Olfactory and visual plant cues as drivers of selective herbivory

Stutz, Rebecca S.; Croak, Benjamin M.; Proschogo, Nicholas; Banks, Peter B.; McArthur, Clare

doi:10.1111/oik.03422

Cited by 29 publications

(21 citation statements)

References 72 publications

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“…Quantitative apparency will generally increase attacks from enemies, while the roles of qualitative apparency are complicated. For example, specific plant defensive compounds may reduce visiting and feeding by most insects but attract some herbivore specialists (Smilanich et al., ), and red leaf color is a warning signal for many animals, but there are some exceptions (Stutz et al ., ). However, the total apparency of one plant is the combination of all quantitative and qualitative apparency indicators and functions as a whole in relation to enemies.…”

Section: Introductionmentioning

confidence: 97%

Global pattern of plant utilization across different organisms: Does plant apparency or plant phylogeny matter?

Dai

Zhang

et al. 2017

Ecology and Evolution

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The present study is the first to consider human and nonhuman consumers together to reveal several general patterns of plant utilization. We provide evidence that at a global scale, plant apparency and phylogenetic isolation can be important predictors of plant utilization and consumer diversity. Using the number of species or genera or the distribution area of each plant family as the island “area” and the minimum phylogenetic distance to common plant families as the island “distance”, we fitted presence–area relationships and presence–distance relationships with a binomial GLM (generalized linear model) with a logit link. The presence–absence of consumers among each plant family strongly depended on plant apparency (family size and distribution area); the diversity of consumers increased with plant apparency but decreased with phylogenetic isolation. When consumers extended their host breadth, unapparent plants became more likely to be used. Common uses occurred more often on common plants and their relatives, showing higher host phylogenetic clustering than uncommon uses. On the contrary, highly specialized uses might be related to the rarity of plant chemicals and were therefore very species‐specific. In summary, our results provide a global illustration of plant–consumer combinations and reveal several general patterns of plant utilization across humans, insects and microbes. First, plant apparency and plant phylogenetic isolation generally govern plant utilization value, with uncommon and isolated plants suffering fewer parasites. Second, extension of the breadth of utilized hosts helps explain the presence of consumers on unapparent plants. Finally, the phylogenetic clustering structure of host plants is different between common uses and uncommon uses. The strength of such consistent plant utilization patterns across a diverse set of usage types suggests that the persistence and accumulation of consumer diversity and use value for plant species are determined by similar ecological and evolutionary processes.

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Section: Introductionmentioning

confidence: 97%

Global pattern of plant utilization across different organisms: Does plant apparency or plant phylogeny matter?

Dai

Zhang

et al. 2017

Ecology and Evolution

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“…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.…”

Section: Stage 1: Visiting Patchesmentioning

confidence: 54%

“…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.…”

Section: Discussionmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Mella

Possell

Troxell-Smith

et al. 2018

Journal of Animal Ecology

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Foraging is a three-stage process during which animals visit patches, consume food and quit. Foraging theory exploring relative patch quality has mostly focused on patch use and quitting decisions, ignoring the first crucial step for any forager: finding food. Yet, the decision to visit a patch is just as important as the decision to quit, as quitting theories can only be used if animals visit patches in the first place. Therefore, to better understand the foraging process and predict its outcomes, it is necessary to explore its three stages together. We used the common brushtail possum (Trichosurus vulpecula) as a model to investigate foraging decisions in response to food varying in quality. In particular, we tested whether patch nutritional quality affected the following: (1) patch visits; (2) behaviours at the patch during a foraging visit; and (3) patch quitting decisions (quantified using giving up density-GUD). Free-ranging possums were presented with diets varying in nitrogen content and concomitantly volatile organic compound (VOC) composition at feeding stations in the wild. We found that possums were able to distinguish between different quality foods from afar, despite the location of the diets changed daily. Possums used VOC (i.e. odour cues) emitted by the diets to find and select patches from a distance. High-quality diets with higher protein and lower fibre were visited more often and for longer. Possums spent more time foraging on diets high in nutritional content, resulting in lower GUDs. Our study provides important quantitative evidence that foraging efficiency plays out during all the three stages of the foraging process (i.e. visit, consume and quit), and demonstrates the significance of considering all these stages together in future studies and foraging models. Sensory cues such as food odours play a critical role in helping foragers, including mammalian herbivores, find high-quality food. This allows foragers to make quick, accurate and important decisions about food patches well before patch quitting decisions come into play.

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“…The difference in host preference and performance by the soybean looper could be an indication of the evolution of herbivore defense in M. polymorpha where changes in defense strategies are based on risk of herbivore attack (Orians & Ward, 2010). If herbivores are present but rarely attack in the invaded range, possibly because of differences in food cues (Stutz, Croak, Proschogo, Banks, & McArthur, 2017) or the presence of a more nutritional food source, then a shift from constitutive defenses toward inducible defenses might be expected. While nonsignificant, our results showed a trend toward higher growth rates on the Eurasian (Doorduin & Vrieling, 2011;Orians & Ward, 2010) in New World (invaded range) plant genotypes.…”

Section: Discussionmentioning

confidence: 99%

Rapid evolution of Medicago polymorpha during invasion shifts interactions with the soybean looper

Jack

Friesen

2019

Ecology and Evolution

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The Enemy Release Hypothesis posits that invasion of novel habitats can be facilitated by the absence of coevolved herbivores. However, a new environment and interactions with unfamiliar herbivores may impose selection on invading plants for traits that reduce their attractiveness to herbivores or for enhanced defenses compared to native host plants, leading to a pattern similar to enemy release but driven by evolutionary change rather than ecological differences. The Shifting Defense Hypothesis posits that plants in novel habitats will shift from specialized defense mechanisms to defense mechanisms effective against generalist herbivores in the new range. We tested these ideas by comparing herbivore preference and performance of native (Eurasia)‐ and invasive (New World)‐range Medicago polymorpha, using a generalist herbivore, the soybean looper, that co‐occurs with M. polymorpha in its New World invaded range. We found that soybean loopers varied in preference and performance depending on host genotype and that overall the herbivore preferred to consume plant genotypes from naïve populations from Eurasia. This potentially suggests that range expansion of M. polymorpha into the New World has led to rapid evolution of a variety of traits that have helped multiple populations become established, including those that may allow invasive populations to resist herbivory. Thus, enemy release in a novel range can occur through rapid evolution by the plant during invasion, as predicted by the Shifting Defense Hypothesis, rather than via historical divergence.

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Olfactory and visual plant cues as drivers of selective herbivory

Cited by 29 publications

References 72 publications

Global pattern of plant utilization across different organisms: Does plant apparency or plant phylogeny matter?

Global pattern of plant utilization across different organisms: Does plant apparency or plant phylogeny matter?

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

Rapid evolution of Medicago polymorpha during invasion shifts interactions with the soybean looper

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