Plant Secondary Metabolites Compromise the Energy Budgets of Specialist and Generalist Mammalian Herbivores

Abstract

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.

The dilemma of foraging herbivores: dealing with food and fear

“…They can either wait until they have detoxified sufficiently to continue eating or change their food source by quitting the patch. The "sit and wait" strategy appears better suited to specialist herbivores, which tend to have efficient physiological mechanisms for dealing with toxins and a lower resting metabolism, such as koalas (Degabriele and Dawson 1979) and woodrats (Neotoma stephensi) (Sorensen et al 2005b). We suggest generalists are more likely benefit from moving to another food source.…”

“…Plant defence compounds such as toxins and digestibility reducers impose significant costs on foraging herbivores, including a range of negative pharmacological consequences (reviewed in Forbey et al 2013) and energetic costs of detoxification (Sorensen et al 2005b). Many compounds can cause physiological damage, force a reduction in food intake or may cause starvation (Bryant and Kuropat 1980;Sorensen et al 2005a;Shipley et al 2012).…”

“…We differentiate these two food "axes" because herbivores strive for an appropriate mix of the former while confronting the costs of the latter (Freeland and Janzen 1974;Foley et al 1999;Simpson et al 2004), and because physiological tolerance along these axes varies among herbivore species (Sorensen et al 2005b;Shipley et al 2012) and populations (Dearing 1996). Predation risk can also vary within prey species as a function of population size or an individual's reproductive condition, sex, age, body size; between prey species as a function of body size (Sinclair et al 2003) and prey evolutionary history (acute or chronic response to predation risk (Boonstra 2013)); and among communities depending on the diversity of prey and predators.…”

A Pharm-Ecological Perspective of Terrestrial and Aquatic Plant-Herbivore Interactions

“…For example, common brushtail possums had higher tolerance to diets rich in benzoic acid when they were provided with substrates needed for the detoxification and excretion of benzoates (Marsh et al, 2005). In addition, supplemental energy and protein may increase the ability of herbivores to consume foods that contain diverse PSMs (Nersesian et al, 2012;Provenza et al, 2003) by providing the resources needed to pay for high energetic costs of detoxification (Foley and McArthur, 1994;Mangione et al, 2004;Sorensen et al, 2005c).…”

“…Other responses such as locomotor activity (Sorensen et al, 2005c), metabolic rates (Bozinovic and Novoa, 1997;Sorensen et al, 2005c), thermoregulation (McLister et al, 2004), organ damage (Fu et al, 2004), water balance (Dearing et al, 2002;Mangione et al, 2004) and acid-base homeostasis (Foley et al, 1995) have also been investigated. Only a single study has examined the effect of blood concentration of PSMs on intake in a wild mammal (Mclean et al, 2007), which may be critical to predicting foraging phenotypes in nature.…”