insects."/> Figure 6.2 Homeostatic regulation of dietary balance by insects. (a) Self‐selection of dietary macronutrient ratios by German cockroaches (Blatella germanica). Solid diamonds represent mean + SE intakes during a 48 hours pre‐conditioning period in which the insects were restricted to food with either low, intermediate, or high protein:carbohydrate (P:C) ratio. Hollow circles represent cumulative macronutrient intakes at various intervals when subsequently allowed to self‐compose a diet from all three foods. Data from Raubenheimer and Jones [23]. (b) Benefits of nutrient balancing in female Anchomenus dorsalis beetles. Diets were experimentally manipulated to span a wide range of lipid and protein intakes, and a response surface was constructed relating these intakes to egg production (red = high and blue = low egg production). The negative diagonal is an energy isoline and the grey radials projecting from the origin are nutritional rails representing the experimental diets (as in Fig. 6.1). Egg production showed a distinct peak, varying both with the balance (across nutritional rails) and amounts (along nutritional rails) of protein and lipid eaten. Beetles allowed to compose a diet by combining the two extreme foods (labeled low P/L and high P/L), selected an intake target that corresponded with maximum egg production (the white cross, representing mean + SE intakes of the self‐selecting beetles).
Source: Modified from Jensen et al. [26].
Such studies demonstrate that insects regulate the intake of each macronutrient homeostatically; they have separate appetites for protein and carbohydrate, and these appetites interact during feeding to compose a diet with a specific mix of the nutrients. Several experiments have demonstrated that the mix insects select best meets their nutritional requirement for such functions as growth, reproduction, immunity, etc. – i.e. they self‐select a balanced diet [24–26] (Fig. 6.2b). Within the Nutritional Geometry framework, this selected point is termed an intake target. Other studies have shown that diet selection by insects changes to track specific changes in nutrient requirements. Examples include increased carbohydrate intake following prolonged flight [3], increased fat intake following depletion of energy stores during hibernation [27], and increased protein intake associated with growth and reproduction [26].
The selection of intake targets has been demonstrated in laboratory studies not only for insects but also many vertebrate species [13]. In general, animals compose diets that contain the balance of macronutrients characteristic of the foods they normally eat – carnivores select diets with a high ratio of protein to fats and carbohydrates, omnivores an intermediate ratio, and herbivores the lowest ratio. It might, at first sight, appear unsurprising, even circular, that animals select the diets that they usually eat, but in fact, it is not. Bearing in mind that these experiments are done using synthetic foods – mixtures that the species in question have never encountered in their evolutionary history, and in many cases also their lifetimes – this shows that the proximal driver of diet selection is not the foods themselves, but the nutrients they contain. In effect, it provides a window into how the nutrient‐specific appetite systems are calibrated through evolution to direct animals to eat diets that satisfy their specific nutrient needs.
Natural food environments are not always the idyllic Gardens of Eden they are sometimes assumed to be, but regularly present animals with situations where the relative availability of different foods forces them into imbalanced nutrition. This occurs sufficiently frequently that animals have evolved specific nutritional strategies to deal with such imbalances. An important part of understanding (and for humans, managing) nutrition is learning what these strategies are, a challenge to which the Nutritional Geometry framework is well suited. To do so, experimental animals are confined to diets that systematically differ from the balanced target diet, placing them in a predicament where they cannot attain their target intake of all nutrients but are forced to under eat some and/or over‐eat others (Fig. 6.1b and c). The relative priority the animal assigns to achieving its target intake for each nutrient – i.e. avoiding excesses and deficits – is determined by measuring the ad‐libitum intakes of the experimental groups assigned to each of the foods. Such data provide a measure of the relative strength of the appetites for each nutrient – the stronger the appetite, the closer the intake of that nutrient will be to its target coordinate, with the inevitable consequence of forcing deficits or excesses of other nutrients [3].
Several laboratory studies have examined this issue for a range of invertebrate and vertebrate species [13]. In general, the pattern of response to constrained macronutrient imbalance varies with the normal diets of species. Herbivores and omnivores tend to maintain protein at or close to the target levels, allowing fat and carbohydrate to vary more widely, a response termed “protein prioritization” (Fig. 6.1c). Carnivores tend to do the opposite, where protein intake varies more with dietary macronutrient balance.
Animals in natural food environments
Experiments such as those described above are a means to examine the nutrient regulatory responses of animals to simulated variation in highly simplified experimental environments, but they do not tell us whether and how these responses operate in the realistic setting of natural food environments. In recent years, several studies have examined this issue through recording the dietary intakes of individual animals in unmanipulated or minimally manipulated natural environments. Much of this work has concerned primates because they readily habituate to the presence of human observers, enabling detailed observation over entire days or even multiple consecutive days. The focus on primates is beneficial from our perspective because it helps to place the human nutritional research discussed below into a broader biological context.
It is now clear that animals in the wild, as in the laboratory, employ nutrient‐specific appetites to compose diets with specific amounts and ratios of macronutrients. Felton et al. [28] found that spider monkeys in Bolivia have a strong preference for Ficus boliviana figs, and when these are not available, eat other food combinations to form a diet with a protein‐energy ratio very similar to that of the figs. Mountain gorillas in Bwindi and Virunga compose nutritionally similar diets from very different food combinations [29,30]. Johnson et al. [31] found that a baboon studied for 30 consecutive days composed daily diets with similar percentage energy from protein, even though she ate very different food combinations on different days. Other studies have demonstrated that wild primates change the selected diet to track specific changes in nutrient requirements. Guo et al. [32] showed that the intake of fat and carbohydrate by golden snub‐nosed monkeys living in a highly seasonal environment increased during the cold winters by an amount that closely matched the increased energy requirements for maintaining body temperature in the cold, whereas protein intake did not change. Cui et al. [33] found that rhesus macaques increased their energy intake by ~30% when lactating, but in this case, there was no difference in the ratio of macronutrients selected.
Several studies have examined the regulatory responses of wild primates when natural variation in food availability constrains them from achieving their macronutrient target. A variety of responses has been recorded for different species. Spider monkeys [34] (Fig. 6.3), chimpanzees [35], and blue monkeys [36] show protein prioritization, where protein intake is maintained at or close to the target level while fat and carbohydrate intake vary with the percentage of energy contributed by protein in the diet (Fig. 6.1c). Mountain gorillas show the opposite response, in which they over‐eat protein to maintain a constant intake of non‐protein energy [37]. Rhesus macaques show an intermediate strategy, in which the deficit of one nutrient matches the
