DIGESTIBLE ENERGY REQUIREMENTS FOR MAINTENANCE OF BODY MASS OF WHITE-TAILED DEER IN SOUTHERN TEXAS
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1 Journal of Mammalogy, 86(1):56 60, 2005 DIGESTIBLE ENERGY REQUIREMENTS FOR MAINTENANCE OF BODY MASS OF WHITE-TAILED DEER IN SOUTHERN TEXAS BRONSON K. STRICKLAND,* DAVID G. HEWITT, CHARLES A. DEYOUNG, AND RALPH L. BINGHAM Caesar Kleberg Wildlife Research Institute, Texas A&M University Kingsville, Campus Box 218, Kingsville, TX 78363, USA Present Address of BKS: Department of Wildlife & Fisheries, Mississippi State University, Mail Stop 9690, Mississippi State, MS , USA Previous experiments designed to estimate daily digestible energy requirements for body-mass maintenance in white-tailed deer (Odocoileus virginianus) were conducted using deer adapted to northern environments. However, animals adapted to warmer, drier environments may have lower metabolic requirements than their temperate conspecifics. We conducted a feeding trial to estimate digestible energy requirements for maintenance of body mass of white-tailed deer in southern Texas and to determine if those requirements vary over time. By restricting dietary levels of digestible energy and measuring deer body mass every 3 days for a 30-day period, we developed a model relating digestible energy intake and change in body mass over time for 11 adult, nongravid females during autumn. Predicted daily digestible energy intake requirements for body-mass maintenance (kj/kg body mass 0.75 ) ranged from SE at trial initiation to at trial completion. Our experiment demonstrated that daily digestible energy maintenance requirements decline during extended periods of energetic restriction and that values previously reported may overestimate the requirements for deer in southern latitudes. Key words: body-mass maintenance, digestible energy, intake, Odocoileus virginianus, Texas, white-tailed deer Many mammalian species in arid environments have metabolic requirements that are lower than expected for their body size (Hudson and Christopherson 1985; Lovegrove 2000; Schmidt-Nielsen 1984). Species from arid areas of lower primary productivity have lower metabolic rates than congenerics from mesic areas with greater productivity (Mueller and Diamond 2001). The effects of differing environmental conditions (e.g., temperature, rainfall) on animal thermoregulation and on availability and quality of forage may influence metabolic requirements and resultant energy requirements for maintenance of body mass. Daily digestible energy requirements for stasis of body mass (hereafter referred to as maintenance) have been documented for adult white-tailed deer from northern latitudes (Pennsylvania Cowan and Clark 1981; Michigan Ullrey et al. 1969, 1970). Ullrey et al. (1969) were the first to develop an equation relating change in body mass to digestible energy consumption for adult white-tailed deer. Using 24 gravid females, their experiment yielded a linear relationship between daily change in body mass (kg) and daily digestible energy intake (kj), adjusted for * Correspondent: bstrickland@cfr.msstate.edu Ó 2005 American Society of Mammalogists metabolic body mass (kj/kg 0.75 ), which extrapolated to 670 kj/kg 0.75 for maintenance of body mass. Similar estimates (674 and 661 kj/kg body mass 0.75 ) were documented in other studies from northern environments (Cowan and Clark 1981; Ullrey et al. 1970). Further, Ullrey et al. (1969, 1970) determined that daily digestible energy requirements were greater earlier in the study than at the end, thus demonstrating that daily digestible energy requirements change during prolonged periods of food restriction. They explained the reduction in requirements as a response to the loss of adipose tissue and the tendency of basic metabolic rates to decrease during periods of starvation. Because the relationship between intake and maintenance is timedependent, an equation that incorporates this temporal dependency is needed to estimate daily digestible energy requirements for white-tailed deer, particularly when change in body mass is used to determine maintenance requirements or digestible energy intake (McCall et al. 1997). Therefore, to determine if estimates of daily digestible energy requirements for deer in more southern latitudes are similar to those previously reported, we conducted an experiment to develop a model that estimates the relationship between body mass change, daily digestible energy intake, and time for southern Texas deer (Odocoileus virginianus). MATERIALS AND METHODS Experimental procedures. We conducted our experiment at the research facility of the Caesar Kleberg Wildlife Research Institute at 56
2 February 2005 STRICKLAND ET AL. DEER DIGESTIBLE ENERGY REQUIREMENTS 57 Texas A&M University-Kingsville in Kingsville, Texas, from 13 November to 13 December We used 12 adult (4 years old), nongravid females that were bottle-raised as fawns and were accustomed to human interaction and being housed in pens to facilitate handling and weighing. Experimental animals were progeny of deer captured in southern Texas with an average mass of 44.8 kg SE before our experiment. We isolated each deer in a 3 3 m pen covered by a roof yet exposed to ambient temperatures and light cycles. Mean temperatures were 178C and 148C for November and December, respectively (National Oceanic and Atmospheric Administration 1997). We fed deer 56A3 Kleberg Custom Deer Feed Hi-P pellets (16% crude protein and 9.46 kj/g of digestible energy; Purina Mills, Inc., St. Louis, Missouri) for 1 week to determine the average ad libitum intake for each deer. Digestible energy was calculated from a total balance digestion trial conducted during the study of Campbell and Hewitt (2000). We blocked deer in groups of 4 according to body mass. Each deer in a block was randomly placed in 1 of 4 feeding treatments (3 deer in each treatment; treatments consisted of 85%, 65%, 45%, and 25% of each deer s pretrial ad libitum intake). Deer remained in their respective feeding treatment throughout the trial. A sample (100 g) of the daily ration and any uneaten food was oven dried at 1008C for 24 h to determine dry matter intake. We provided water ad libitum. We weighed deer every 3 days at 1500 h in a crate with a scale (Allflex FX 11, Dallas Fort Worth Airport, Texas) positioned beneath it. We removed food and water at 0900 h on the days we weighed deer. At trial termination, we calculated metabolically scaled, mean daily digestible energy intake (kj/kg 0.75 ) and metabolically scaled, mean daily mass change (g/kg 0.75 ) for each deer for 10 time periods, i.e., 1 3 days, 1 6 days, 1 9 days, 1 12 days, 1 15 days, 1 18 days, 1 21 days, 1 24 days, 1 27 days, and 1 30 days. For each period, we calculated mean daily digestible energy intake by multiplying total dry matter intake (g) during the period by 9.46 kj/g of digestible energy and divided the product by the number of days in the period. We then divided the quotient by the mean metabolic mass (kg 0.75 ) of the deer for that period to determine the daily mean digestible energy intake (kj/ kg 0.75 ). We calculated mean daily mass change (g/kg 0.75 ) for a period by subtracting the initial mass (day 1) from the final mass in the period and dividing the difference by the period-specific, mean metabolic mass (kg 0.75 ) and the number of days in the period. The trial lasted 30 days, but if a deer lost 15% of its body mass, it was removed from the trial and provided feed ad libitum. This study conformed to the guidelines established by the American Society of Mammalogists (1998) and was approved by the Texas A&M University-Kingsville Animal Care and Use Committee. Statistical analysis. We regressed mean daily mass change (g/kg 0.75 ) on average daily digestible energy intake (kj/kg 0.75 ), day, intake day, intake 2, and day 2 in the response surface regression (RSREG) procedure (Freund and Littell 2000) in SAS (1999) to determine if mean mass change responded linearly or nonlinearly to aid in subsequent model development. We recognize that repeated samples of individuals were not independent, but for the purpose of determining the general shape of the response curve, we thought this was a straightforward method. We removed 2 deer in the 25% feeding treatment from trial due to excessive mass loss (15%) at 24 and 27 days following trial initiation. Also, we considered 1 deer an outlier and removed it from analysis because its predicted intake requirements for maintenance were biologically unreasonable (i.e.,.2,000 kjkg body mass 0.7 day 1 at trial initiation) and its inclusion in our models greatly distorted model parameters, variation associated with model predictions, and caused distributions of maintenance estimates to deviate from normality. Results from the RSREG procedure indicated that linear (F ¼ 90.51, d.f. ¼ 2, 111, P, 0.001) and quadratic (F ¼ 21.98, d.f. ¼ 2, 111, P, 0.001) terms were important in our model but a cross-product term (F ¼ 2.04, d.f. ¼ 1, 111, P ¼ 0.156) did not contribute to the model. Thus, we decided to evaluate 3 models: a quadratic model (intake, days, and days 2 ), a linear model with a spline (intake, days, and [days knot]), and a quadratic model with a spline (intake, days, days 2, [days-knot], and [days knot] 2 ). A spline model may fit better than a quadratic model if there is a pronounced change in the slope over a narrow range of x values. In essence, a spline model incorporates 2 functions in 1 model. That is, depending on the value of an independent variable, additional variables are included or excluded from the model. For example, a linear spline model with independent variable x would take the form y ¼ b 0 þðb 1 xþþe if x is a specified value (called the knot ), and the model takes the form y ¼ b 0 þðb 1 xþþðb 2 ½x knotšþ þ e if x is. the specified knot value (Freund and Littel 2000). The knot value is where (in the range of x values) the distinct change in slope occurs. With our data, we estimated a knot value of 7 days using the nonlinear (NLIN) procedure (Freund and Littel 2000) in SAS (1999). To account for repeated measurements of individuals and individual variation among deer in the relationship, we estimated values for model parameters using a random coefficients model in the MIXED procedure (Littell et al. 1996) in SAS (1999). With a random coefficients model the relationship between body-mass change and the intercept and slope coefficient(s) for each deer can be considered a random sample from a population of possible model coefficients (Littell et al. 1996). As a result, the procedure yields a model for each deer and a population model derived from all deer. So for each model, we included intercept and intake as random coefficients (we could not include days due to convergence problems). We compared population models using Akaike s information criterion (AIC) adjusted for smaller samples (AIC c Burnham and Anderson 1998), which is derived from the 2 log likelihood function and the number of estimable parameters in the model. Models were ranked according to AIC c, and the model(s) with the lowest AIC c was considered the best model in the set of models evaluated. However, if 2 models differed by 2, there is no evidence that only 1 model can be considered the best; in that case, there would be equal support for both models (Burnham and Anderson 1998). If that occurred, we chose to invoke parsimony and select the model with fewer terms. Also, we assessed model fit with the coefficient of determination defined as R 2 ¼ 1 X ðy ^yþ 2 Xðy yþ 2 (Kvalseth 1985). Based on the best model, we set the value of change in body mass (dependent variable) to 0 and solved the equation for intake to calculate daily digestible energy intake levels (kj/kg 0.75 ) required for maintenance from days 3 to 30. To estimate variation associated with the daily maintenance predictions, we calculated maintenance requirements for each deer using the individual models (from the best population model) and computed SE from the daily individual maintenance estimates. RESULTS Two models, the quadratic-spline (AIC c ¼ 611.0; R 2 ¼ 0.77), and linear-spline (AIC c ¼ 610.3; R 2 ¼ 0.77), fit equally well. We eliminated the quadratic model due to a much higher AIC c (664.0) and lower R 2 (0.69). Because the linear-spline had fewer terms, we chose it as the best model for subsequent
3 58 JOURNAL OF MAMMALOGY Vol. 86, No. 1 FIG. 2. Predicted maintenance requirements (6 SE) based on the equation change in body mass ¼ þ (0.051 intake) þ (4.865 day) (4.681 [day 7]) developed from a feeding trial conducted from 13 November to 13 December 1997 in Kingsville, Texas, using 11, nongravid, female white-tailed deer. Intake maintenance requirements are calculated by setting change in body mass (gkg body mass 0.75 day 1 ) to 0 and solving the equation for intake (kjkg body mass 0.75 day 1 ). Line marked A represents intake maintenance requirement reported by Ullrey et al. (1969), and line marked B represents our adjustment of the Ullrey et al. (1969) estimate. required for maintenance decreased over time (Fig. 2) from 820 (kjkg body mass 0.75 day 1 ) at trial initiation (day 3) to 357 (kjkg body mass 0.75 day 1 ) at trial completion (day 30). FIG. 1. Actual and predicted relationships between digestible energy intake (kjkg body mass 0.75 ) and change in body mass (gkg body mass 0.75 day 1 ) over time for female white-tailed deer in southern Texas. A) Average daily change in body mass (gkg body mass 0.75 day 1 ) related to daily digestible energy intake (kjkg body mass 0.75 ) for 10 time periods (i.e., 1 3 days, 1 6 days, 1 9 days,..., 1 30 days) from a feeding trial conducted from 13 November to 13 December 1997 in Kingsville, Texas, using 11, nongravid females. Each type symbol represents an individual deer. B) Predicted change in body mass (gkg body mass 0.75 day 1 ) from daily digestible energy intake (kjkg body mass 0.75 ) over time (days) based on the equation change in body mass ¼ þ (0.051 intake) þ (4.865 day) (4.681 [day 7]); R 2 ¼ maintenance calculations. The predictive equation from the linear-spline model was change in body mass ¼ 56:549 þð0:051 intakeþþð4:865 dayþ ð4:681 ½day 7ŠÞ where units for change in body mass and intake were (gkg body mass 0.75 day 1 ) and (kjkg body mass 0.75 day 1 ), respectively (Fig. 1). Based on this relationship, the predicted daily digestible energy intake (kjkg body mass 0.75 day 1 ) DISCUSSION Reported average estimates of daily digestible energy required for body-mass maintenance have ranged from 661 to 674 kj/kg body mass 0.75 for adult females (Cowan and Clark 1981; Ullrey 1969, 1970) and from 603 to 833 kj/kg body mass 0.75 (Croyle 1969; Thompson et al. 1973) for fawns. However, Ullrey et al. (1969) also provided daily digestible energy estimates of 812, 569, and 515 kj/kg body mass 0.75 for 1 3, 4 6, and 6 9 week periods, respectively, based on feeding trials. Our predicted daily digestible energy intake estimate of 820 (kj/kg body mass 0.75 ) from day 3 is similar to the 1 3 week estimate provided by Ullrey et al. (1969), although at day 30 our predicted estimate reached a minimum at 357 kj/kg body mass 0.75 (Fig. 2), much lower than estimates reported in previous studies. The high daily digestible energy estimate at the beginning of our trial may have been influenced by loss of body mass resulting from reduced rumen fill. In other words, deer may have appeared to lose mass at a greater rate than suggested by their daily digestible energy intake due to lower amounts of digesta from the restricted diet. The knot value of 7 days for our spline model delineates a change in the relationship between intake and change in body mass that may coincide with time required for rumen fill to equilibrate with intake.
4 February 2005 STRICKLAND ET AL. DEER DIGESTIBLE ENERGY REQUIREMENTS 59 Our model predicts a decline in daily digestible energy requirements for maintenance during extended periods of energy restriction. Ullrey et al. (1969, 1970) documented the same decrease in maintenance intake requirements throughout their feeding trials. However, because deer were weighed every 3 (Ullrey et al. 1969), 4, and 5 weeks (Ullrey et al. 1970) during their experiments, they could not develop an equation that modeled time on a continuous scale. Instead, they developed different equations for different time periods. Because we weighed our animals every 3 days, we were able to develop a single equation that included both intake and time. Our results suggest lower maintenance requirements for deer in southern latitudes compared with those from more northern latitudes; however, our experiment differed from those of Ullrey et al. (1969, 1970) in several ways. First, females used in the Ullrey et al. (1969, 1970) experiments were pregnant, which could increase the daily maintenance energy requirement as a result of energy deposited in the concepta and increases in dam metabolism resulting from gestation. To approximate the additional costs of pregnancy in the Ullrey et al. (1969) experiment, we multiplied their estimate of daily gross energy requirement for maintenance ( kj based on the entire 9-week trial) by the number of days in the feeding trial (63) to estimate total energy required for maintenance during the trial ( kj). We then adjusted this for digestibility (56.5% digestible ¼ kj of digestible energy). Next, we took the most conservative approach and assumed the feeding trial concluded simultaneously with gestation (195 days), at which time, the total energy content of the gravid uterus is about kj (Robbins and Moen 1975). We subtracted kj from the estimated digestible energy requirement for maintenance throughout the 9-week trial ( kj) and divided the difference by 63 days to make the estimate a daily requirement. Finally, we divided by the average metabolic mass of their deer ( ; Ullrey et al. 1969) and arrived at an adjusted daily digestible energy maintenance estimate of 645 kj/kg body mass Further, we accounted for the 16.4% increase in dam metabolic rate during gestation reported by Pekins et al. (1998), to arrive at a final estimate of 540 kj/kg body mass 0.75 for deer in the Ullrey et al. (1969) trial. Though these calculations may be an oversimplification, there clearly remains a disparity between the Ullrey et al. (1969) estimate adjusted for pregnancy and our minimum estimate of 357 kj/kg body mass We acknowledge that thermoregulation was likely greater for deer in the Ullrey et al. (1969) experiment; however, prior research has focused on the thermoregulatory costs of fasted animals (e.g., Mautz et al. [1992], whose work suggests a 16% increase in metabolism for fasted deer at the temperatures experienced by deer in the Ullrey et al. [1969] study). Because heat produced from digestion, activity, and gestation may offset thermoregulation costs to an unknown amount (Robbins 1993:156), a 16% increase in metabolism due to thermoregulation is probably an overestimate. Hobbs (1989) estimated that thermoregulation was less than 4% of the energy budget of freeranging mule deer (Odocoileus hemionus). Thus, maintenance estimates for deer in the Ullrey et al. (1969) trials ranged from kjkg body mass 0.75 day 1, depending on energy expended for thermoregulation, which is still greater than maintenance requirements estimated for deer in our trial. Published estimates of daily digestible energy required for maintenance of body mass have been used in numerous studies to assess habitat quality and carrying capacity for white-tailed deer (Drake and Palmer 1986, 1991; Gray and Servello 1995; Hellickson and DeYoung 1997; McCall et al. 1997). Our data suggest daily digestible energy requirements for deer in southern environments are lower than those previously reported. Therefore, past research designed to assess habitat quality and carrying capacity in more southern environments that incorporated estimates of daily digestible energy requirements based on feeding trials conducted in northern environments (Hellickson and DeYoung 1997; McCall et al. 1997) may have biased their results; that is, they quite possibly underestimated habitat quality (or carrying capacity) because deer in southern environments seem to require less digestible energy for body mass maintenance than their northern conspecifics. The correlation between voluntary food intake restrictions and seasonal changes in forage quality and quantity represents an assumed adaptation to maximize survival during times of food limitation (Fowler et al. 1967; Ozoga and Verme 1970; Moen 1978). Worden and Pekins (1995) reported voluntary metabolizable energy intake estimates from 720 kjkg 0.75 day 1 in September to 327 kjkg 0.75 day 1 in February for 5 adult, female, pregnant white-tailed deer in New Hampshire. These deer lost body mass when metabolizable energy intake fell below 460 kjkg 0.75 day 1, which equates to 529 kjkg 0.75 day 1 of digestible energy assuming an apparent metabolizable energy coefficient of 0.87 for ruminants on concentrate diets (Robbins 1993). Changes in maintenance requirements may follow ecological gradients as well. Mueller and Diamond (2001) demonstrated that metabolic rates of mammals may be correlated to the net primary productivity of their environment. They conjectured species that evolved with abundant food resources may have a higher metabolism than species from less productive environments. Domestic ruminants indigenous to areas where food quality is poor also have lower nutrient requirements than animals from more productive areas (Kearl 1982). Hudson and Christopherson (1985) reported metabolic rates from northern Cervidae are the highest reported for wild ungulates. In northern environments, food may be seasonally abundant and greater metabolic rates are needed for tissue synthesis during those periods (Hudson and Christopherson 1985). Conversely, deer in southern Texas have evolved in a semiarid environment with variable rainfall patterns that limit net primary productivity; accordingly, lower maintenance requirements may be an adaptive response to a low productivity environment. Hudson and Christopherson (1985) reported the lowest metabolic rates are found in desertadapted species that subsist on low-quality forages. Whitetailed deer in southern Texas may provide an example of decreased daily digestible energy requirements, relative to its northern conspecifics, as an adaptation to the semiarid environment.
5 60 JOURNAL OF MAMMALOGY Vol. 86, No. 1 ACKNOWLEDGMENTS We thank S. W. Stedman, the Neva and Wesley West Foundation, and the Caesar Kleberg Wildlife Research Institute of Texas A&M University Kingsville for financial support of this project. T. Campbell deserves special recognition for providing logistical assistance. We thank J. Feild, J. Young, I. DeLaGarza, and B. Hall for providing assistance and M. Chamberlain, M. Hellickson, T. Fulbright, and L. Shipley for comments on earlier drafts. (This is publication of the Caesar Kleberg Wildlife Research Institute.) LITERATURE CITED AMERICAN SOCIETY OF MAMMALOGISTS Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. Journal of Mammalogy 79: BURNHAM, K. P., AND D. R. ANDERSON Model selection and inference: a practical information-theoretic approach. Springer- Verlag, New York. CAMPBELL, T. A., AND D. G. HEWITT Effect of metabolic acidosis on white-tailed deer antler development. 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