The Influence of Plant Secondary Metabolites on the Nutritional Ecology of Herbivorous Terrestrial Vertebrates

Abstract

Plant secondary metabolites (PSMs) significantly impact the nutritional ecology of terrestrial vertebrate herbivores. Herbivores have a wide range of mechanisms (herbivore offenses) to mitigate the negative effects of PSMs. We discuss several behavioral and physiological offenses used by terrestrial vertebrates. Several newly recognized herbivore offenses such as regulated absorption and regulation of toxin intake are presented. We give a detailed description of the biotransformation system with respect to PSMs. We also summarize recent findings of plant-animal interactions for lizards, birds, and mammals. Finally, we discuss some new tools that can be applied to long-standing questions of plant-vertebrate interactions.

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

“…In invertebrates, fat bodies and the digestive system, including the different gut compartments and the digestive gland, are responsible for the biotransformation of toxins (Appel, 1993;Gross et al, 2008;Hyne and Maher, 2003;Keeley, 1985;Rewitz et al, 2006). The enzymes responsible for the metabolism of drugs have been extensively investigated in laboratory and domestic mammals but far less so with respect to PSMs in wild herbivores, particularly aquatic ones (Dearing et al, 2005;Sotka et al, 2009). Drug metabolizing enzymes are extremely diverse and categorized broadly by function into Phase 1 enzymes such as the cytochromes P450 or Phase 2 enzymes such as glutathione S-transferases and glucuronyltransferases (Casarett et al, 2008).…”

“…In general, metabolizing enzymes act to convert lipid soluble PSMs (and other ingested chemicals) into more water-soluble metabolites that can then be excreted (Casarett et al, 2008;McLean and Duncan, 2006). Individual mammals have hundreds of different drug metabolizing enzymes that are described elsewhere (for reviews see (Casarett et al, 2008;Dearing et al, 2005;McLean and Duncan, 2006). The cytochromes P450 enzymes of aquatic crustaceans responsible for detoxification differed from those of fish (Koenig et al, 2012), indicating differences between invertebrates and vertebrates.…”

“…Another function of gut microbes might be the detoxification of ingested PSMs (Chandler et al, 2008;Dearing et al, 2005;Foley et al, 1999;Kohl and Dearing, 2012;Kohl et al, 2011). There is at least one spectacular example of this phenomenon in domestic ruminants.…”

“…For several decades now, a central focus in the field of nutritional ecology has been to understand the factors that influence the foraging behavior of terrestrial and aquatic herbivores (Choat and Clements, 1998;Clements et al, 2009;Dearing et al, 2005;Foley et al, 1999;Scriber and Slansky, 1981). There is ample evidence from each of these areas that the foraging behavior of herbivores is driven by both nutrients and chemical defenses.…”

“…However, the presence of plant secondary (or specialized) metabolites (PSMs), which can act as chemical defenses, often constrain intake despite the abundance of critical nutrients in those foods (Appel, 1993;Behmer et al, 2002;Dearing et al, 2005;Foley and McArthur, 1994;Hay and Fenical, 1988;Palo and Robbins, 1991;Paul et al, 2006;). …”