Downstairs drivers ‐ root herbivores shape communities of above‐ground herbivores and natural enemies via changes in plant nutrients

Abstract

Summary 1.Terrestrial food webs are woven from complex interactions, often underpinned by plant-mediated interactions between herbivores and higher trophic groups. Below-and aboveground herbivores can influence one another via induced changes to a shared host plant, potentially shaping the wider community. However, empirical evidence linking laboratory observations to natural field populations has so far been elusive. 2. This study investigated how root-feeding weevils (Otiorhynchus sulcatus) influence different feeding guilds of herbivore (phloem-feeding aphids, Cryptomyzus galeopsidis, and leaf-chewing sawflies, Nematus olfaciens) in both controlled and field conditions. 3. We hypothesized that root herbivore-induced changes in plant nutrients (C, N, P and amino acids) and defensive compounds (phenolics) would underpin the interactions between root and foliar herbivores, and ultimately populations of natural enemies of the foliar herbivores in the field. 4. Weevils increased field populations of aphids by ca. 700%, which was followed by an increase in the abundance of aphid natural enemies. Weevils increased the proportion of foliar essential amino acids, and this change was positively correlated with aphid abundance, which increased by 90% on plants with weevils in controlled experiments. 5. In contrast, sawfly populations were 77% smaller during mid-June and adult emergence delayed by >14 days on plants with weevils. In controlled experiments, weevils impaired sawfly growth by 18%, which correlated with 35% reductions in leaf phosphorus caused by root herbivory, a previously unreported mechanism for above-ground-below-ground herbivore interactions. 6. This represents a clear demonstration of root herbivores affecting foliar herbivore community composition and natural enemy abundance in the field via two distinct plant-mediated nutritional mechanisms. Aphid populations, in particular, were initially driven by bottom-up effects (i.e. plant-mediated effects of root herbivory), but consequent increases in natural enemies triggered top-down regulation.

Spatially distinct responses within willow to bark stripping by deer: effects on insect herbivory

“…Second, lower nitrogen concentrations in the resprouting leaves may result in lower nutritional quality for insect herbivores (Mattson 1980). Herbivory can also affect leaf traits distant from the damaged site by changing resource allocation at the whole-plant scale (Gange and Brown 1989;Bezemer et al 2003;Johnson et al 2013). Johnson et al (2013) reported that root feeding weevils induced changes in aboveground plant nutrients (C, N, P, and amino acids) and defensive compounds (phenolics) of blackcurrant.…”

“…In contrast, several authors have reported that herbivory by one herbivore can positively or negatively affect other herbivores that are distant from the damaged site due to changes in resource allocation at the whole-plant scale (Gange and Brown 1989;Bezemer et al 2003;Johnson et al 2013). Regardless, previous studies have generally focused on particular plant parts either close to or distant from the damaged site (Roininen et al 1997;Bezemer et al 2003;Nakamura et al 2003;Johnson et al 2013). However, if the direction (positive or negative) and magnitude of plant-mediated effects differ between spatially separated plant parts, focusing only on a particular part would lead to under-or over-estimation of the effect at the whole-plant scale.…”

“…Many studies on these Bplant-mediated effects^have investigated plant parts (e.g., leaves and shoots) close to the site of herbivory (Danell and Huss-Danell 1985;Roininen et al 1997;Martinsen et al 1998;Nakamura et al 2003;Bailey and Whitham 2006;Lind et al 2012), on the assumption that induced responses tend to be stronger closer to the damage. In contrast, several authors have reported that herbivory by one herbivore can positively or negatively affect other herbivores that are distant from the damaged site due to changes in resource allocation at the whole-plant scale (Gange and Brown 1989;Bezemer et al 2003;Johnson et al 2013). Regardless, previous studies have generally focused on particular plant parts either close to or distant from the damaged site (Roininen et al 1997;Bezemer et al 2003;Nakamura et al 2003;Johnson et al 2013).…”

Responses of Insect Pests and Plant Diseases to Changing and Variable Climate: A Review

“…This increases survival, dissemination and spread of mainly the soil borne pathogens to areas that were not previously infected (Thompson et al, 2013). Fungal pathogens benefit from flood events compared to any other pathogens (Parvatha, 2015).…”

“…The increase in frequency and intensity of extreme weather events, changes in moisture conditions, temperature rises and elevated carbon dioxide concentrations are expected to magnify pest pressure on agricultural systems through various ways (Johnson et al, 2013). Insect pests are likely to respond through range expansion of the existing insect pests, invasion by new insect pests and accelerated insect pest development (Parvatha, 2015).…”