energy costs and intake
Nutritional constraints for free-ranging ungulates typically have been assumed to be energetic ones, largely because of environmental limitations induced by seasonally changing environments. Metabolic rates for the maintenance of body mass by northern ungulates are generally high compared to other ungulates (Hudson & Christopherson 1985; Hudson & Haigh 2002). In the arctic where food is abundant only over a very short season, higher metabolic rates enable tissue synthesis for growth and replenishment of body reserves during the short summer window (e.g., Lawler & White 2003). The lower energy requirements for maintenance by white-tailed deer in southern environments compared to more northern conspecifics serve as an adaptation to semi-arid environments with limited net primary productivity (Strickland et al. 2005). It is unknown whether seasonal cycles in basal metabolism, when corrected for previous intake, occur in all species (Mautz et al. 1992). When they do occur, it is unclear whether they are driven by photoperiod-induced appetite or by requirements for maintenance of different tissues and secretions because appetite and metabolic rate are linked to different hormones as well as influenced by the environment (Hudson & Haigh 2002).
Across species, lactation is the biological state when daily energy costs are highest for females. Energy requirements for female ungulates increase 65–215% during the first month post partum (Oftedal 1985; Robbins 1993). Before lactation, >90% of the energy requirements for gestating females occurs during the last trimester, and these costs are almost 50% higher for pregnant than non-pregnant animals (e.g., Pekins et al. 1998). Hence, highest energy costs for females occur from late winter to mid summer. For male ungulates, mass-specific seasonal energy requirements are typically highest during the autumn breeding period when animals are most active and when foraging is usually reduced, resulting in mass loss (e.g., bighorn sheep: Pelletier 2005; Himalayan tahr (Hemitragus jemlahicus): Forsyth et al. 2005; red deer: Yoccoz et al. 2002; Rangifer: Barboza et al. 2004). The consequences of reproductive effort were reviewed by Mysterud et al. (2004).
Variable and harsh weather augments seasonal energetic costs, with variable impacts depending on age structure of the population (Coulson et al. 2000) and potentially strong cohort effects (Fritz & Loison 2006). A weather-sensitivity hypothesis related to rain, strong wind, and low temperatures explained habitat segregation by male and female red deer (Conradt et al. 2000); the higher weather sensitivity of males due to higher energy losses relative to intake rates and the depletion of body reserves during the breeding season may make males more susceptible to the loss of forest cover. Rainfall during cool summer temperatures increased energy costs for black-tailed deer by 28% after 5 h in the rain (Parker 1989), and winter rainfall was a significant predictor of body condition in white-tailed deer (Garroway & Broders 2005). Although they are typically only small increases in metabolic cost, constant supplemental thermoregulatory expenditures can pose cumulative over-winter energetic drains, compounded with effects on daily foraging behaviours (e.g., feral goats (Capra hircus): Shi et al. 2003; kudus (Tragelaphus strepsiceros): Owen-Smith 2002). Managers have used lower and upper limits of thermoneutrality to define the importance of vegetative cover as thermal cover from heat and cold. Of note, the long-time prescriptions for retaining forested stands as thermal cover from temperature and wind for elk populations are now being revisited in light of the contrasting benefits of solar heat gain by wintering animals in non-cover areas (Cook et al. 1998). Increased energetic demands associated with cold temperatures, wind and deep snow are the long-standing impetus for the management of deer yards as shelter.
In regions with snowfall, snow depths directly influence the choice of traditional wintering areas, where energy costs are usually lower and food availability is higher (e.g., Sabine et al. 2002). Energetic costs of movement increase exponentially depending on sinking depth of the animal, doubling at 60% of brisket height (Hudson & Haigh 2002) and reaching three to eight times the cost of locomotion without snow depending on snow density for both cervids (Parker et al. 1984; Fancy & White 1987) and bovids (Dailey & Hobbs 1989). Snow depth is the primary influence on body condition of wintering white-tailed deer (Garroway & Broders 2005) and plays a significant role in energy balance of Alaskan black-tailed deer (Parker et al. 1999). Delayed snowmelt increases winter mortality of deer and bighorn sheep (Dumont et al. 2000; Jacobson et al. 2004) if body reserves are depleted long before new plant growth resumes. Following winters with deep snows, caribou give birth to smaller calves (Adams 2005). Consequently, the cumulative energetic effects of snow over consecutive winters can negatively influence population demography (e.g., Patterson & Power 2002).
Metabolic demands necessitate dietary consequences. For many ungulates characterized by sexual dimorphism, absolute metabolic costs are higher for larger males and relative (per kg) energy costs differ between sexes depending on season, resulting in intra-specific dietary differences (reviewed by Pérez-Barbería et al. 2008). Barboza & Bowyer (2000, 2001) proposed a gastrocentric hypothesis for cervids that explains seasonal differences in diet selection and habitat segregation among reproductive females, non-reproductive females, and males. Because reproductive females have higher nutritional demands during gestation and lactation, the requirements for higher dietary minima favour segregation from non-reproductive females and males in late winter and summer, but not during autumn. Reproductive females also increase feeding times in both winter and summer compared to non-reproductive animals. Males, with larger ruminal capacity and longer retention of forages, can subsist on the lowest quality diets. This nutritional basis for segregation of the sexes indicates that differences in foraging behaviour may be a consequence of different metabolic demands rather than social constraints or competitive exclusion.
In environments with prominent seasonal changes, food resources are commonly limited during dormant seasons. Dietary quantity and quality are highly variable, with significant declines in digestible nutrients during the winter or dry season. Consequently, highest intakes of digestible nutrients by herbivores occur in summer or rainy seasons. Seasonal patterns of intake generally coincide with seasonal patterns of reproduction and maintenance (Owen-Smith 2002). Ungulates are able to discriminate between feeding patches on the basis of quantity and quality of food, which has major implications for time budgets and nutritional status (Langvatn & Hanley 1993). Metabolic and nutritional requirements may preclude animals from feeding in areas with low forage abundance or low nutritive value (Cook 2002).
The mechanics of how animals forage for nutritional gain over different temporal and spatial scales, and the physiological and physical factors that influence intake rates have been defined by numerous reductionist studies. Across species, maximum short-term intake rates scale with body mass and correspond with scaling of metabolic rates (Shipley et al. 1994). Rates of food intake in relation to food abundance (the functional response of an animal to its nutritional environment) vary directly with bite size and indirectly with fibrousness of the food; they depend further on digestive constraints, gut morphology, and interactions with plant chemistry (Shipley et al. 1999; see also Torregrossa & Dearing 2009). Food availability is the main constraint on daily intake at low food abundance, whereas digestive processing capacity limits intake at high food abundance when food quality is low or metabolic demands are very high (Owen-Smith 2002). At high food abundance and high quality, surplus energy intake beyond immediate metabolic needs may be stored. At intermediate food abundance, animals adjust intakes in relation to nutritional values. Food abundance from the animal's perspective includes only available foods that it will consume, and which subsequently support metabolism, growth, and reproduction.
Ungulates use physiological and behavioural mechanisms to accommodate seasonal variation in both their nutritional requirements and the nutritional value of habitats. Presumably to conserve energy, cervids in north-temperate regions reduce intake rates voluntarily in winter (corresponding with natural declines in food availability), even when provided with ad libitum access to foods (e.g., black-tailed deer: Parker et al. 1993; white-tailed deer: Taillon et al. 2006; elk: Hudson & Haigh 2002; moose: Schwartz & Renecker 1998; Rangifer: Barboza & Parker 2008). Interestingly, white-tailed deer on low-quality diets reduced food intake less than deer on higher quality food, potentially to compensate for the lower nutrient content of the diet (Taillon et al. 2006). Dietary breadth was constrained for white-tailed deer by low forage quality as well as by mobility in snow (Dumont et al. 2005). For black-tailed deer, the processing of lower quality food in coastal environments in winter resulted in more time spent ruminating and fewer foraging bouts; deer did not increase time spent foraging to compensate for decreasing dietary quality, perhaps to avoid the high energy costs of movement in snow (Parker et al. 1999). They also reduced dietary breadth with decreasing nutritional value of available forages. In contrast, during the adverse dry season in tropical savanna, kudus spent more time active and increased both foraging time and dietary breadth to compensate for declines in forage quality (Owen-Smith 1994). Resource heterogeneity, duration of the dormant season, and the rate of decline in forage quality all affect the seasonal cycle of intake (Illius 2006). Because of interactions between the abundance and value of food resources, the quantity, quality and composition of the diet also vary with changes in population density (Nicholson et al. 2006).
Ultimately, nutrient intake, which depends on bite size and the digestible nutrient content of those bites, in relation to nutritional requirements, provides a critical link between food resources and animal performance (Parker et al. 1996). Bite sizes taken during foraging are a small-scale process that can have large consequences. The nutritional influence of numerous bites compounds over a foraging bout, a day, and a season to affect growth, survival, and reproduction (reviewed by Shipley 2007). Even small differences in food value can have large influences on animal performance through multiplier effects (White 1983). More than 75% of diet selection by red deer could be attributed to maximizing energy intake during winter and spring (van Wieren 1996), and daily rates of energy intake explained selection of feeding patches (Wilmshurst & Fryxell 1995). As a consequence of snow in winter and the increased demands of lactation in summer, availability of digestible energy was the greatest nutritional limiting factor for black-tailed deer in Alaska (Parker et al. 1999). Similarly, white-tailed deer in Quebec consistently preferred diets that were highest in digestible energy content in winter (Berteaux et al. 1998), presumably reflecting physiological needs. Energy intake during summer strongly affects body mass gain, including deposition of both body fat and body protein (Allaye Chan-McLeod et al. 1994). Energy balance on a year-round basis is generally more sensitive to variations in energy intake than in energy costs (Fancy 1986; Hobbs 1989), and consequently, intake rates drive what is possible in terms of body mass and condition of the animal. Yet animals probably have less control over maximum energy intake, which is largely dependent on plant growth, than their energy expenditures for activity.
Nutritional constraints for ungulates may be more than just energetic constraints. In addition to short-term elemental or chemical needs that influence movements and distribution of ungulates (Ayotte et al. 2006, 2008), there is increasing evidence that protein constraints may be an important nutritional challenge. Protein requirements are typically highest during body growth, which usually coincides with highest forage protein. Neonatal growth of red deer depends on milk protein, and protein to fat ratios in milk are highly correlated with birth mass (Landete-Castillejos et al. 2001, 2003). Lactating caribou allocate mostly surplus protein not used for the replacement of maternal protein to milk production (Allaye Chan-McLeod et al. 1994, 1999). Male reindeer that lose 23% of body protein during the breeding period and incur potentially more protein losses over winter must rely on spring and summer forage to replenish these protein stores (Barboza et al. 2004). Short-term protein intake rates in summer influence the selection of food patches (Langvatn & Hanley 1993).
Similar to energy demands, high-protein demands also can occur when the nutrient content of food resources is low. Protein requirements increase during foetal growth, particularly in late winter when 80% of foetal mass is deposited (Robbins & Robbins 1979; Robbins 1993) and forage protein is lowest of the year. During lactation, protein requirements may increase 110–130% in Rangifer (Barboza & Parker 2008), with high early-lactation requirements often occurring before the new growth of plants in spring. For reindeer and caribou that consume large quantities of low-protein lichens during a long winter followed by lactation demands, protein balance can be negative for 7 months of the year (Gerhart et al. 1996). Lichens, with their low protein content, are relatively high in digestible energy content, and the ratio of digestible energy to protein is much higher in lichens than in forage species consumed by other cervids during winter (Parker et al. 2005). To minimize excretory nitrogen losses and spare the use of body protein, Rangifer employs mechanisms such as urea recycling and oxidizing nitrogen from dietary protein (Barboza & Parker 2006, 2008). The extent to which protein is a limiting factor (possibly in addition to energy) has not been researched in detail for many northern wintering ungulates. Northern populations of moose consume winter forages that are near the limits of adequate protein content to support maintenance or reproductive requirements (D.E. Spalinger, unpublished; Schwartz & Renecker 1998). There is also some evidence from sapling fertilization experiments suggesting that white-tailed deer discern differences in protein content of individual plants and increase foraging rates on browse species with highest protein content during winter (Tripler et al. 2002).