant effect of energy intake on protein retention, with increased protein deposition at higher energy intakes (linear contrast, p<0.05). Crude protein retention for the LW group ranged from negative (for the lowest level of energy intake) to positive mean values, while the mean values for the HW group were always greater and positive. No evidence of maintenance energy requirements changing quantitatively during the milk-fed phase was found in this study. Daily NE requirements for maintenance were not signi®cantly different (p>0.05) for LW and HW groups either, the overall value being 494 kJ/kg BW0.75 (SE 74.4). # 1999 Elsevier Science B.V. All rights reserved. Keywords: Milk-fed lambs; Undernutrition; Body composition; Energy maintenance requirements
1. Introduction In calculating feed requirements for lambs given liquid diets, the Agriculture Research Council recommends a constant value for energy maintenance requirements until weaning (ARC, 1980). Nevertheless, it has been reported that the fasting metabolism of lambs could change quantitatively throughout the milk-fed period (Graham et al., 1974). Additionally, maintenance requirement estimates from different energy evaluation schemes do not agree well (NRC, *Corresponding author. Tel.: 0034 987 31 71 56; fax: 0034 987 31 71 61
1975; ARC, 1980; Wallach et al., 1984). These differences are of little signi®cance when lambs are slaughtered at high body weight (BW) and the milk feeding period comprising only a small part of the animal's life. However, under some traditional farming systems, lambs are slaughtered unweaned at approximately 10 kg BW (e.g. Churra lambs in Spain; LavõÂn, 1996). Therefore, the milk feeding period is an important phase of the productive cycle and detailed knowledge of metabolism and nutritive requirements in the preruminant stage is basic to reliable prediction of animal performance. Therefore, the present experiment was designed to: (a) study the body composition changes and energy retention of
0921-4488/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S0921-4488(98)00129-1
128
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
milk-fed lambs of different BW during short periods of energy restriction and (b) estimate the energy maintenance requirement of milk-fed lambs at different BW. 2. Material and methods 2.1. Animals and experimental design Eighteen male Churra lambs were randomly allocated to six groups of three animals according to a 23 factorial design, with factors consisting of two BWs at the beginning of the feed restriction period (LW: 5 kg; HW: 8 kg) and three levels of GE intake below theoretical maintenance allowances (ARC, 1980), (LI: 293 kJ GE/kg BW0.75; MI: 377 kJ GE/ kg BW0.75; HI: 460 kJ GE/kg BW0.75). 2.2. Management and feeding The lambs were removed from the ewes within 3 h of birth, identi®ed and housed individually in metabolic cages. The air temperature in the building was kept between 15 and 208C over the preliminary (from birth until lambs achieved the experimental BW) and experimental periods. Animals were weighed (ca. 5 g) for the ®rst time after 6 h of fasting and then once daily, before morning feeding, until the day of slaughter. They were individually placed on the experiment when their BWs were between 4.9 and 5.1 kg for LW and between 7.9 and 8.1 for HW. During the ®rst 2 days animals received colostrum at the rate of approximately 40% of BW. After those 2 days and until the end of the experiment, they were fed in two equal meals per day (9 and 17 h) with reconstituted cow's milk (18.6% of total solids, 23.14 mJ/kg of GE, 290 g/kg of CP, 245 g/kg of fat and 69 g/kg of ash). Milk was prepared twice daily immediately before its distribution and supplemented with NaCl (0.5 g/kg), Ca2PO4 (1 g/kg) and vitamins A (500 mg/ g), D3 (7.5 mg/g) and E (600 mg/kg). The level of milk offered was ®xed at 1255 kJ GE/kg BW0.75 during the preliminary period and at one of the three planned levels during the 10 days of the experimental period. Daily allowance was adjusted three times a week, according to BW. Feed refusals were weighed daily to determine the actual intake.
2.3. Slaughter procedure Lambs were weighed on the morning of the 11th day of the experimental period and anaesthetised with sodium pentobarbitone. Then, they were shorn and slaughtered by exsanguination from the jugular vein. The whole body of each lamb was dissected into carcass and `non-carcass' components which were minced, mixed and homogenised in a commercial blender. Samples from each component were taken for chemical analysis and determination of their energy content. 2.4. Analytical methods Dry matter content of milk replacer was determined by drying samples to constant weight in an oven at 100±1058C. Crude Protein content (N6.38) was determined by macro-Kjeldahl technique and lipid content according to the method of Gerber (Bateman, 1970). Ash was determined by burning in a muf¯e furnace at 5508C and the GE by adiabatic bomb calorimetry. Dry matter of body components was determined by freeze-drying samples to constant weight. CP (N6.25), ash and GE were determined by the same techniques as for milk replacer. Lipid content was estimated by difference. Initial body composition of the experimental animals was calculated using the following equations obtained by MantecoÂn (1986) in milk-fed Churra lambs ranging from 3.5 to 9 kg of BW (n108) Water (g) Nitrogen (g) Fat (g) Ash (g) Energy (kJ)
259.6 (SE 50.76)0.61 (SE 0.008)BW (g) 12.6 (SE 3.92)0.02 (SE 0.001)BW (g) ÿ568 (SE 39.96)0.17 (SE 0.006)BW (g) 41.5 (SE 11.20)0.03 (SE 0.002)BW (g) ÿ20375.9 (SE 1455.7)9.95 (SE 0.226)BW (g)
r0.9911 r0.9701 r0.9331 r0.8534 r0.9736
In order to estimate the NE requirements for maintenance (NEm) and the ef®ciency of utilisation of metabolisable energy (Km), a regression of energy
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
retention (ER) vs. ME intake (ME), with both ER and ME scaled up to BW0.75, was determined for each BW group. ME intake was estimated from GE milk replacer assuming a constant value of 0.92 for the metabolisability (MantecoÂn, 1986). 2.5. Statistical analysis Analysis of variance was used to determine the effect of BW and energy intake on body composition and energy content. Orthogonal contrasts were used to test for linear and quadratic effects of energy intake level, and also for interactions between these linear and quadratic energy level effects and BW treatment. A LSD test was used to compare mean values within factors, except for estimated values of NEm and Km, where a t-test was used. Analyses were performed according to Steel and Torrie (1980) procedures. 3. Results Fig. 1 shows mean values of chemical composition and energy content of the empty body weight (EBW) at the beginning of the experimental period, for LW (493826.4 g) and HW (801371.4 g) groups.
129
Mean values of the changes (g/day) in BW, EBW, water, CP, fat and ash during feed restriction for the two BW groups and for the three levels of energy intake are shown in Table 1. There were no signi®cant BW and energy intake interactions and, thus, only results for the two main effects are presented. The differences (p>0.05) between LW and HW groups in the changes in BW, EBW, water and ash were not signi®cant. However, the HW group mobilised more fat and accreted more protein than did the LW group (p<0.05). These differences were also observed when daily retentions were expressed relative to BW0.75 (Table 2). Live weight, EBW, water and crude protein changes (g/day) were signi®cantly affected by level of energy intake (linear contrast, p<0.05). Fat mobilisation was also affected by energy intake (linear contrast, p<0.05) when daily variation was related to W0.75. However, whereas at the lowest level of energy intake lambs lost BW, EBW, fat and water, at the highest level intake only BW and fat showed negative changes. Crude protein retention (g/kg W0.75/day) was also related to energy intake (linear contrast, p<0.05). Crude protein retention for the LW group ranged from negative mean values for the lowest level of energy intake, to positive ones, while the mean values of protein retention for the HW group were always higher and posi-
Fig. 1. Chemical composition (g/kg) and energy content (kJ/100 g) of the empty body weight at the beginning of the experimental period, for the two live body weight groups (LW, &; HW, &).
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
130
Table 1 Mean values of the changes (g/day) of BW, empty BW (EBW), and water, CP, fat and ash contents in the EBW BW groups LW BW EBW Water CP Fat Ash
ÿ42.48 ÿ14.68 2.35 ÿ0.22a ÿ15.85a ÿ0.96
Level of GE intake HW
LI a
ÿ35.03 ÿ9.49 13.41 11.38b ÿ34.57b 1.00
RSD
MI a
ÿ68.25 ÿ39.73a ÿ12.09a 1.26a ÿ28.57 ÿ0.33
HI b
ÿ40.08 ÿ13.30b 6.98b 5.91b ÿ25.50 ÿ0.59
c
ÿ7.93 16.78c 28.84c 9.57c ÿ21.56 ÿ0.07
21.903 18.189 13.526 2.652 4.950 1.606
Analysis of variance W
GE
GElin
GEquad
ns ns ns ** **
** ** ** ** ns
** *** *** *** ns
ns ns ns ns ns ns
ns: not significant (p>0.10); : p<0.10; *: p<0.05; **: p<0.01; ***: p<0.001. within each source of variation values in the same line followed by different letters are significantly different by LSD test (p<0.05). GElinlinear effect of GE intake level (orthogonal contrast). GEquadquadratic effect of GE intake level (orthogonal contrast). No interaction was significant (p>0.10). a,b,c
Table 2 Mean values of the changes (g/kg W0.75/day) of BW, empty body weight (EBW), and water, CP, fat and ash contents in the EBW BW groups LW W EBW Water CP Fat Ash
ÿ13.41 ÿ4.71 0.64 ÿ0.09a ÿ4.96a ÿ0.30
Level of GE intake HW ÿ7.53 ÿ2.06 2.84 2.43b ÿ7.38b 0.06
LI
RSD
MI a
ÿ18.24 ÿ10.60a ÿ3.39a ÿ0.02a ÿ7.10a ÿ0.13
HI b
ÿ10.85 ÿ3.63b 1.54b 1.27b ÿ6.27ab ÿ0.18
c
ÿ2.32 4.09c 7.07c 2.21b ÿ5.14b ÿ0.04
5.367 4.268 3.103 0.749 1.111 0.446
Analysis of variance W
GE
GElin
GEquad
ns ns ** **
** ** ** ** * ns
*** *** *** ** * ns
ns ns ns ns ns ns
ns: not significant (p>0.10); : p<0.10; *: p<0.05; **: p<0.01; ***: p<0.001. within each source of variation values in the same line followed by different letters are significantly different by LSD test (p<0.05). GElinlinear effect of GE intake level (orthogonal contrast). GEquadquadratic effect of GE intake level (orthogonal contrast). No interaction was significant (p>0.10). a,b,c
tive. In no case was a signi®cant quadratic contrast found. Mean values of ER are shown in Table 3. ER values were negative for all the treatments and there were signi®cant differences (p<0.05) between LW and HW groups and among levels of energy intake, but the interaction was not signi®cant (p>0.10). Energy retention was lower for the LH than for the HW group although there were not signi®cant differences (p>0.10) when ER was expressed in relation to BW0.75. Body energy losses were inversely related to energy intake, decreasing more than 30% from the lowest to the highest level of energy intake (linear contrast, p<0.05; quadratic contrast, p>0.05). Estimated values for NEm and km are presented in Table 4. There were no signi®cant differences
(p>0.05) between BW groups for NEm or for km estimations. Overall mean values were 494 kJ/kg W0.75/day (SE 74.4) for NEm and 0.79 (SE 0.211) for km. 4. Discussion Lambs remained healthy during the preliminary and experimental periods, although some of them showed losses of more than 10% of initial BW. There were no refusals of the offered milk throughout the experimental period and hence the planned levels of energy intake were achieved. As was expected, lambs from both LW and HW groups lost fat at all three levels of energy intake, the
F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
131
Table 3 Mean values of energy retention BW groups LW kJ/day kJ/kg W0.75/day kJ/100 kJ of GE in the initial EBW
Level of GE intake HW
a
ÿ659.40 ÿ206.91 ÿ22.93a
LI b
ÿ1103.78 ÿ235.89 ÿ18.53b
RSD
MI a
ÿ1105.75 ÿ282.41a ÿ26.08a
HI ab
ÿ874.98 ÿ220.46ab ÿ20.85ab
b
ÿ663.98 ÿ161.33b ÿ15.26b
272.845 61.800 5.177
Analysis of variance W
GE
GRlin
GEquad
*** ns
** ** ***
** ** **
ns ns ns
ns: not significant (p>0.10); : p<0.10; *: p<0.05; **: p<0.01; ***: p<0.001. within each source of variation values in the same line followed by different letters are significantly different by LSD test (p<0.05). GElinlinear effect of GE intake level (orthogonal contrast). GEquadquadratic effect of GE intake level (orthogonal contrast). No interaction was significant (p>0.10). a,b,c
Table 4 Maintenance energy requirements (NEm; kJ/Kg W0.75) and efficiency of utilisation of metabolisable energy for maintenance (km) BW groups
NEm
km
r
Level of significance
LW HW Overalla
503 (SE 72.5) 484 (SE 134.2) 494 (SE 74.4)
0.85 (SE 0.206) 0.72 (SE 0.301) 0.79 (SE 0.211)
0.84 0.58 0.68
p<0.05 p<0.10 p<0.05
a
Overall value estimated considering all the experimental animals.
rate being inversely related to energy intake. These observations are consistent with the notion that in underfed animals, fatty acid catabolism increases progressively as the supply of oxidisable alimentary nutrients declines (Pethick et al., 1984). An interesting aspect concerning fat mobilisation was the difference observed between experimental BW groups when fat losses were expressed in relation to metabolic BW. There is evidence from ewes in different physiological states that the capacity to mobilise body fat reserves is positively related to the level of body fat (Gibb and Treacher, 1980; Buratovich, 1995). Differences in fat mobilisation between lambs of different BW detected in this experiment could be related to the development of the adipose tissue. Lambs from the HW group had almost double body fat than the lambs from the LW group (102 vs. 55 g of fat/kg EBW). When fat losses were expressed in relation to the initial body fat reserves, the LW group showed a larger daily rate (p<0.05) than the HW group (6.3 vs. 4.5%) which suggests that the higher body fat losses in the HW group were simply due to a higher amount of body fat rather than to differences in the rate of the metabolic processes involved in lipolysis and fatty acid catabolism.
Studies of different animal species, including lambs, have demonstrated that fat mobilisation can provide energy to sustain positive N balance in animals with inadequate energy-yielding nutrition but with an adequate protein supply (Fowler et al., 1983; Hovell et al., 1983; érskov et al., 1983; Vipond et al., 1989; Chawdury et al., 1990). Low intake after weaning of lambs can also cause fat losses while protein gain continues (Graham, 1982). The present results support these ®ndings, although the HW group showed a larger protein accretion than LW group. Since N supply (g/kg BW0.75) within the same level of energy intake was similar for LW and HW lambs but fat losses were higher for HW lambs, fat mobilisation seems to be the main factor explaining the differences observed between BW groups in protein retention. Although more energy was used for protein synthesis by the HW group, neither total energy losses (relative to metabolic BW) nor fasting metabolism and ef®ciency with which dietary ME replaces body fat and protein as a source of energy for maintenance differed between BW groups. In contrast and as a consequence of the different levels of fat mobilisation, N balance occurred at lower energy input for the HW (17942.7 kJ ME/kg
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F.J. GiraÂldez et al. / Small Ruminant Research 31 (1999) 127±133
Table 5 Estimates of the net energy requirements for maintenance (kJ NEm/kg metabolic weight) of milk-fed lambs Source
Method of estimation
NEm requirements
Walker and Faichney, 1964 Kielanowski, 1965 Chiou and Jordan, 1973 Graham et al., 1974 ARC, 1980 Degen and Young, 1982 MantecoÂn, 1986 Present studya
Calorimetric Serial slaughter Serial slaughter Calorimetric Calorimetric Calorimetric Serial slaughter Serial slaughter
438 kJ/kg W0.73 372 kJ/kg W0.73 444 kJ/kg W0.75 539 kJ/kg W0.75 350 kJ/(kg W/1.05)0.75 536 kJ/kg W0.75 506 kJ/kg W0.75 494 kJ/kg W0.75
a
Overall value estimated considering all the experimental animals.
BW0.75) than for the LW group (34913.3 kJ ME/kg BW0.75) which implies a better ability to mobilise extra energy from body fat reserves for the HW group. Fattet et al. (1984) suggest that protein accretion in animals with negative energy balance may depend on the overall energy status of the animals, which is in agreement with the present results. As shown in Table 5, values of NEm obtained here are comparable to other published data, although present estimates seem consistently higher than NEm values proposed by the Agricultural Research Council (ARC, 1980). The ARC estimates of maintenance energy requirements are based on calorimetric studies and it is known that fasting metabolism declines during starvation periods (Alexander, 1962; ARC, 1980). Additionally and in contrast to mature sheep, heat production of milk-fed lambs is not constant after fasting for 72 h, although at this time metabolism can decrease to more than 50% of initial heat production (Graham et al., 1974). Therefore, these features could explain the higher values found in the present study compared with ARC (1980), even though it might also be expected that fasting metabolism decreases in underfed animals. However, our estimates of NEm are comparable to NEm values obtained by MantecoÂn (1986) with Churra milk-fed lambs fed above maintenance. In summarising the above results, it may be concluded ®rstly that fatty acid catabolism from body fat reserves can supply extra energy to sustain positive N balances in lambs fed below maintenance energy requirements provided that protein is supplied above the level needed to replace the endogenous losses. It is concluded that the rate of fat mobilisation per kg of metabolic BW is directly related to total body fat
reserves. However, under severe energy restrictions the level of adipose tissue may not be suf®cient to avoid the catabolism of body protein reserves. In contrast to earlier studies, there is no evidence in this study that maintenance energy requirements changed quantitatively during the milk-fed phase, although the limited range of BW tested must be considered before getting de®nitive conclusions.
Acknowledgements The authors wish to thank I.A. Wright for revision of the manuscript and A. GoÂmez for technical assistance. This research was supported by the project GAN 90-0906.
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