Disentangling dimensions of phytochemical diversity: alpha and beta have contrasting effects on an insect herbivore

Abstract

Phytochemical diversity is comprised of two main dimensions—the average (alpha) within‐plant neighbors or the difference (beta) in the composition of chemicals between plant neighbors. Research, however, has primarily examined the consequences of phytochemical diversity on herbivore performance through a single dimension, even though diversity is multidimensional. Furthermore, the ecological role of phytochemical diversity is not well understood because each of these dimensions exhibits unique biological effects on herbivore performance. Therefore, it has been difficult to tease apart the relative importance of alpha and beta chemical diversities on plant–herbivore interactions. We experimentally manipulated alpha and beta diversities along a chemical gradient to disentangle the relative effects of these dimensions on the performance of a mobile generalist herbivore, Trichoplusia ni (Hübner), using 16 genotypes from the Solanum pennellii introgression lines. First, we found contrasting effects of alpha and beta diversities on herbivore performance. Second, when comparing diversity across and within chemical classes, herbivore performance was reduced when plant neighbors had greater diversity within chemical classes that are biologically inhibiting at higher quantities (i.e., quantitative defenses such as phenolics and acyl sugars). However, herbivore performance was enhanced when plant neighbors had higher levels of chemical classes that are biologically toxic (i.e., qualitative defenses such as alkaloids). Finally, herbivores performed better on plant dicultures compared to monocultures, and performance was positively associated with plant dicultures only when there were high levels of average alpha diversity within plant neighbors. Our results suggest T. ni generalist caterpillars do better when plant neighbors are chemically different because differences provide options for them to choose or to switch between plants to balance chemical uptake. Overall, herbivores interact with a large diversity of plant chemicals at multiple scales, and our results indicate that not all chemical diversity is equal: specific dimensions of phytochemical diversity have unique effects on the dynamics of herbivore performance.

Chemical diversity rather than cultivar diversity predicts natural enemy control of herbivore pests

“…Feeding on multiple toxins could affect caterpillar foraging and subsequently growth by reducing aversion to a plant with a specific toxin, not allowing any specific secondary metabolite to get to a noxious level inside the caterpillar, or by consuming secondary metabolites that have different modes of action and therefore a non-additive effect (Bernays et al 1994). This is evident in a recent study in the same system, where T. ni caterpillars performed best in plant neighborhoods that were chemically different (Glassmire et al 2020). Increasing complexity may make it more difficult to locate and consume high quality plant tissue.…”

Structural and compositional dimensions of phytochemical diversity in the genus Piper reflect distinct ecological modes of action

“…As a result, most prior studies on phytochemical diversity have focused on Accepted Article compositional diversity. (Raguso et al, 2015, Kessler and Kalske, 2018, Verma et al, 2009, Moore et al, 2014, Becerra et al, 2009, Jones and Firn, 1991, Glassmire et al, 2020. Although advances in metabolomics approaches have facilitated a more complete investigation of compositional diversity (Kuhlisch and Pohnert, 2015), methodological challenges have limited our understanding of the functional role of chemical structure in plant-insect interactions.…”

Plant defense synergies and antagonisms affect performance of specialist herbivores of common milkweed

“…Jones and Firn (1991) articulated the problem of multiple defenses clearly: individual plants often express many different types of secondary metabolites, and it is difficult to explain why. One of the leading explanations is synergistic interactions between secondary metabolites (Duffey and Stout 1996, Richards et al 2016, Wetzel and Whitehead 2020). For example, the furanocoumarin Xanthotoxin is more effective when mixed with other furanocoumarins than expected from its performance alone (Berenbaum et al 1991); similarly, amides in Piper plants are more effective in combination than their performance separately suggests (Scott et al 2002, Dyer et al 2003, 2010, Whitehead and Bower 2014).…”