The figures at left illustrate an interesting phenomenon. Even when bears eat a diet increasingly rich in calories, overall intake of energy, standardized to body mass, doesn't correspondingly increase, especially once a treshold of 1 kcal of digestible energy per gram of fresh food is reached. This is most clearly illustrated in figure B; figure A shows the same trend standardized to body mass as percent of total mass.
Just to be clear, larger bears can and do ingest more absolute amounts of digestible energy during a given day, even as the digestible energy in the food they eat increases from 1 to 2 and even 4 kcal per gram. The point is that the energy per kg of mass doesn't increase and, as a percentage of total mass, even decreases, which pertains to efficiencies as much as anything else.
To put this another way, a diet richer per gram in digestible energy--as would be the case with a diet rich in fat or protein--doesn't necessarily translate into a lot more digested energy for any kg of mass that a bear might be carting around. Related back to digestion, this pattern fits the much lower rates of transit and accompanying higher rates of digestion for ingested food that have been documented among bears fed a diet of meat.
So where does accretion (or loss) of body mass occur when diet protein changes? In body fat or lean body mass? Of relevance to these questions, the two figures at right show differences in allocation of gain (or loss) for diets of two different protein contents: a berry diet comprised of 1.6-3.5% protein in A, and a mixed diet comprised of 15.4% protein in B. The red dots and associated trend line show changes in lean body mass (LBM) for each diet; the orange dots and associated trend line, changes in body fat.
The patterns? All of the gain in body mass at a very low diet protein is as fat (A), whereas the majority of gain at moderate diet protein is in lean body mass (B). Moreover, bears eating a very-low-protein diet consistently lose lean body mass; an untenable situation. An important note: These patterns are as much a reflection of the fact that a vegetal diet low in protein (as in A) is necessarily rich in carboydrates, whether glucose, sucrose, or starch (see Digestion). So the patterns in these figures reflect not only protein metabolism but also metabolic processes associated with varying concentrations of digestible carbohydrates, especially related to lipogenesis and protein biosynthesis.
The implication? If a bear, eat a diet rich in carbohydrates and get fat while potentially losing lean body mass. Admix some amount of protein in the diet and you will maintain if not gain lean body mass. So a carb-rich diet with enough protein to maintain LBM makes more sense for a female needing to put on fat to reproduce; protein more sense for a male needing to grow physically large; which fits patterns of dimorphism among bears.
So at this point it is worth looking at what happens (unlike above) when the amount of dry matter ingested and digested by bears varies, adding variation in diet protein content. And, of course, the complement to variation in diet protein is complementary variation in diet fat or carbohydrates.
The two figures at left summarize the results of several studies done in Charlie Robbins' lab, unified by a design that allowed bears to eat different amounts of digestable dry matter (the horizontal or x axis) while measuring responses in terms of change in body mass--i.e., growth (the vertical or y axis). All of this standardized to the metabolism-corrected mass of the involved bear, and considering diets with different amounts of protein, ranging from berries (3-4%) to deer and salmon (nearer 70% or more). In addition to the data points and curves describing the response in mass gain to variation in dry matter intake I've also benchmarked where each curve transitions from mass loss to mass gain (the vertical gray line).
Protein & Energy Effects
Nutrition obviously entails more than just the digestibilities of different foods. The absolute and relative amounts of various macronutrients (e.g., proteins, lipids, and carbohydrates) are critical elements of nutrition, as are the absolute and relative amounts of digestible energy. Even though all of these additional nutrient-related aspects of nutrition are correlated with the digestion of various foods in the gut, there are additional consequences that play out through metabolic processes involved in the creation and use of body protein, fat, and glucose--i.e., protein biosynthesis and protealysis, lipogenesis and lipolysis, and gluconeogenesis and glycolysis. Moreover, the density of digestible energy in foods matters for reasons that transcend simple nutrient composition. Resting metabolism varies widely in close syncrony with nutrient-specific processes and related energy expenditure--with consequences for levels of heat production in the body (i.e., thermogenesis).
The net result of all of this is not only variation in the efficiencies of energy, protein, lipid, and glucose metabolisms, but also variation in the composition, efficiency, and total level of body mass accretion...or loss. Different combinations of relative and absolute amounts of protein, fat, carbohydrates, and digestible energy in the diet can determine whether an animal gains or loses body mass, and whether that mass gain or loss is comprised of lean body mass or fat reserves.
With respect to bears, then, this amounts to a lot of complexity when it comes to understanding the ramifications of different diets. Having made this point, Dr. Charles Robbins and his graduate students have taken us well on our way to understanding these complexities. What follows draws almost wholly on the research that has come out of Dr. Robbin's lab using captive black and grizzly bears housed at Washington State University. Geof Pritchard, Sean Farley, Grant Hilderbrand, Christy Welch, Karyn Rode, Laura Felicetti, and Joy Erlenbach have all contributed substantially to our understanding of bear nutrition as a result of their investigations as graduate students under Charlie's tutelage.
Efficiencies, protein, & growth
Given that a bear is eating a diet containing ample digestible energy (say 800 kcal per kg raised to the 0.75 power per day): It turns out that there can be both too little and too much protein when it comes to efficiencies of gain in body mass. The figures to the left are relevant to this point, adapted from those in a paper on which Joy Erlenbach was lead author; a paper in which she sythesized a lot of research specific to bear nutrition. Each figure features a bunch of dots of two different colors corresponding to the metabolic and accretional consequences for bears fed diets comprised of different macronutrients, including diets rich in protein or carbohydrates (salmon colored) as well as diets rich in protein or fat (burgundy).
The main points? The top figure (A) shows that the efficiency of weight gain rises rapidly to a peak as diet protein increases from roughly 1% to 15% and then gradually declines, all of this with the density of diet energy remaining roughly the same. Correspondingly, the middle figure (B) illustrates a decline in resting metabolism (i.e., energetic costs of maintaining the body) as diet protein increases from 1% to roughly 30%, after which maintenance costs increase. When you put these two trends together you get the bottom figure (C) which shows the predicted total rate of gain per kg of body mass, standardized to the expected basal metabolic rate for carnivores (i.e., raised to the 0.75 power); a rapid rise as diet protein increases, followed by a steady decline.
It turns out that the predicted level of diet protein at which rates of gain in body mass peaks (roughly 21%) corresponds almost exactly with the mean diet protein content of diets selected by bears when given a free choice of what to eat (22% plus or minus 6%)--shown by the large burgundy dot and horizontal error bars in figure C.
From this a person could conclude that the optimal protein content of a bear's aggregate diet is around 22%, at least as far as growth of body mass is concerned--and without considering whether that growth is primarily in terms of lean body mass or fat. But with some important provisos. This rule of thumb for diet protein holds for a given energy concentration in the diet (in this case, around 800 kcal/kg 0.75/day) and for bears of intermediate body size. As shown on the page devoted to body mass effects, size of bear affects nutrition in several ways, as does energy concentration of the diet (see below). Again, this hearkens to the theme of complexity.
The obvious question arises; Why a diet protein content of around 20% yields greater growth rates than, say, 60%--standardized, of course, to a given volumetric intake and to the metabolic rate expected at a given body mass? As a start, all else equal, elevated diet protein causes greater heat production in the body compared to elevated carbohydrates or fats. This thermic effect is called diet-induced thermogenesis (DIT). Much of this elevation in metabolic rate (as shown in figure B, above) is attributable to the thermic properties of protein synthesis, including increased heat production and reduced energetic efficiency. Depending on total diet composition, some of the increased heat production associated with a high-protein-content diet can be attributable to heightened formation of glucose (gluconeogenesis) above and beyond what would occur with a high-carb diet.
So...how about the effects of too little protein? Generally speaking, if a bear's diet is deficient in protein, he or she compensates by increasing the volume of intake, usually of foods rich in carbodydrates (think berries and roots; see Digestion). But the results above pertain to an isocaloric intake (that is, a constant or equal intake of calories), which means that diet composition, not amount of energy intake, is implicated. As figure B above shows, the metabolic rate of bears fed a low-protein diet increases substantially, which, because of the resulting increased energy expenditure, leads to decreased absolute and relative rates of gain in body mass. Why? Well, ultimately, because an increased proportionate consumption of fats or carbohydrates when bears are fed a diet low in protein leads to a chain of energy consumptive phenomena. The sympathetic nervous system is stimulated, which increases production of the hormone norepinephrine, which stimulates brown adipose tissue metabolism, which results in an elevated metabolic rate. Whew. But, in the end, more energy expenditure and less weight gain.
Intake, protein, & growth
The basic patterns are pretty obvious. In all instances weight gain tends to plateau (i.e., tends towards an asymptote) as intake increases. At some point, increased intake does not yield increased mass gain; the bears reach the limits imposed by internal metabolic processes. But this plateau is considerably higher (45-60 g per kg raised to 0.75 per day) for meat diets (B) compared to vegetal diets (nearer 20 g; A). Even so, the transition from weight loss to weight gain is similar (around 20-40 standardized ingested grams) for meat diets and vegetal diets having at least 12-18% protein content, the latter of which is within the lower range of optimal (see above). The biggest deviant is the low-protein-content diet comprised of berries. Weight gain only occurs when the standardized volumetric intake is high--in excess of 80 g, which is roughly 2-4 times higher than for other diets.
The implications? Even given the standardized metabolic inefficiences associated with a protein-rich diet shown in the graph at the top of this page, bears can grow much more rapidly on such a diet, especially if they have access to large volumes. The most notable example of this circumstance would be along salmon spawning streams during the height of spawning runs; hence very large coastal brown bears (see here for details). By contrast, bears with access primarily to berries have to eat relatively large volumes to gain mass and, even so, the potential for growth is relatively limited. Think bears in the interior regions of British Columbia, northeast Washington, northern Idaho, and northwest Montana (for dietary details follow this link). One important proviso to all of this is that there is no distinction made regarding the tissues in which weight gain occurs, principally whether in fat or lean body mass. Which brings me to the next topic...
Intake, protein, energy, & composition of growth
So now bring diet energy , as such, into the picture, and slightly recast the dynamics of total intake per day, at least for protein. The graph at left above shows the relation between standardized accretion of body fat and standardized ingestion of energy--regardless of the contributing macronutrient; and this for various diets comprised of very low (1.6-3.5%, the pink dots) and closer to optimum (15.4%, the red dots) concentrations of protein. In short, as intake of energy increases, so does accumulation of body fat. But more importantly, bears tend to gain more body fat (as above) on diets low in protein content, which is tantamount to saying on diets rich in either carbohydrates or fats. In fact, high-fat diets contain the highest concentrations of digestible energy, which translates into high rates of body fat gain.
The graph at upper right complements the graph immediately left by showing rates of lean body mass gain related to the total intake of digestible protein--with both values standardized. Not surprisingly, the more protein that a bear ingests and digests, the more lean body mass it accretes, with highest rates of both associated with diets containing a higher concentration of protein. And, as in the figures next above, protein intake on diets very low in protein content (1.6-3.5%, e.g., berries) does not allow even for maintenance of LBM. By contrast, the rate of LBM gain is remarkably high (8-9 grams per kg of body mass raised to the 0.75 power) at the highest rates of protein intake (around 6 grams per kg of body mass). In other words, in excess of a 1:1 translation.
I conclude this page with a few points that are either not adequately encompassed by the data presented above or that simply need additional clarification, and then end by quoting an elegant synopsis of nutritional fundamentals for bears that was included by Joy Erlenbach in her 2014 paper.
First, diets comprised solely of fruit are a potential problem for bears, especially if the involved bear is large in size. The low protein content and high glucose or fructose content of fruit diets require bears to eat exceptionally large volumes just to maintain LBM, but with resultingly high rates of energy intake. This energy either needs to be dissipated as heat (diet-induced thermogenesis) or converted to body fat through lipgenesis, which is notably elevated on diets rich in fructose--one of the main sugars in blue- and blackberries. Large bears are notably much less efficient than small bears at harvesting any given concentration of fruit, which means that mass standardized consumption of fruit is maximized for large bears at rates far less than what they need to meet protein and even energy requirements. Hence, fruit-eating is more often a strategy of smaller bears or bear species (e.g., juveniles, females, and black bears) than it is of those that are larger (e.g., adult males and grizzly bears; for more on the implications of size see the pages Foraging efficiency and Body mass effects).
Second, bears prefer fat-rich foods and diets. In instances where captive bears had free access to diets of different composition they ended up eating diets from which they obtained roughly 68% of metabolisable energy from fats. Fats provide the highest concentrations of digestible energy of all macronutrients and are, in turn, the most efficiently converted of any to body fat. And ample body fat, to the point of obsesity, is a center-piece of the bear life strategy. Moreover, unlike diets rich in protein or carbodyrates, diets rich in fat do not trigger autoregulatory reductions in intake, which also contributes to high rates of body fat accumulation on high-fat diets. Or, put another way, diets comprised mostly of protein or carbodydrates are not optimal for most bears.
Third, and related to the points immediately above, bears are energy maximizers. In fact, as noted by Joy Erlenbach, bears exhibit some of the highest levels of standardized energy intake observed for any mammal. When offered unlimited access to food these rates can be twice what some early researchers such as James Kirkwood considered to be the maximum rate likely or possible and up to 18 times greater than the expected basal metabolic rate for carnviores. Which is a lot of energy.
So...in conclusion, I quote Joy Erlenbach, who suggested that bears live by three "rules" when it comes to intake of energy and nutrients, to whit:
(1) Maximize energy intake while optimizing dietary protein intake.
(2) Select lipids over digestible carbohydrates, which reduces dietary protein while maximizing food energy density.
(3) If lipids are not available, use digestible carbohydrates to optimize diet protein through diet balancing.