Follow your nose: leaf odour as an important foraging cue for mammalian herbivores

Abstract

Studies of odour-driven foraging by mammals focus on attractant cues emitted by flowers, fruits, and fungi. Yet, the leaves of many plant species worldwide produce odour, which could act as a cue for foraging mammalian herbivores. Leaf odour may thus improve foraging efficiency for such herbivores in many ecosystems by reducing search time, particularly but not only, for plants that are visually obscured. We tested the use of leaf odour by a free-ranging mammalian browser, the swamp wallaby (Wallabia bicolor) to find and browse palatable tree seedlings (Eucalyptus pilularis). Wallabies visited patches non-randomly with respect to the presence of seedlings. In the absence of visual plant cues, they used leaf odour (cut seedlings in vials) to find patches earlier, and visited and investigated them more often than control patches (empty vials), supporting the hypothesis that wallabies used seedling odour to enhance search efficiency. In contrast, the grey kangaroo (Macropus giganteus), a grazer, showed no response to seedling odour. When the availability of seedling visual and olfactory cues was manipulated, wallabies browsed seedlings equally quickly in all treatments: upright (normal cues), pinned to the ground (reduced visual cues), and upright plus pinned seedlings (double olfactory cues). Odour cues play a critical role in food-finding by swamp wallabies, and these animals are finely tuned to detecting these cues with their threshold for detection reached by odours from only a single plant. The global significance of leaf odour in foraging by mammalian herbivores consuming conifers, eucalypts, and other odour-rich species requires greater attention.

Olfactory and visual plant cues as drivers of selective herbivory

“…In experiment 1, we tested whether wallabies could use odour cues alone to differentiate low‐ and high‐nutrient seedlings, in the absence of any visual seedling cues. In a previous study, we demonstrated that swamp wallabies could use odours to find E. pilularis seedlings (Stutz et al ). Here, we quantified behavioural responses of wallabies to patches under three odour treatments: buried vials that were empty, or that contained a cut E. pilularis seedling grown under either low‐ or high‐nutrient conditions.…”

“…But many browsing herbivores have evolved physiological and behavioural mechanisms to deal with toxins (McArthur et al , Dearing et al , Iason and Villalba ). Browsers may therefore use VOCs, not only to avoid, but also to find food plants as well as assess their quality once found (Halitschke et al , Bedoya‐Pérez et al , Stutz et al ).…”

Visit, consume and quit: Patch quality affects the three stages of foraging

“…The advantage of the ability to detect high-quality food items from afar using smell is the foraging efficiency gained by not having to waste time tasting food to assess its nutritional value. Taste is a powerful mechanism for assessing food quality and hence determining food selection (Provenza, 1995a,b), but in our study and others (Bedoya-Pérez et al, 2013;Finnerty et al, 2017;Stutz et al, 2016Stutz et al, , 2017, odour played an earlier key role for the selection of high-quality diets, well before the food was even sampled.…”

“…The ability to use odour cues to differentiate between nutrient‐rich vs. nutrient‐poor foods has been demonstrated in gastropod herbivores (Hanley, Collins, & Swann, ; Moelzner & Fink, ). The swamp wallaby also uses odour to aid in the detection of high‐nutrient food items, visiting, investigating (Finnerty et al., ; Stutz et al., , ) and eating (Bedoya‐Pérez et al., ) more nutrient‐rich food than lower quality foods. These studies and others (Bedoya‐Pérez et al., ; Provenza et al., ) show that herbivores exploit olfactory cues released after plant damage or from plant toxic compounds to find food.…”

“…The exploitation of odour cues emitted by food to increase forging efficiency has been studied mainly in the context of predator (Hughes et al, 2010) or invertebrate foragers (Beyaert & Hilker, 2014;Kaiser, Hughes, & Gibson, 1993), including blood sucking ectoparasites (Guerin et al, 2000), and there is mounting evidence that birds use olfaction to find food (Amo, Jansen, Dam, Dicke, & Visser, 2013;Mäntylä, Blande, & Klemola, 2014;Nevitt, Veit, & Kareiva, 1995). Recent studies have shown that a mammalian browser, the swamp wallaby (Wallabia bicolor), can exploit olfactory sensory cues from leaves to find and select food patches, and thus forage nonrandomly (Bedoya-Pérez, Isler, Banks, & McArthur, 2013;Finnerty, Stutz, Price, Banks, & McArthur, 2017;Stutz, Banks, Proschogo, & McArthur, 2016;Stutz, Croak, Banks, Proschogo, & McArthur, 2017). Apart from this, we know little about the olfactory cues used by mammalian herbivores to find food, despite the knowledge that olfaction is highly acute in many of these species (Donaldson & Stoddart, 1994;Miller et al, 2015;Provenza, Kimball, & Villalba, 2000) and that olfaction and taste functions are linked (Jakubas & Mason, 1991;Slotnick, Westbrook, & Darling, 1997), reinforcing the possibility that olfactory cues may be used to determine food quality.…”