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Herbivore diet breadth mediates the cascading effects of carnivores in food webs.

ABSTRACT: Predicting the impact of carnivores on plants has challenged community and food web ecologists for decades. At the same time, the role of predators in the evolution of herbivore dietary specialization has been an unresolved issue in evolutionary ecology. Here, we integrate these perspectives by testing the role of herbivore diet breadth as a predictor of top-down effects of avian predators on herbivores and plants in a forest food web. Using experimental bird exclosures to study a complex community of trees, caterpillars, and birds, we found a robust positive association between caterpillar diet breadth (phylodiversity of host plants used) and the strength of bird predation across 41 caterpillar and eight tree species. Dietary specialization was associated with increased enemy-free space for both camouflaged (n = 33) and warningly signaled (n = 8) caterpillar species. Furthermore, dietary specialization was associated with increased crypsis (camouflaged species only) and more stereotyped resting poses (camouflaged and warningly signaled species), but was unrelated to caterpillar body size. These dynamics in turn cascaded down to plants: a metaanalysis (n = 15 tree species) showed the beneficial effect of birds on trees (i.e., reduced leaf damage) decreased with the proportion of dietary specialist taxa composing a tree species' herbivore fauna. We conclude that herbivore diet breadth is a key functional trait underlying the trophic effects of carnivores on both herbivores and plants.

SUBMITTER: Singer MS

PROVIDER: S-EPMC4084428 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Herbivore diet breadth mediates the cascading effects of carnivores in food webs.

Singer Michael S MS Lichter-Marck Isaac H IH Farkas Timothy E TE Aaron Eric E Whitney Kenneth D KD Mooney Kailen A KA

Proceedings of the National Academy of Sciences of the United States of America 20140616 26

Predicting the impact of carnivores on plants has challenged community and food web ecologists for decades. At the same time, the role of predators in the evolution of herbivore dietary specialization has been an unresolved issue in evolutionary ecology. Here, we integrate these perspectives by testing the role of herbivore diet breadth as a predictor of top-down effects of avian predators on herbivores and plants in a forest food web. Using experimental bird exclosures to study a complex commun ...[more]

PMID: 24979778

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Project description:Terrestrial tri-trophic interactions account for a large part of biodiversity, with approximately 75% represented in plant-insect-parasitoid interactions. Herbivore diet breadth is an important factor mediating these tri-trophic interactions, as specialisation can influence how herbivore fitness is affected by plant traits. We investigated how phytochemistry, herbivore immunity, and herbivore diet breadth mediate plant-caterpillar-parasitoid interactions on the tropical plant genus Piper (Piperaceae) at La Selva Biological station in Costa Rica and at Yanayacu Biological Station in Ecuador. We collected larval stages of one Piper generalist species, Quadrus cerealis, (Lepidoptera: Hesperiidae) and 4 specialist species in the genus Eois (Lepidoptera: Geometridae) from 15 different species of Piper, reared them on host leaf material, and assayed phenoloxidase activity as a measure of potential larval immunity. We combined these data with parasitism and caterpillar species diet breadth calculated from a 19-year database, as well as established values of phytochemical diversity calculated for each plant species, in order to test specific hypotheses about how these variables are related. We found that phytochemical diversity was an important predictor for herbivore immunity, herbivore parasitism, and diet breadth for specialist caterpillars, but that the direction and magnitude of these relationships differed between sites. In Costa Rica, specialist herbivore immune function was negatively associated with the phytochemical diversity of the Piper host plants, and rates of parasitism decreased with higher immune function. The same was true for Ecuador with the exception that there was a positive association between immune function and phytochemical diversity. Furthermore, phytochemical diversity did not affect herbivore immunity and parasitism for the more generalised herbivore. Results also indicated that small differences in herbivore diet breadth are an important factor mediating herbivore immunity and parasitism success for Eois at both sites. These patterns contribute to a growing body of literature that demonstrate strong cascading effects of phytochemistry on higher trophic levels that are dependent on herbivore specialisation and that can vary in space and time. Investigating the interface between herbivore immunity, plant chemical defence, and parasitoids is an important facet of tri-trophic interactions that can help to explain the enormous amount of biodiversity found in the tropics.

Project description:Host plant defenses are known to cascade up food chains to influence herbivores and their natural enemies, but how herbivore and predator traits and identity mediate such tri-trophic dynamics is largely unknown. We assessed the influence of plant defense on aphid and coccinellid performance in laboratory trials with low- vs. high-glucosinolate varieties of Brassica napus, a dietary specialist (Brevicoryne brassicae) and generalist (Myzus persicae) aphid, and five species of aphidophagous coccinellids. The performance of the specialist and generalist aphids was similar and unaffected by variation in plant defense. Aphid glucosinolate concentration and resistance to predators differed by aphid species and host plant defense, and these effects acted independently. With respect to aphid species, the dietary generalist aphid (vs. specialist) had 14% lower glucosinolate concentration and coccinellid predators ate three-fold more aphids. With respect to host plant variety, the high-glucosinolate plants (vs. low) increased aphid glucosinolate concentration by 21%, but had relatively weak effects on predation by coccinellids and these effects varied among coccinellid species. In turn, coccinellid performance was influenced by the interactive effects of plant defense and aphid species, as the cascading, indirect effect of plant defense was greater when feeding upon the specialist than generalist aphid. When feeding upon specialist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by 78% and accelerated development by 14%. In contrast, when feeding upon generalist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by only 11% and had no detectable effect on development time. These interactive effects of plant defense and aphid diet breadth on predator performance also varied among coccinellid species; the indirect negative effects of plant defenses on predator performance was consistent among the five predators when transmitted via the dietary specialist aphid, but these effects varied substantially among predators-in both the magnitude and direction-when transmitted via the dietary generalist aphid. Accordingly, the cascading effect of plant defense on predators was stronger in magnitude and more consistent among predator taxa when transmitted by the specialist than generalist herbivore. Overall, these findings support a central role of herbivore diet breadth in mediating both the strength and contingency of tri-trophic interactions.

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Herbivore diet breadth mediates the cascading effects of carnivores in food webs.

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Herbivore diet breadth mediates the cascading effects of carnivores in food webs.

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