Fine‐scale plant defence variability increases top‐down control of an herbivore

Abstract

Herbivore populations are regulated by a combination of plant defences and natural enemies. While plant defence can suppress herbivore populations, these defences can also adversely affect natural enemies, thereby releasing herbivores from top‐down control. Over their life spans, herbivores and their natural enemies may experience substantial variation in plant defence. Recent studies have demonstrated that individual herbivores feeding on diets containing variable concentrations of plant toxins suffer substantially reduced fitness compared to herbivores feeding on a constant toxin concentration, even when both groups of herbivores experience equivalent means. However, the impacts of defence variability on natural enemies and top‐down control of herbivores are unknown. Using artificial diets, we independently manipulated the mean concentration and variation of a plant toxin experienced by individual Trichoplusia ni caterpillars and its parasitoid Copidosoma floridanum. Additionally, by combining the performance of individual caterpillars on different constant diet concentrations of toxin, we were able to estimate the effect of toxin variability between herbivores using nonlinear averaging. Increases in the mean toxin concentration in the diet of parasitized T. ni hosts decreased the fitness of C. floridanum, while variance in individual diets did not impact parasitoid fitness, even though both mean and variance decreased the fitness of T. ni caterpillars. Increased variability in encountered plant defences suppressed individual herbivore fitness with no perceptible cost to top‐down control. At the population level, however, increased variability between individual herbivore diets decreased the success of parasitoids relative to herbivores, thus reducing the strength of top‐down control. Our study highlights the importance of defence variability at different scales in regulating herbivore performance. Variability in plant defence has the potential to reduce herbivore populations through a combination of bottom‐up and top‐down effects, but only at small spatial scales experienced by individual herbivores. A free Plain Language Summary can be found within the Supporting Information of this article.

Effects of wild, local, and cultivated tobacco varieties on the performance of Spodoptera litura and its parasitoid Meteorus pulchricornis

“…8,9 Plant defense mechanisms can not only decrease the fitness of a herbivore but also adversely affect the herbivore's natural enemies. 2,8,10 Plants have evolved a variety of defense mechanisms that vary greatly among species. Different varieties of the same plant species, such as wild, local, and cultivated varieties, differ with regard to their content of nutrients and the types of toxic substances they produce.…”

“…3,7,[11][12] Plants may reduce herbivore populations directly through bottom-up defenses and indirectly through top-down defenses. 8,9 However, the effects of wild, local, and cultivated varieties of the same plant species, originating in the same region, on their natural enemies and the process of top-down control of herbivores are not clear.…”

“…[5][6][7] Herbivore populations are regulated by a combination of plant defense mechanisms (bottom-up pressure) and their natural enemies, such as parasitoids (top-down pressure). 8,9 Plant defense mechanisms can not only decrease the fitness of a herbivore but also adversely affect the herbivore's natural enemies. 2,8,10 Plants have evolved a variety of defense mechanisms that vary greatly among species.…”

“…To resist the encroachment of herbivores, plants have evolved chemical and physical defenses, which can affect the digestion and metabolism of herbivores, their feeding preference, and other factors; these effects are detrimental to the growth and development of herbivores 5‐7 . Herbivore populations are regulated by a combination of plant defense mechanisms (bottom‐up pressure) and their natural enemies, such as parasitoids (top‐down pressure) 8,9 . Plant defense mechanisms can not only decrease the fitness of a herbivore but also adversely affect the herbivore's natural enemies 2,8,10 …”

Plant chemical diversity and its frequency have distinct but complementary effects on insect foraging

“…This suggests that the effects of spatial variability on a consumer cannot be understood without considering how the spatial frequency, or the patch or grain size, of the variability relates to the movement patterns of the consumer (Pearse et al, 2018). Studies of forced insect diet switching through time show that variability in plant nutrients (Stockhoff, 1993) and defences (Pearse et al, 2018) have major effects on insect performance and can cascade up to the third trophic level (Paul et al, 2021). Forced diet switching laboratory studies are a powerful way to isolate the physiological effects of variability, but they prevent insects from responding behaviourally.…”