Testing the diet-breadth trade-off hypothesis: differential regulation of novel plant secondary compounds by a specialist and a generalist herbivore

Abstract

Specialist herbivores are predicted to have evolved biotransformation pathways that can process large doses of secondary compounds from the plant species on which they specialize. It is hypothesized that this physiological specialization results in a trade-off such that specialists may be limited in ability to ingest novel plant secondary compounds (PSCs). In contrast, the generalist foraging strategy requires that herbivores alternate consumption of plant species and PSC types to reduce the possibility of over-ingestion of any particular PSC. The ability to behaviorally regulate is a key component of this strategy. These ideas underpin the prediction that in the face of novel PSCs, generalists should be better able to maintain body mass and avoid toxic consequences compared to specialists. We explored these predictions by comparing the feeding behavior of two herbivorous rodents: a juniper specialist, Neotoma stephensi, and a generalist, Neotoma albigula, fed diets with increasing concentrations of phenolic resin extracted from the creosote bush (Larrea tridentata), which produces a suite of PSCs novel to both species. The specialist lost more mass than the generalist during the 15-day trial. In addition, although the specialist and generalist both regulated phenolic resin intake by reducing meal size while on the highest resin concentration (4%), the generalist began to regulate intake on the 2% diet. The ability of the generalist to regulate intake at a lower PSC concentration may be the source of the generalist's performance advantage over the specialist. These data provide evidence for the hypothesis that the specialist's foraging strategy may result in behavioral as well as physiological trade-offs in the ability to consume novel PSCs.

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

“…Threshold intakes of PSMs have been documented in several species of terrestrial (Govenor et al, 1997;Simpson and Raubenheimer, 2001;Stapley et al, 2000;Torregrossa et al, 2012) and aquatic (Demott, 1999;Gross and Bakker, 2012) herbivores.…”

“…Several mammalian herbivores appear to use the strategy of altering meal size as a function of PSM concentration (Boyle et al, 2005;Marsh et al, 2007;Sorensen et al, 2005a;Torregrossa et al, 2011;Torregrossa et al, 2012;Wiggins et al, 2006a;Wiggins et al, 2006b;Wiggins et al, 2003). Of the five species studied to date (three woodrats of the genus Neotoma and two marsupials: the koala and brushtail possum), only one exhibited a change in intermeal interval when fed increasing concentration of dietary PSMs (Sorensen et al, 2005a;Torregrossa and Dearing, 2009).…”

“…Of the five species studied to date (three woodrats of the genus Neotoma and two marsupials: the koala and brushtail possum), only one exhibited a change in intermeal interval when fed increasing concentration of dietary PSMs (Sorensen et al, 2005a;Torregrossa and Dearing, 2009). Recent studies suggest that generalist herbivores may be better at regulating PSM dose than specialist herbivores (Torregrossa et al, 2012). Specialist herbivores may not need to regulate intake of PSMs since their biotransformation system has evolved to process high doses of PSMs in a limited diet or because they absorb a lower proportion of PSMs consumed (Marsh et al, 2006b;Shipley et al, 2009;Sorensen et al, 2004).…”

“…The mechanisms through which regulation of meal size and frequency occurs and why they differ between species are currently unknown. The leading proposed mechanisms are detection of PSMs in food and in blood plasma, conditioned learning, and intestinal or gustatory receptors Torregrossa et al, 2011;Torregrossa et al, 2012). To date, regulation of PSMs through meal size and intermeal interval has not been studied in aquatic herbivores.…”

Animal plant warfare and secondary metabolite evolution

“…The mixed diet of generalistic herbivores reduce the need for detoxification of similar groups of toxic PSM, whereas herbivores specialist to one or few plant species as food source developed especially improved metabolic detoxification pathways. [26][27][28][29][30][31] In the past decades, many phytochemicals have been isolated and investigated for their pharmacological activities. Examples include Lamiaceae plants such as lavender (Lavandula angustifolia Mille.…”