Bottom‐up and top‐down effects of tree species diversity on leaf insect herbivory

Abstract

The diversity of plant neighbors commonly results in direct, bottom‐up effects on herbivore ability to locate their host, and in indirect effects on herbivores involving changes in plant traits and a top‐down control by their enemies. Yet, the relative contribution of bottom‐up and top‐down forces remains poorly understood. We also lack knowledge on the effect of abiotic constraints such as summer drought on the strength and direction of these effects. We measured leaf damage on pedunculate oak (Quercus robur), alone or associated with birch, pine or both in a long‐term tree diversity experiment (ORPHEE), where half of the plots were irrigated while the other half remained without irrigation and received only rainfall. We tested three mechanisms likely to explain the effects of oak neighbors on herbivory: (1) Direct bottom‐up effects of heterospecific neighbors on oak accessibility to herbivores, (2) indirect bottom‐up effects of neighbors on the expression of leaf traits, and (3) top‐down control of herbivores by predators. Insect herbivory increased during the growth season but was independent of neighbor identity and irrigation. Specific leaf area, leaf toughness, and thickness varied with neighbor identity while leaf dry matter content or C:N ratio did not. When summarized in a principal component analysis (PCA), neighbor identity explained 87% of variability in leaf traits. PCA axes partially predicted herbivory. Despite greater rates of attack on dummy caterpillars in irrigated plots, avian predation, and insect herbivory remained unrelated. Our study suggests that neighbor identity can indirectly influence insect herbivory in mixed forests by modifying leaf traits. However, we found only partial evidence for these trait‐mediated effects and suggest that more attention should be paid to some unmeasured plant traits such as secondary metabolites, including volatile organic compounds, to better anticipate the effects of climate change on plant‐insect interactions in the future.

Individual tree traits shape insect and disease damage on oak in a climate‐matching tree diversity experiment

“…Although associational resistance was observed in some comparisons between mixed species plots and oak monocultures, no group of foliar organisms was consistently reduced across sites and years in mixed species plots. Inconsistent tree diversity effects on insect herbivores between years within the same diversity experiment have also been observed in other studies (Castagneyrol et al, , ). Like Climate Match, most tree diversity experiments used in such studies are still at the establishment stage (Verheyen et al, ).…”

“…Tree species diversity may also modify plant apparency, which can be defined the height of focal trees relative to their surroundings, and has been shown to be an important predictor of insect herbivore loads on individual trees (Castagneyrol, Giffard, Péré, & Jactel, ; Régolini et al, ). Moreover, complex indirect effects of plant neighborhood identity on insect herbivory and pathogens may be mediated via modifications to plant traits, including foliar nutritional quality and defenses against herbivory (Castagneyrol et al, ; Forey et al, ).…”

Leaf traits mediate changes in invertebrate herbivory along broad environmental gradients on Mt. Kilimanjaro, Tanzania

“…Collecting a wide spectrum of invertebrate herbivores in different vegetation types is a very challenging task and a combination of different sampling methods could possibly lead to a higher linkage between herbivory, MAT and herbivore abundance. Importantly, leaf herbivory is not only driven by the bottom‐up control but also by the top‐down control (Castagneyrol et al, ; Marczak et al, ; Terborgh, ). Regulation of herbivore abundance by natural enemies could be related to temperature which causes higher predation rates at lower elevations (Roslin et al, ).…”

Forest diversity effects on insect herbivores: do leaf traits matter?

“…Of the few studies that have explored whether plant traits might mediate associational resistance, none have been able to demonstrate a direct link between stand diversity, host trait variation and herbivore abundance or damage (Mraja et al ., ; Moreira et al ., ; Wäschke et al ., ; Castagneyrol et al ., ; but see McArt & Thaler, ). To some extent, this might be attributed to their focus on chemical defensive traits rather than the physical or nutritional properties of leaves.…”

“…This phenomenon of associational resistance has often been attributed to a reduced proportion of host plants as diversity increases (resource concentration hypothesis; Root, 1973;Otway et al, 2005;Heiermann & Sch€ utz, 2008;Sholes, 2008;Bj€ orkman et al, 2010;Plath et al, 2012) and to physical and chemical traits of neighbouring plant species (Atsatt & O'Dowd, 1976;Ruttan & Lortie, 2014). However, the possibility that host plant traits involved in plant-herbivore interactions vary according to the diversity of the surrounding plant community has received little attention (but see Kos et al, 2015;Castagneyrol et al, 2017;Kostenko et al, 2017;Moreira et al, 2017). A better understanding of host trait variation across diversity gradients might improve our understanding of the mechanisms underpinning plant diversity effects on herbivores (Moreira et al, 2016) and might also inform the manipulation of stand diversity for sustainable pest management.…”