The effect of plant secondary metabolites on the interplay between the internal and external environments of marsupial folivores

Abstract

Most woody plants contain a diverse array of plant secondary metabolites (PSMs) that deter vertebrate herbivores. However, mammalian folivores have evolved a complex of physiological and behavioural strategies to counter these compounds, leading to the development of an ''evolutionary arms race''. Marsupial folivores are ideal models to investigate the role of PSMs in the interaction between the external foraging environment and the digestive physiology of mammalian herbivores, as we have a very strong understanding of the diversity and modes of action of PSMs in Eucalyptus, as well as the mechanisms by which animals overcome the effects of these compounds. Studies of marsupial folivores have benefited from the facts that: these herbivores subsist on relatively poor quality diets; they include feeding types from specialist species such as the koala, to generalists; and life history factors such as maternal investment in reproduction can be measured more easily than in eutherians. Here, we describe patterns of spatial variation in the types and distributions of plant secondary metabolites in Australian forests and discuss how this variation influences foraging behaviour, habitat selection and life history strategies in arboreal, folivorous marsupials. We also provide a summary of our understanding of the mechanisms by which marsupials detect and regulate their intake of toxic compounds. While our examples are drawn largely from studies of the interaction between marsupials and Eucalyptus, this knowledge is applicable to advancing our understanding of interactions in plant-mammal systems more broadly. We also identify and discuss key areas that should be the focus of future research.

Comparative dietary ecology of two congeneric marsupial folivores

“…The small fraction of native plant species included in the diets, of the total native flora present in the remnants, however, indicates that much of the indigenous flora was not used as food by either brushtail species. This is not surprising, as many native plants contain toxic secondary metabolites to defend themselves against herbivory (Foley et al 2004;Gleadow et al 2008;DeGabriel et al 2010), in addition to other plant secondary metabolites that preferentially bind to dietary protein, rendering it indigestible and thus largely unavailable to folivores (Barbehenn & Constabel 2011). Additionally, many native taxa have developed sclerophylly (significant development of sclerenchyma tissue; resulting in thickened, hardened foliage) (Specht & Rundel 1990), and such plants are typically unpalatable, low in available nitrogen and high in complex structural compounds such as lignin, making them energetically expensive to digest (Cork & Foley 1991).…”

“…The diet of folivorous species is particularly important when considered in the context of the long co-evolutionary history between plants and herbivores (Coley & Barone 1996;DeGabriel et al 2010). In Australia, marsupial arboreal folivores have evolved a diverse set of behavioural, morphological and physiological adaptations (see Hume 2004;Wiggins et al 2006b) to cope with the nutrient-poor, sclerophyllous and highly toxic foliage characteristic of native flora (Noble 1989;Specht & Rundel 1990;Irlbeck & Hume 2003;Wallis et al 2010).…”

Role of Volatile and Non-Volatile Plant Secondary Metabolites in Host Tree Selection by Christmas Beetles

“…Sideroxylonals appear to cause emetic responses in animals that have ingested the chemical (Lawler et al, 1998;DeGabriel et al, 2010). However, because sideroxylonals are not volatile, animals have to ingest some leaves to detect concentrations in foliage.…”

The dietary preferences of koalas,Phascolarctos cinereus, in southwest Queensland

“…Similarly, the nitrogen-to-sideroxylonal ratio did not explain the feeding decisions of brushtail possum, another marsupial folivore (Wallis et al 2002). Hence, the diet of marsupial folivores cannot be fully explained by a simple ratio (Moore et al 2004a;DeGabriel et al 2010), which might be caused by the complicated digestion process with chemicals reactions and bacterial impacts.…”