Temporal responses in energy expenditure and respiratory quotient ...

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Temporal responses in energy expenditure and respiratory quotient following feeding in the muskox: influence of season on energy costs of eating and standing and an endogenous heat increment James P. Lawler and Robert G. White

Abstract: Seasonal energy metabolism was investigated in young (2- to 3-year-old) muskoxen (Ovibos moschatus) during the winters of 1994 (January–April) and 1996 (January) and summer of 1995 (July and August). Energy expenditure (EE) increased 35%–42% following a meal of chopped brome hay (Bromus inermis) and declined as a doubleexponential process over 8 h. The mean energy cost of eating (321 and 361 J·g dry matter–1) was lower in winter than in summer, and declined with body mass (BM) (r2 = 0.58). The mean energy cost of standing was 21% (SE = 2.7%) higher than that of bedding. Prefeeding energy expenditure (EEp) was 26% higher in summer than in winter. An endogenous heat increment, measured as EEp – EE, at 7–8 h post feeding was lower (P < 0.001) in winter than in summer (39 and 58 kJ·kg BM–0.75·d–1, respectively). Mean cumulative EE (minus activity costs) for 8 h post feeding was 124 (SE = 4) and 148 (SE = 4) kJ·kg BM–0.75 (P < 0.001) in winter and summer, respectively. Respiratory quotients (RQs) >1 were recorded during feeding in winter and a mean RQ of 0.9 was recorded in summer. Seasonal EEp, postfeeding EE, and RQ are consistent with a low cost of maintenance metabolism in winter and an increased requirement for productivity in summer. Résumé : Nous avons étudié le métabolisme énergétique saisonnier chez de jeunes (2–3 ans) boeufs musqués (Ovibos moschatus) durant les hivers 1994 (janvier–avril) et 1996 (janvier) et durant l’été 1995 (juillet et août). La dépense d’énergie (EE) augmente de 35 % à 42 % après un repas de brome inerme (Bromus inermis) haché et elle décroît selon un processus exponentiel double sur une période de 8 h. Le coût énergétique moyen de l’alimentation (321 et 361 J·(g DM)–1) est plus faible en hiver qu’en été et décroît avec la masse du corps (BM) (r2 = 0,58). Le coût énergétique de la station debout est de 21 % (erreur type = 2,7) plus élevée que celui de la station couchée. L’EE avant l’alimentation (EEp) est de 26 % plus élevé en été qu’en hiver. L’accroissement endogène de chaleur, mesuré par EEp – EE, 7–8 h après l’alimentation, est plus faible (P < 0,001) en hiver qu’en été, (39 et 58 kJ·kg BM–0,75·d–1, respectivement). L’EE cumulé (moins les coûts de l’activité) pour les 8 h suivant l’alimentation est de 124 (erreur type = 4) et de 148 (erreur type = 4) kJ·kg BM–0,75 (P < 0,001) respectivement en hiver et en été. Un quotient respiratoire (RQ) >1 s’observe durant l’alimentation en hiver et un quotient moyen de 0,9 en été. Ces EEp saisonniers, les EE après l’alimentation et les RQs sont en accord avec des coûts du métabolisme de maintien faibles en hiver et de besoins accrus pour la productivité en été. [Traduit par la Rédaction]

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Introduction Measurements of the energy costs of eating and foraging in relation to energy intake are used to make factorial estimates of the energy costs incurred by the foraging animal and to test ecological and evolutionary strategies of wild ruReceived 14 January 2003. Accepted 7 July 2003. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 26 September 2003. J.P. Lawler,1,2 and R.G. White. Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK 99775, U.S.A. 1 2

Corresponding author (e-mail: [email protected]). Present address: U.S. National Park Service, 201 1st Avenue, Fairbanks, AK 99701, U.S.A.

Can. J. Zool. 81: 1524–1538 (2003)

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minants (Gessaman 1973; Osuji 1974; Boertje 1985; Russell et al. 1983; Moen et al. 1997; Parker et al. 1996; Delgiudice et al. 2001). Heat loss measured by gas exchange can be used to determine the energy costs of eating (Armstrong et al. 1957; Blaxter and Joyce 1963; Young and Webster 1963; Christopherson and Webster 1972) and the heat increment of a meal (Brody 1964). Estimates of the efficiency of processing meals are useful for making comparisons between species and types of food, as well as comparisons within species, such as those species that exhibit sexual dimorphism (Bowyer 1984; Bleich et al. 1997; Kie and Bowyer 1999). Few estimates of the energy costs of eating exist for wildlife species, yet eating costs may constitute a substantial component of the energy budget (Wickstrom et al. 1984; Fancy and White 1985). There is a dearth of information on the pattern of energy expenditure by wild ruminants during

doi: 10.1139/Z03-133

© 2003 NRC Canada


Lawler and White

the entire eating and heat-increment period between meals. Therefore, a full description of temporal trends is not available for interpreting metabolic events that occur during and following feeding in ruminants. For ruminants, the period that food is withheld before a meal influences metabolic determinations because an endogenous heat increment accompanies the utilization of mobilized body tissues (Marston 1948; Chowdhury and Ørskov 1997). If the endogenous heat increment constitutes a significant energy loss, that value should be detectable with standard measurements of energy expenditure. We hypothesized that the first energy released from a meal should substitute for the endogenous heat increment, and at some point following feeding (before the animal begins to mobilize body tissue), observed energy expenditure should decline below that of a fasted animal. Activity of animals can have a substantial influence on short-term measurements of energy expenditure (Parker et al. 1984; Fancy and White 1985). Activity can mask metabolic rhythms that are important for understanding temporal patterns of food processing (White 1993). Hence, making measurements only when the animal is lying (Regelin et al. 1985; Schwartz et al. 1987; Mautz et al. 1992; Jensen et al. 1999) or standing quietly (Blaxter and Joyce 1963; Young and Webster 1963; Christopherson and Webster 1972; White and Yousef 1978) minimizes the influence of activity costs. Both methodologies, however, have limited applicability when the study period is >1–2 h. We investigated the possibility of mathematically subtracting, or “stripping”, the energy cost of standing plus associated activities from the temporal pattern of energy expenditure to reveal the pattern of “resting” energy expenditure. North-temperate-zone ungulates match seasonal differences in voluntary food intake to energy requirements (Rhind et al. 2002). We hypothesize that temporal patterns of energy expenditure following feeding should match energy requirements on a seasonal basis. The muskox (Ovibos moschatus) is an arctic ungulate well adapted to environmental (Scholander et al. 1950a) and nutritional extremes (Holleman et al. 1984; White et al. 1984a, 1984b; Adamczewski et al. 1994b; Nilssen et al. 1994; Lawler and White 1997), and is an excellent model species for examining seasonal aspects of energy metabolism. The objective of this study was to determine seasonal differences in the pattern of gas exchange associated with ingestion of a meal over a time period sufficient to capture postfeeding heat production. From this temporal pattern, we determined the energy costs of eating, and searched for evidence of an endogenous heat increment based on whether postfeeding energy expenditure declined below the prefeeding level. We determined the energy cost of standing and developed a technique for correcting energy expenditure for the cost of standing and activity that occurred during long-term metabolic studies.

Methods Approach All trials were conducted at the Robert G. White Large Animal Research Station of the Institute of Arctic Biology at the University of Alaska Fairbanks, Fairbanks, Alaska,

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U.S.A. (64°50′N, 147°43′W). Muskoxen were taken from pasture, weighed to the nearest 0.2 kg, and fed a standardized meal of 50% brome hay (Bromus inermis) and 50% Quality Texture Ration (Alaska Mill and Feed, Anchorage, Alaska, U.S.A.) at 10 g dry matter (DM)·kg body mass (BM)–0.75. Animals were then held without food for 24–26 h before being weighed and placed in a metabolism chamber. Data collection commenced approximately 0.5 h later, once gases within the chamber had equilibrated. Consumption of O2 and production of CO2 and CH4 were determined at 2-min intervals for the next 10 h. All metabolic trials were started at approximately the same time of day (between 1300 and 1600). Animal activity was monitored remotely with a video camera placed within the chamber. Animals had free access to water in summer and snow in winter while in the chamber. During the first 2 h of the metabolic trial, muskoxen were offered no food in order to determine baseline values of energy expenditure. At 2 h, the experimental meal of chopped brome hay (10 g DM·kg BM–0.75) was made available by opening the lid of a feed bin built into the chamber. Gas exchange and activity were monitored for the next 8 h. Feed composition DM content of hay was determined by drying at 60 °C for 48 h. Neutral detergent fiber, acid detergent fiber, and aciddetergent lignin were determined sequentially, and hemicellulose and cellulose were calculated by subtraction (Goering and Van Soest 1970). Total nitrogen and carbon contents were determined by combustion in a nitrogenanalyzer system (CNS-2000 elemental analyzer, LECO, St. Joseph, Mich.). We used a bomb calorimeter to determine gross energy content (1108 O2 combustion bomb, Parr, Moline, Ill.). Metabolic trials and study animals During winter 1994, three 3-year-old muskoxen (2 males and 1 female) were used in 54 metabolic trials as part of a related study. Each animal was evaluated on a 100% hay diet on 2 occasions randomly distributed within the 54 metabolic trials. During summer 1995 and winter 1996 a second cohort of eight muskoxen, six 2-year-olds and two 3-year-olds were used. Five were males, including one 3-year-old, and three were females, including one 3-year-old. Twenty-eight metabolic trials were conducted in summer 1995; the eight study animals were evaluated on the hay diet on one occasion. In winter 1996, 16 trials were conducted and seven of the eight animals were evaluated on hay. The 8th trial on hay during the winter of 1996 was rejected because the animal did not remain calm in the chamber. All muskoxen used during the metabolic studies were sexually intact. All females were nonpregnant and nonlactating. When muskoxen were not being used in trials, they were maintained in pastures dominated by smooth brome grass. Muskoxen had ad libitum access to brome hay during all seasons. Animals were weighed 1–2 times weekly when not in trials. All animals involved in this study had been habituated to confinement in the metabolic chamber as young animals. Only trials during which animals remained calm and unagitated throughout the 10-h period were used for analyses. The University of Alaska Fairbanks Institutional Animal © 2003 NRC Canada



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Care and Use Committee approved protocols for this experiment and the care of these animals and protocols were in keeping with methods approved by the American Society of Mammalogists (Animal Care and Use Committee 1998) for research on captive mammals. Measurement of gas exchange The metabolism chamber measured 2.1 m × 2.1 m × 1.5 m (6450 L). A fan within the chamber kept the air continually mixed. Outdoor air was drawn through the chamber by a rheostatically controlled vacuum motor (model M-1, National Super Service Company, Toledo, Ohio). The rate of airflow was calculated a priori to realize a chamber CO2 concentration of 1.0 occurred in winter but not in summer on this hay diet. A combination of rapid rumen fermentation and low pH could not account for the seasonal difference, as a greater increase in CO2 and RQ would be expected in summer than in winter. We propose, therefore, that the high postfeeding RQ in winter could represent short-term synthesis of fat from volatile fatty acids (Kleiber 1975). Given the higher peak in EE following a feeding event in summer than in winter, a lower RQ in summer may indicate an increase in gluconeogenesis from ruminal propionic acid in an animal primed for hair synthesis and body growth. That outcome is consistent with a summer increase in BM, the higher demands made on glucose, and therefore on ruminal propionic acid, for bodytissue deposition (growth) and hair/wool synthesis in ruminants (White and Leng 1980; Preston and Leng 1987), overall higher metabolic rates (Nilssen et al. 1994; Lawler and White 1997), and faster liquid-passage rates (Holleman et al. 1984; Adamczewski et al. 1994a) in summer than in winter. Temporal responses following feeding and the cumulative EEs presented in this study are applicable to models simulating the effects of an altered number of daily feeding events. Because forage quality and meal size affect rumination requirements, rumination may have a controlling influence over the lying period in muskoxen (Forchhammer 1995). Rumination bouts are fewer in winter (2·h–1) than in summer (5–6·h–1). Our results suggest a faster rate of food processing in summer than in winter, indicating that activity patterns in the wild reflect an endogenous seasonal rhythm as well as seasonal differences in food quality and availability. Theoretical projections of intake per event calculated from data of Forchhammer and Boomsma (1995) suggest that the value we used, 10 g·kg BM–0.75, may be at the lower level of meal

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size for grazing muskoxen, but is equivalent to the average meal size of pen-fed muskoxen (calculated from White et al. 1984). Conversely, because of rapid eating rates (approximately 30 g·min–1; Table 3), the time taken to eat chopped hay ration (30–35 min) is short compared with average grazing periods observed in wild muskoxen (60–80 min; Forchhammer 1995). In conclusion, the determination of EE following the consumption of a standardized meal indicated that the eating cost for muskoxen is similar to that for typical grazers, and that the cost is highly related to BM. Over 8 h and following 24 h without food, the temporal pattern of EE showed a consistent rhythmicity consisting of bursts of EE superimposed on a double-exponential decline from a peak at 30 min post feeding in summer and a secondary peak at 150 min in winter. Digestion processes and the resultant metabolism of nutrients were prompt in summer and more sustained in winter. RQs during feeding and the next 30 min in summer were consistent with a hypothesized short-term conversion of propionic acid to glucose to support protein accretion. In contrast, the high postfeeding RQ in winter could be indicative of a short-term conversion of volatile fatty acids to lipids. We obtained evidence for an endogenous heat increment after 24 h post feeding, possibly because of high metabolic costs of visceral organs, protein turnover, or mobilization of protein for gluconeogenesis. The endogenous heat increment was lower in winter than in summer, which could reflect the considerably higher demands for glucose in summer than in winter. The consistent seasonal differences in the temporal pattern and magnitude of EE following eating, when the food type, quality, and intake were standardized, support the hypothesis that seasonal metabolic adjustments made by muskoxen have an endogenous basis. The results do not necessarily conflict with the hypothesis that wellinsulated animals do not adjust their basal metabolism seasonally (sensu Scholander et al. 1950b) because this hypothesis does not address the phenomenon of an endogenous heat increment, which could change seasonally, owing to efficiency in the use of lipid and protein mobilized to meet the requirements of postprandial resting metabolism.

Acknowledgments Funding and support for this project came from the 1995 Student Research Grant from the Center for Global Change and Arctic System Research, University of Alaska Fairbanks, the Center for Field Research, and Earthwatch, which funded an Earthwatch Project at the Robert G. White Large Animal Research Station (LARS), and the Institute of Arctic Biology. This project contributed to National Science Foundation, Office of Polar Programs, Grant No. 233064, Sustainability of Arctic Communities, through support for R.G.W., and J.P.L. was supported as a Teaching Assistant through the Department of Biology and Wildlife, University of Alaska Fairbanks. We thank Drs. R. Terry Bowyer, Perry Barboza, and Bret Luick for critical review of the manuscript. Expert handling of muskoxen was provided by Bill Hauer, Karen Higgs, Tom DeRuyter, Valerie Blaxter, Suzie Pence, and the rest of the LARS staff. Rich Kedrowski provided expert laboratory assistance. © 2003 NRC Canada



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