Functional macronutritional generalism in a large omnivore, the brown bear

Abstract

We combine a recently developed framework for describing dietary generalism with compositional data analysis to examine patterns of omnivory in a large widely distributed mammal. Using the brown bear (Ursus arctos) as a model species, we collected and analyzed data from the literature to estimate the proportions of macronutrients (protein, carbohydrate, and lipid) in the diets of bear populations. Across their range, bears consumed a diversity of foods that resulted in annual population diets that varied in macronutrient proportions, suggesting a wide fundamental macronutrient niche. The variance matrix of pairwise macronutrient log‐ratios indicated that the most variable macronutrient among diets was carbohydrate, while protein and lipid were more proportional or codependent (i.e., relatively more constant log‐ratios). Populations that consumed anthropogenic foods, such agricultural crops and supplementary feed (e.g., corn), had a higher geometric mean proportion of carbohydrate, and lower proportion of protein, in annual diets. Seasonally, mean diets were lower in protein and higher in carbohydrate, during autumn compared to spring. Populations with anthropogenic subsidies, however, had higher mean proportions of carbohydrate and lower protein, across seasons compared to populations with natural diets. Proportions of macronutrients similar to those selected in experiments by captive brown bears, and which optimized primarily fat mass gain, were observed among hyperphagic prehibernation autumn diets. However, the majority of these were from populations consuming anthropogenic foods, while diets of natural populations were more variable and typically higher in protein. Some anthropogenic diets were close to the proportions selected by captive bears during summer. Our results suggest that omnivory in brown bears is a functional adaptation enabling them to occupy a diverse range of habitats and tolerate variation in the nutritional composition and availability of food resources. Furthermore, we show that populations consuming human‐sourced foods have different dietary macronutrient proportions relative to populations with natural diets.

Diet and macronutrient niche of Asiatic black bear (Ursus thibetanus) in two regions of Nepal during summer and autumn

“…We found that the realized macronutrient niches of Asiatic black bear in both Nepalese study areas were similar, despite differences in macronutrient niche breadth, suggesting that they were regulating their diet toward a shared and preferred proportion of dietary macronutrients. The realized niches of Asiatic black bears in our study were similar to those of global brown bear populations during autumn (Coogan, Raubenheimer, Stenhouse et al, ). Likewise, the proportion of macronutrients in the black bear's diets were similar to those self‐selected by captive brown bears, which maintained an average ratio of 17% protein to an 83% mixture of carbohydrates and lipids (i.e., nonprotein macronutrients; Erlenbach et al, )—similarity in macronutrient preferences among species of bears is a possibility, because brown bear, American black bear, and giant panda ( Ailuropoda melanoleuca ) were shown to have similar digestive efficiencies (Pritchard & Robbins, ).…”

“…Both of these crop foods have a high proportion of carbohydrate energy (~82–84°C), which further demonstrates a link between high‐carbohydrate foods and bear‐human conflict (Coogan & Raubenheimer, ), yet in this case for Asiatic black bear. Furthermore, diets of bears in the KSL, which had approximately 1.6 × higher RF% of crop foods in summer compared to the DHR (12.8 RF% in DHR vs. 20.0 RF% in KSL), were also proportionally higher in carbohydrate and lower in protein, which is consistent with a global review of brown bear diets (Coogan, Raubenheimer, Stenhouse et al, ). Anthropogenic crop depredation has been documented throughout the range of Asian black bear (Can, D'Cruze, Garshelis, Beecham, & Macdonald, ; Hwang et al, ; Hyugens, Manen, Marotello, Hayashi, & Ishida, ; Reid et al, ; Sathyakumar & Viswanath, ) and has been linked to natural limitations in the availability of both hard and soft mast (Honda, ).…”

“…Traditionally, the variety (i.e., breadth) of foods consumed by a species has been used to characterize a species niche, including classification as a specialist or generalist (Hutchinson, ; Machovsky‐Capuska, Senior, Simpson, & Raubenheimer, ). Given the influence of nutrients on animal behavior and fitness, nutritional ecologists have recently started examining the nutrient compositions of species’ diets in the context of niche theory (Coogan, Raubenheimer, Stenhouse, Coops, & Nielsen, ; Machovsky‐Capuska, Amiot, Denuncio, Grainger, & Raubenheimer, ; Machovsky‐Capuska, Senior et al, ; Senior, Grueber, Machovsky‐Capuska, Simpson, & Raubenheimer, ). This multidimensional nutritional niche framework characterizes the niche of species across four functional levels: (a) the “food exploitation niche” considers the physical and ecological characteristics of foods consumed; (b) the “food composition niche” describes the variation in nutritional composition of foods consumed; (c) the “realized macronutrient niche” describes the dietary macronutrient composition of a species at some level (e.g., subpopulation, population) that allows it to persist; and (d) the “fundamental macronutrient niche” describes the full range of dietary macronutrient compositions that a species can physiologically persist on.…”

“…The realized macronutrient niches of brown bear populations were shown to vary widely, suggesting a broad fundamental macronutrient niche (Coogan, Raubenheimer, Stenhouse et al, ). Brown bears also experienced variation in dietary macronutrient composition seasonally, due to their reliance on seasonally available foods (Coogan, Raubenheimer, Stenhouse et al, ; Coogan, Raubenheimer, Stenhouse, & Nielsen, ). Under ad libitum experimental conditions, however, brown bears self‐selected a relatively high proportion of nonprotein macronutrients (lipid and carbohydrate) relative to protein across seasons (Erlenbach, Rode, Raubenheimer, & Robbins, ).…”

“…The macronutrient preferences of brown bears likely play a role in food‐related conflict with humans, particularly when natural foods that satisfy their high‐lipid (e.g., hard mast) or high‐carbohydrate (e.g., soft mast) preferences are scarce (Coogan & Raubenheimer, ). In fact, brown bears with diets containing anthropogenic foods were found to have diets proportionally higher in carbohydrate than bears with natural diets (Coogan, Raubenheimer, Stenhouse et al, ).…”