Leaf odour cues enable non‐random foraging by mammalian herbivores

Abstract

Searching for food is the first critical stage of foraging, and search efficiency is enhanced when foragers use cues from foods they seek. Yet we know little about food cues used by one major group of mammals, the herbivores, a highly interactive component of most ecosystems. How herbivores forage and what disrupts this process, both have significant ecological and evolutionary consequences beyond the animals themselves. Our aim was to investigate how free-ranging mammalian herbivores exploit leaf odour cues to find food plants amongst a natural and complex vegetation community. Our study system comprised the native "deer equivalent" of eastern Australian forests, the swamp wallaby Wallabia bicolor, and seedlings of Eucalyptus, the foundation tree genus in these ecosystems. We quantified how foraging wallabies responded to odour cues from plants manipulated in several ways: varying the quantity of visually concealed leaves, comparing damaged vs. undamaged leaves, and whole plants vs. those with suppressed cues. The rate of discovery of leaves by wallabies increased with odour cue magnitude, yet animals were extremely sensitive to even a tiny odour source of just a few leaves. Whole seedlings were discovered faster if their leaves were damaged. Wallabies found whole seedlings and those with suppressed visual cues equally rapidly, day and night. Seedlings with very little odour were discovered mainly by day, as nocturnal foraging success was severely disrupted. This study shows how leaf odour attracts mammalian herbivores to food plants, enabling non-random search for even tiny odour sources. As damaged leaves enhanced discovery, we suggest that the benefit of attracting natural enemies to invertebrate herbivores feeding on plants (potential "cry for help") may be offset by a cost-increased browsing by mammalian herbivores. This cost should be incorporated into multi-trophic plant-animal studies. Finally, the breakdown in capacity to find plants at night suggests substantial but unrecognized foraging costs to herbivores when abiotic factors, such as cold temperatures or pollution, reduce or degrade plant odour cues. We predict that an increasingly polluted world will alter the foraging success of mammalian herbivores, with significant ecological ramifications given that browsing can shape ecosystems.

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

“…Herbivoreinduced plant volatiles (HIPVs), that are emitted by plants upon attack by herbivores, are remarkable olfactory cues in the sense that they provide indirect information on the presence of herbivores because they are produced by the plant under attack and not directly by the herbivores themselves (Vet and Dicke 1992, Hare 2011, Turlings and Erb 2018. HIPVs and other plant-derived volatiles are used during long-distance foraging by mammals (Finnerty et al 2017), birds (Mäntylä et al 2004, Amo et al 2013, reptiles (Stork et al 2011), and insects (Turlings and Erb 2018). Yet, HIPV use is particularly well studied for parasitoid wasps (Vet andDicke 1992, Turlings andErb 2018).…”

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.…”

Unravelling the functions of biogenic volatiles in boreal and temperate forest ecosystems

“…Biotic stress is caused by herbivores, parasitic plants and microbial plant pathogens. Constitutively emitted BVOCs of plants provide important foraging cues to herbivorous animals and especially for specialist herbivore species, which use volatile cues to locate their specific host plant species among other plants (Finnerty et al 2017). Herbivoreinduced plant volatiles (HIPV) are mostly BVOCs synthesised in plants after feeding damage by a herbivore, although some of the constitutively emitted BVOCs are emitted at higher rates and they are an important part of the herbivoreinduced volatile blend (Holopainen and Gershenzon 2010;Aartsma et al 2017).…”