Ingestion of plant secondary metabolites (PSMs) presents a physiological and behavioral challenge for mammalian herbivores. Herbivores must not only detoxify PSMs, but they may also deal with energetic constraints such as reduced food intake, mass loss, increased excretion of energy, and increased metabolic demands. We hypothesized that the energetic consequences of consuming PSMs will significantly compromise apparent metabolizable energy intake (AMEI) and energy expenditure in mammalian herbivores. Furthermore, we hypothesized that foraging strategy would influence the degree to which plant consumption impacts energy budgets, such that dietary specialists would be less impacted than generalists when both are consuming the plant species preferred by the specialist. Hypotheses were tested by comparing AMEI and energy expended on basal metabolic rate (BMR) and locomotion in a juniper specialist (Neotoma stephensi) and generalist (N. albigula) woodrat fed control diet and diet containing juniper foliage (Juniperus monosperma). In general, the intake of PSMs in juniper increased the energy excreted in urine and feces in both specialist and generalist woodrats. Specialist woodrats minimized the costs associated with the intake of juniper by ingesting more juniper diet, thereby increasing energy intake, and reducing energy expended on BMR and locomotor activity. Generalist woodrats also decreased locomotor activity on a juniper diet but did not increase intake and maintained BMR. In turn, specialist woodrats had twice as much energy available for activities such as reproduction when consuming a juniper diet than generalists. These results suggest that the intake of PSMs impinges on AMEI and compromises energy expenditure, but that the impact of PSMs on energy budgets is relative to ecological experience with PSMs. Moreover, compensatory feeding, metabolic depression, and low activity may be strategies employed by specialist woodrats that can mitigate the cost of processing PSMs, but these strategies may be constrained in generalist woodrats.

Theory predicts that dietary specialization is limited in part because of physiological trade‐offs associated with specialization. Specifically, dietary specialists are predicted to evolve mechanisms that reduce costs and enhance excretion of plant secondary metabolites (PSMs) that they frequently consume, but are less energetically and/or mechanistically efficient at eliminating novel PSMs. Although examples of trade‐offs associated with dietary specialization have been documented among insects, trade‐offs have not been investigated in mammalian herbivores. To initially investigate the physiological trade‐offs associated with specialization in mammalian herbivores, we determined the impact of ingesting novel PSMs on the energy budgets of a juniper specialist (Neotoma stephensi) and generalist (N. albigula) woodrat. These results were then compared to the impact of juniper intake, the plant species preferred by the specialist, on energy budgets in these same species. Energy budgets were evaluated by measuring apparent metabolizable energy intake (AMEI, energy consumed − energy excreted) and energy expended on basal metabolic rate (BMR) and voluntary wheel running in specialist and generalist woodrats fed a formulated diet with and without PSMs from the novel plant creosote (Larrea tridentata). Both specialists and generalists were energetically impacted by the intake of a diet containing novel PSMs, primarily through decreased intake of creosote diet and increased excretion of energy in the urine. However, specialists were impacted to a greater extent than generalists. Specialists decreased body mass, whereas generalists maintained body mass. Specialists also reduced intake and AMEI when consuming creosote diet compared to control to a greater extent than generalists. In turn, specialists had one‐sixth the energy available for energy dependent activities than generalists on a diet containing novel PSMs. These results are in stark contrast to the comparisons between specialists and generalists consuming PSMs from their natural diet. Specialists consumed more juniper, had higher AMEI and available energy than generalists when fed diets containing juniper foliage. These data provide the first support that physiological trade‐offs associated with dietary specialization may exist in mammalian herbivores.

The whitethroat woodrat (Neotoma albigula) eats juniper (Juniperus monosperma), but the amount of juniper in its diet varies seasonally. We tested whether changes in juniper consumption are due to changes in ambient temperature and what the physiological consequences of consuming plant secondary compounds (PSCs) at different ambient temperatures might be. Woodrats were acclimated to either 20ЊC or 28ЊC. Later, they were given two diets to choose from (50% juniper and a nontoxic control) for 7 d. Food intake, resting metabolic rate (RMR), and body temperature (T b ) were measured over the last 2 d. Woodrats at 28ЊC ate significantly less juniper, both proportionally and absolutely, than woodrats at 20ЊC. RMRs were higher for woodrats consuming juniper regardless of ambient temperature, and T b was higher for woodrats consuming juniper at 28ЊC than for woodrats eating control diet at 28ЊC. Thus, juniper consumption by N. albigula is influenced by ambient temperature. We conclude that juniper may influence thermoregulation in N. albigula in ways that are helpful at low temperatures but harmful at warmer temperatures in that juniper PSCs may be more toxic at warmer temperatures. The results suggest that increases in ambient temperature associated with climate change could significantly influence foraging behavior of mammalian herbivores.