Novel Plant Secondary Metabolites Impact Dietary Specialists More than Generalists (neotoma Spp.)

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 2 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.