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J. Anim. Sci. 2003. 81:1847-1852
© 2003 American Society of Animal Science

Relationship between aging and nutritionally controlled growth rate on heat production of heifers1

H. C. Freetly1, J. A. Nienaber and T. M. Brown-Brandl

USDA, ARS, U.S. Meat Animal Research Center, Clay Center, NE 68933

2 Correspondence:
P.O. Box 166 (phone: 402-762-4202; fax: 402-762-4209; E-mail:
freetly{at}email.marc.usda.gov).


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The first objective of this study was to test how well a function that was developed to describe heat production (HP) in growing ewes fit HP data in growing heifers. The second objective was to determine the pattern of adaptation of HP to feed restriction and subsequent realimentation of nutrients. At 234.5 ± 0.5 d of age, HP was determined by indirect calorimetry on 32 Meat Animal Research Center III heifers. Following the first calorimetry measurement, heifers on the High-High (HH) treatment continued to receive ad libitum access to feed, and daily feed offered to the Low-High (LH) heifers was set at 157 Mcal of ME/kg of BW0.75. Feed restriction of LH heifers continued for 84 d. After 84 d of restriction, LH heifers were allowed ad libitum access to feed. Heat production was determined 4 and 11 wk following feed restriction and 2, 5, 12, and 18 wk following realimentation. There was no residual bias when HP in ad libitum-fed heifers was estimated with an equation form developed in growing ewes: [(kcal/d) = f(BW, matBW) = BW {Ae[k(BW/mature BW)]}], nor was there a residual bias when HP was predicted with an allometric equation: [(kcal/d) = f(BW) = A(BWk)]. However, there were residual biases when HP was estimated with an allometric equation that set the exponent to 0.75. Heat production per unit of BW of LH heifers was lower than that of HH heifers at 4 wk of feed restriction (P < 0.001), but HP did not differ between treatments at 11 wk of feed restriction (P = 0.87). At 2 (P = 0.002) and 5 wk (P < 0.001) following the increase in feed offered, HP per unit of BW of the LH heifers was greater than that of the HH heifers. Heat production did not differ between treatments at 12 and 18 wk following refeeding (P < 0.17). Our findings demonstrate that the relationship between HP and BW is described equally well by a logistic and allometric function, but applying a generalized interspecies exponent in an allometric equation to growing heifers results in a bias in estimating HP. The equation form developed in ewes can be used to develop a single equation for the prediction of HP across ages in heifers.

Key Words: Aging • Heat Production • Heifers • Nutrition


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Heat production (HP) per unit of BW decreases as heifers age (Ritzman and Colovos, 1943). Many of the current models used to estimate the energy expenditure of growing heifers account for this decrease by expressing HP as a function of BW raised to a power (CSIRO, 1990; AFRC, 1993; NRC, 1996). Brody (1945) reported that in dairy heifers, HP per unit of BW decreased more rapidly during the first 5 to 6 mo of age than in older females. Subsequently, two separate allometric equations were required to describe the relationship between HP per unit of BW and age. Previously, we reported that a single equation that included a measurement of level of maturity improved the predictability of energy expenditure of growing ewes (Freetly et al., 2002a). We also found that the pattern of decrease in HP with aging was altered by level of nutrition (Freetly et al., 2002b). Based on our observations in sheep and those of Brody (1945), we hypothesized that the reduction in HP with aging in beef females is inversely related to advancing maturity. The first objective of this study was to test how well a function that was developed to describe HP in growing ewes fit HP data in growing heifers (Freetly et al., 2002a). The second objective was to determine the pattern of adaptation of HP to feed restriction and subsequent repletion of nutrients.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
Thirty-two Meat Animal Research Center (MARC) III (four breed composite: 1/4 Hereford, 1/4 Angus, 1/4 Red Poll, 1/4 Pinzgauer) heifers were weaned when they were 147.5 ± 0.7 d of age and weighed 172 ± 3 kg. Heifers were placed eight to a pen (452 m2) and individually fed with Calan gates (American Calan Inc., Northwood, NH). Heifers were fed a diet of 20% alfalfa hay, 22% corn, 54.3% corn silage, 0.5% limestone, 3% soybean meal, and 0.2% sodium chloride as a percentage of DM (ME = 2.60 Mcal/kg and CP = 12.4%). The chemical composition of the diet was 48.7% DM, 5.6% ash, 36.5% NDF, 63.5% cell contents, 21.8% ADF, and 17.3% cellulose. Heifers were fed twice a day and allowed ad libitum access to feed. Feed refusals were determined weekly, and BW was determined every 3 wk. Heifers were trained to be used in indirect calorimeters, and at 234.5 ± 0.5 d of age, HP was determined by indirect calorimetry. Following the first calorimetry measurement, heifers on the High-High (HH) treatment continued to receive ad libitum access to feed, and daily feed offered to the Low-High (LH) heifers was set at 157 Mcal ME/kg BW0.75. Feed restriction of LH heifers continued for 84 d. After 84 d of feed restriction, LH heifers were allowed ad libitum access to feed. Heat production was determined 4 and 11 wk following feed restriction and 2, 5, 12, and 18 wk following realimentation.

Individual heifer gaseous exchange was determined for 23 h. Measurement of gaseous exchange and calculation of HP were performed as previously described by Nienaber and Maddy (1985). Heifers received their daily feed at the beginning of calorimetry measurement. Body weight was the average of the BW at the beginning and end of the 23-h measurement. Daily HP was extrapolated from the 23-h HP by dividing the 23-h HP by 23 h and multiplying by 24 h. Experimental procedures were conducted in accordance with the U.S. MARC Animal Care Guidelines and the Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching (FASS, 1999).

Data from the LH heifers in Period 1 and all of the data from the HH heifers were used to determine the relationship between BW on age (Figure 1Go), HP on age (Figure 2Go), and HP on BW (Figure 3Go and 4Go). The relationship between BW and age was initially fit with a quadratic equation, but there was not an improvement in fit compared with a linear regression; subsequently, a linear equation was used to describe the relationship (Figure 1Go).



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  		Figure 1. Relationship between BW (kg) and age (wk) of heifers: BW = f(t) = 6.23t - 26.0 (R2 = 0.92), where t is equal to weeks of age.

 


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  		Figure 2. Relationship between daily HP (kcal/kg) and age (wk): HP = f(t) = 28.7 + 88.0e-0.0586t of heifers, where t is equal to weeks of age.

 


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  		Figure 3. Relationship between daily HP and BW of heifers: —— HP = f(BW, MatBW) = BW53.1e-0.709(BW/MatBW), — — — — HP = 146.1BW0.75, and - - - HP = 404.1BW0.58, where MatBW is equal to mature BW (550 kg).

 


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  		Figure 4. Residuals for the prediction equation HP = f(BW, MatBW) = BW53.1e-0.709(BW/MatBW): slope -0.039 ± 0.078 (H0: slope = 0; P = 0.62) and intercept 434 ± 874 (H0: intercept = 0; P = 0.62) (a). Residuals for the prediction equation HP = 404.1BW0.58: slope -0.229 ± 0.061 (H0: slope = 0; P < 0.001) and intercept 2597 ± 684 (H0: intercept = 0; P < 0.001) (b). Residuals for the prediction equation HP = 146.1BW0.75: slope -0.0056 ± 0.0791 (H0: slope = 0; P < 0.94) and intercept 64 ± 886 (H0: intercept = 0; P < 0.94) (c).

 
Parameter estimates for nonlinear functions (Figures 2Go and 3Go) were calculated using the Gauss-Newton method to fit the nonlinear regression model. The nonlinear procedures in SAS version 6.1 (SAS Inst., Inc., Cary, NC) were used to calculate estimates.

Differences in nutritional treatments for BW and HP (Figure 5Go) were tested with a split-plot model. The model consisted of nutritional treatment, animal nested in treatment, period, and treatment x period. Effects of nutritional treatment were tested using the animal nested in treatment as the error term. Data were analyzed using the GLM procedure in SAS version 6.1 (SAS Inst., Inc.).



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  		Figure 5. Means and standard errors of heifers with ad libitum access to feed (—•) and heifers feed restricted for 84 d followed by ad libitum access to feed (- - - {blacksquare}). Observations for HH heifers (—•) for Periods 1 though 7 were 14, 13, 14, 16, 16, 17, and 17. Observations for LH heifers (- - - {blacksquare}) for Periods 1 though 7 were 15, 16, 15, 14, 14, 14, and 13.

 

   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
Relationship Between Heat Production and Aging
Body weight increased 6.23 kg/wk with advancing age (Figure 1Go). Heat production per unit of BW decreased exponentially as age advanced (Figure 2Go). Whole-animal HP increased at a decreasing rate as BW increased (Figure 3Go).

Two equation forms were tested to determine their ability to fit the relationship between HP and BW. Equation 1Go was developed in sheep to describe the relationship between HP and BW as ewes age (Freetly et al., 2002a). Mature BW of MARC III cows was estimated to be 550 kg at a body condition score of 5.5 (Freetly et al., 2000).


[1]

The parameter estimates for Eq. 1Go were 53.1 ± 2.7 for A and -0.70 ± 0.08 for k. Analysis of the residuals for Eq. 1Go (Figure 4aGo) shows that the equation predicts HP without bias.

Equation 2Go is the allometric form that is commonly used to predict nutrient requirements. Equation 2Go was solved using two approaches. In the first approach, parameters A and k were both solved. In the second, approach k was set to the interspecies exponent of 0.75 (Kleiber, 1947) and A was solved:


[2]

When both A and k were solved in Equation 2Go, the parameter estimates were 404 ± 109 for A and 0.58 ± 0.05 for k. There were no biases in the residual estimates when both A and k are solved (Figure 4bGo). When the exponent term is set to 0.75, the parameter estimate for A is 146.1 ± 1.5. Analysis of residuals for Eq. 2Go with k set to 0.75 demonstrates that there is a bias in the prediction of HP, where at lower predicted HP, the equation underpredicts HP, and at higher predicted HP, the equation overpredicts HP (Figure 4cGo).

Nutritional History and Heat Production
Heifers on the HH treatment ate less DM on the day of calorimetry then they averaged during the week before calorimetry (P < 0.001; 3.86 ± 0.34 vs. 6.15 ± 0.15 at 0 wk, 4.28 ± 0.35 vs. 6.94 ± 0.17 at 4 wk, 4.93 ± 0.39 vs. 8.16 ± 0.24 at 11 wk, 5.63 ± 0.33 vs. 8.04 ± 0.25 at 14 wk, 5.45 ± 0.32 vs. 8.27 ± 0.27 at 17 wk, 5.58 ± 0.46 vs. 9.16 ± 0.20 at 24 wk, 5.35 ± 0.38 vs. 9.72 ± 0.23 at 30 wk). Heifers on the LH ate less DM on the day of calorimetry than they averaged the week before calorimetry during wk 0, 11, 14, 17, 24, and 30 (P < 0.023), but intakes did not differ (P = 0.27) during wk 4 (4.12 ± 0.40 vs. 6.28 ± 0.16 at 0 wk, 4.17 ± 0.08 vs. 3.90 ± 0.06 at 4 wk, 4.35 ± 0.09 vs. 4.52 ± 0.08 at 11 wk, 6.00 ± 0.34 vs. 6.57 ± 0.53 at 14 wk, 5.83 ± 0.50 vs. 8.80 ± 0.38 at 17 wk, 6.23 ± 0.41 vs. 9.92 ± 0.43 at 24 wk, 5.12 ± 0.38 vs. 10.57 ± 0.44 at 30 wk). Following realimentation, previous week DMI for the LH heifers was lower than HH heifers for wk 14 (P = 0.003), but intakes did not differ between LH and HH heifers for wk 17, 24, and 30 (P > 0.12).

After 84 d of feed restriction, LH heifers weighed less (267 ± 5 kg) than HH heifers (308 ± 5 kg; P < 0.001). Daily gain after 14 d of realimentation was greater for LH heifers (1.01 ± 0.08 kg/d) than for HH heifers (0.87 kg/d; P = 0.001). At the end of the experiment, LH heifers weighed 14 kg less than HH heifers (Figure 5aGo). Heat production per unit of BW of LH heifers was lower than HP for HH heifers at 4 wk of feed restriction (P = 0.001), but HP did not differ between treatments at 11 wk of feed restriction (P = 0.66; Figure 5bGo). At 2 and 5 wk following the increase in feed offered, HP per unit BW of the LH heifers was greater than that of the HH heifers (Figure 5bGo; P < 0.002). Heat production did not differ between the treatments at 12 and 18 wk following refeeding (Figure 5bGo; P > 0.17).


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
In the current study, ad libitum DMI was lower on the day that calorimetry measurements were taken compared with the previous week’s average intake, which will result in an underestimate of HP. Blaxter and Wainman (1996) measured a 10 to 12% decrease in HP after a 24-h fast in steers previously fed for no weight change. This reduction in HP is similar to that observed by Graham et al. (1974) in growing lambs after a 24-h fast. However, the reduction in HP due to reduced feed intake of ad libitum fed animals most likely is greater than that of maintenance-fed animals. Given that our diet has a partial efficiency for gain of 0.42 (Garrett, 1980), ad libitum-fed animals would have a 27% reduction in HP.

Various groups have reported that HP increases at a decreasing rate as BW increases (Brody, 1945; Kleiber, 1947) and that this decrease in HP can be described by the allometric function HP = f(BW) = A x BWb. There have been numerous discussions regarding the correct value for the exponent (b), but the general consensus has been that the interspecies exponent is 0.75. Given that BW and age are highly correlated, the current nutrient recommendations for beef cattle (NRC, 1996) have applied the interspecies coefficient to the growing animal to account for the decrease in HP per unit BW with increased age (NRC, 1996). In the current study, estimates of HP using the interspecies exponent were biased such that HP was underpredicted at lighter BW and overpredicted at heavier BW (Figure 4cGo). Alderman et al. (1970) found that when fasting heat production was predicted using an allometric equation with the exponential term set to 0.73, the "constant" parameter needed to be corrected for age. We found similar biases in estimating HP in ewes with the interspecies coefficient (Freetly et al., 1995). There was no bias associated with the residuals when both parameters of the allometric equation were allowed to vary. Brody (1945) demonstrated that the resting HP of growing heifers could be described by two allometric equations with the transition from the first equation to the second equation occurring between 5 to 6 mo of age. Brody (1945) reported exponential terms of 0.60 (Jersey) and 0.56 (Holstein) for heifers over 6 mo of age, which is similar to the 0.58 value that we calculated. These findings suggest the bias associated with the use of the interspecies coefficient is inherent to the value of the exponent rather than form of the function.

Both of the equation forms describe the decrease in HP per unit BW as heifers age. Potential contributors to this decrease in HP per unit BW with advancing age may include a decrease in the proportional weight of metabolically active tissues, such as nerve, intestinal, and liver to total BW (Moulton et al., 1922). Other factors that may contribute include a reduction in the metabolic rate of tissues with aging that results from a decrease in the rate of substrate cycles such as protein turnover (Lobley et al., 1980).

Studies in sheep (Freetly et al., 2002a) demonstrated that breed differences in HP at any age could be accounted for by expressing HP as a function of level of maturation. Brody (1945) reported that there are breed differences in the rate of decrease in HP of cattle, suggesting that, like sheep, differences in cattle breeds may be described by an equation that accounts for relative maturity. In the current study, we applied the same equation form developed in sheep (Freetly et al., 2002a), which accounts for level of maturity to heifers and concluded that the equation described HP in heifers whose growth is not nutritionally limited (Figure 4aGo). Whereas the form adequately described the current data set, the actual parameter estimates are constrained by the relatively narrow range of ages that data was collected over (33 to 66 wk). Further evaluation of the equation form will require HP measurements in both younger and older females.

Numerous studies have described the phenomenon of compensatory gain (Clanton et al., 1983; Yambayamba and Price, 1991). Compensatory gain is characterized by an accelerated rate of growth and an increase in the gain:feed intake ratio when previously nutritionally restricted growing animals are brought to levels equal to, or in excess of, animals with full access to nutrients. In the current study, the refed animals had a greater rate of gain during the repletion period. Most feeding systems in current use assign energy cost associated with growth to energy required for maintenance or energy required for gain. Whereas this model has proven to be a useful tool in predicting energy requirements, any assumptions made about energy expenditure for maintenance or growth will force an interpretation in the other component. It has been speculated that the cause of compensating gain may be the result of a lag in the energy required for maintenance (Wilson and Osbourn, 1960), or it may result from a temporary change in the efficiency of gain (Meyer and Clawson, 1964). Total HP represents the aggregation of heat produced for maintenance and growth. In the present study, HP increased immediately following refeeding and remained elevated. Ferrell et al. (1986) reported that 6 wk after lambs were refed, HP was higher in the refed lambs than in lambs growing at a constant rate. Their data is consistent with what we observed within the first 5 wk of refeeding. We can speculate that the increase in HP immediately following realimentation may be associated with both maintenance and growth and that assignment of energy cost becomes an issue of accounting rather than one of biology. A number of events probably occur when heifers are repleted. Typically during nutrient restriction, there is a decrease in the weight of visceral tissues, and upon repletion, those tissues increase in weight (Drouillard et al., 1991; Wester et al., 1995; Sainz and Bentley, 1997). The weight of visceral tissues upon repletion seems to be partially a function of the level of refeeding (Ferrell et al., 1986). These increases in visceral weights upon repletion suggest that the immediate increase in HP may be associated partially with the synthesis and accretion of highly metabolically active tissues. If efficiency of tissue accretion is defined as the ratio of energy accreted over energy for tissue turnover, then it is possible to accrete a given amount of tissue at different efficiencies. If both rates of tissue synthesis and degradation increase and the net difference between synthesis and degradation increases (rate of accretion), it would be plausible to have both an increase in HP and an increase in accretion rate. An increase in rate of protein accretion in realimented heifers may be a mechanism by which both BW gain increases and HP increases. Millward et al. (1975) observed both an increase in fractional protein synthesis and degradation in skeletal muscle of rats that had been protein malnourished and subsequently realimented.

In conclusion, our findings demonstrate that the relationship between HP and BW is described equally well by a logistic and allometric function, but applying a generalized interspecies exponent in an allometric equation to growing heifers results in a bias in estimating HP. The decrease in tissue metabolic activity with aging should be considered when developing prediction equations. The equation form developed in ewes can be used to develop a single equation for the prediction of HP across ages in heifers.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
Changes in heat production associated with aging need to be accounted for when developing estimates of how much feed will be retained in animal products. The proposed equation can potentially be used to estimate energy released as heat across a wide range of ages and breeds.


   Footnotes
 
1 The authors would like to acknowledge the technical support of C. Haussler and D. Marintzer. Back

Received for publication July 8, 2002. Accepted for publication March 11, 2003.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


AFRC. 1993. Energy and Protein Requirements of Ruminants. An Advisory Manual Prepared by the AFRC Technical Committee on Responses to Nutrients. CAB International, Wallingford, U.K.

Alderman, G., D. E. Morgan, and W. J. Lessells. 1970. A comparison of live weight gains of beef cattle with values predicted from energy intakes measured as starch equivalent or metabolizable energy. Page 84 in Energy Metabolism of Farm Animals. EAAP Publ. No. 13, Vitznau, Switzerland.

Blaxter, K. L. and F. W. Wainman. 1966. The fasting metabolism of cattle. Br. J. Nutr. 20:103–111.[Medline]

Brody, S. 1945. Bioenergetics and Growth. Hafner Publishing Co., Inc., New York.

Clanton, D. C., L. E. Jones, and M. E. England. 1983. Effect of rate and time of gain after weaning on the development of replacement beef heifers. J. Anim. Sci. 56:280–285.

CSIRO. 1990. Ruminants. Feeding Standards for Australian Livestock. CSIRO Publications, Melbourne, Australia.

Drouillard, J. S., T. J. Klopfenstein, R. A. Britton, M. L. Bauer, S. M. Gramlich, T. J. Wester, and C. L. Ferrell. 1991. Growth, body composition, and visceral organ mass and metabolism in lambs during and after metabolizable protein or net energy restrictions. J. Anim. Sci. 69:3357–3375.[Abstract]

FASS. 1999. Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching. 1st rev. ed. Fed. Anim. Sci. Soc., Savoy, IL.

Ferrell, C. L., L. J. Koong, and J. A. Nienaber. 1986. Effect of previous nutrition on body composition and maintenance energy costs of growing lambs. Br. J. Nutr. 56:595–605.[Medline]

Freetly, H. C., C. L. Ferrell, and T. G. Jenkins. 2000. Timing of realimentation of mature cows that were feed-restricted during pregnancy influences calf birth weights and growth rates. J. Anim. Sci. 78:2790–2796.[Abstract/Free Full Text]

Freetly, H. C., J. A. Nienaber, and T. Brown-Brandl. 2002a. Relationships among heat production, body weight, and age in Finnsheep and Rambouillet ewes. J. Anim. Sci. 80:825–832.[Abstract/Free Full Text]

Freetly, H. C., J. A. Nienaber, and T. Brown-Brandl. 2002b. Relationships between aging and nutritional controlled growth rate on heat production of ewe lambs. J. Anim. Sci. 80:2759–2763.[Abstract/Free Full Text]

Freetly, H. C., J. A. Nienaber, K. A. Leymaster, and T. G. Jenkins. 1995. Relationships among heat production, body weight, and age in Suffolk and Texel ewes. J. Anim. Sci. 73:1030–1037.[Abstract]

Graham, N. M., T. W. Searle, and D. A. Griffiths. 1974. Basal metabolic rate in lambs and young sheep. Aust. J. Agric. Res. 25:957–971.

Kleiber, M. 1947. Body size and metabolic rate. Physiol. Rev. 27:511–541.[Free Full Text]

Lobley, G. E., V. Milne, J. M. Lovie, P. J. Reeds, and K. Pennie. 1980. Whole body and tissue protein synthesis in cattle. Br. J. Nutr. 43:491–502.[Medline]

Meyer, J. H., and W. J. Clawson. 1964. Undernutrition and subsequent realimentation in rats and sheep. J. Anim. Sci. 23:214–224.

Millward, D. J., P. J. Garlick, R. J. C. Stewart, D. O. Nnanyelugo, and J. C. Waterlow. 1975. Skeletal-muscle growth and protein turnover. Biochem. J. 150:235–243.[Medline]

Moulton, C. R., P. F. Trowbridge, and L. D. Haigh. 1922. Studies in animal nutrition. II. Changes in proportions of carcass and offal on different planes of nutrition. MO Agr. Exp. Stn. Res. Bull. 54, Univ. of Missouri, Columbia.

Nienaber, J. A., and A. L. Maddy. 1985. Temperature controlled multiple chamber indirect calorimeter-design and operation. Transact. ASAE 28:555–560.

NRC. 1996. Nutrient Requirements of Beef Cattle. 7th rev. ed. Natl. Acad. Press, Washington, DC.

Ritzman, E. G., and N. F. Colovos. 1943. Physiological requirements and utilization of protein and energy by growing dairy cattle. New Hampshire Exp. Stn. Tech. Bull. No. 80:1–59.

Sainz, R. D., and B. E. Bentley. 1997. Visceral organ mass and cellularity in growth-restricted and refed beef steers. J. Anim. Sci. 75:1229–1236.[Abstract/Free Full Text]

Wester, T. J., R. A. Britton, T. J. Klopfenstein, G. A. Ham, D. T. Hickok, and C. R. Krehbiel. 1995. Differential effects of plane of protein or energy nutrition on visceral organs and hormones in lambs. J. Anim. Sci. 73:1674–1688.[Abstract]

Wilson, P. N., and D. F. Osbourn. 1960. Compensatory growth after undernutrition in mammals and birds. Biological Reviews 35:324–363.[Medline]

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