Below‐ground responses to insect herbivory in ecosystems with woody plant canopies: A meta‐analysis

Abstract

1. Insect herbivory can have important consequences for the functioning of terrestrial ecosystems. Despite a growing recognition of the role of herbivores in above-ground-below-ground interactions, our current understanding is mainly restricted to studies of vertebrates in grassland and tundra ecosystems, while ecosystems with tree-like canopies (termed forests below) and invertebrates remain understudied.2. Here, we assess the current state of knowledge of one key aspect of plant-herbivore interactions by conducting a meta-analysis of the peer-reviewed literature on the below-ground consequences of above-ground insect herbivory in forest ecosystems. Main results are reported as aggregated relative effect sizes (Cohen's d).3. We find that above-ground insect herbivory reduced below-ground carbon (C) allocation by plants to roots (−0.56) and root exudation (−0.85), causing shifts in root-symbiont communities, for example, a decrease (−0.67) in the abundance of ectomycorrhizal fungi. Microbial decomposer abundances showed no significant responses, while soil faunal abundances increased (0.50). C and nitrogen (N) mineralization rates (C: 0.48, N: 0.48) along with nutrient leaching (C: 0.30, N: 0.77) increased, with a stronger response to outbreak relative to background insect densities. The negative responses increased in strength in colder and dryer biomes while positive responses were reinforced in warmer and wetter biomes, thus extending previously shown effects for vertebrate herbivores to also include insect herbivory. The positive response by soil fauna to insect herbivory was the notable exception. This may be associated with the limited physical soil disturbance caused by insects compared to ungulates. Furthermore, we identified an underrepresentation in the literature of large areas of boreal and tropical biomes calling for research priorities to fill these knowledge gaps. We present three recommendations for future research: addressing (a) biological drivers of biogeochemistry and response pathways, (b) knowledge gap from boreal and tropical forests, and (c) heterogeneity of herbivore disturbances.4. Synthesis. Insect herbivores significantly accelerate soil C and N cycling during outbreaks in forest ecosystems, but we lack knowledge on the underlying biological drivers. Overall, below-ground responses to insect herbivory are similar to vertebrate herbivory responses, which may simplify implementing herbivory effects 918 | Journal of Ecology KRISTENSEN ET al.

Insect defoliation is linked to a decrease in soil ectomycorrhizal biomass and shifts in needle endophytic communities

“…Our findings agree with previously described cascading effects of reduced carbon assimilation by trees affecting belowground mutualists (Högberg et al 2001;Pec et al 2016;Kristensen et al 2020). In our study, insect defoliation was linked to changes in the soil fungal community structure and trophic function.…”

“…For example, a decline in primary productivity caused by insect defoliation could negatively affect ecosystem processes such as nutrient cycling through affecting belowground communities (Clemmensen et al 2015;Saravesi et al 2015;Kristensen et al 2020). Climate change is expected to increase the severity and frequency of insect outbreaks (Battisti et al 2005, Hódar & Zamora 2004.…”

Background insect herbivory increases with local elevation but makes minor contribution to element cycling along natural gradients in the Subarctic

“…Studies from grassland systems have shown that insect herbivory increases belowground allocation of photosynthates by their hosts, possibly to boost their nutrient uptake (Belovsky & Slade, 2000; Hamilton et al., 2008). Yet, in forest ecosystems, belowground C allocation by plants is reduced by aboveground insect herbivory (Frost & Hunter, 2008a; Kristensen et al., 2020), which represents a reduction in fast‐cycle processes. Moreover, the immediate induction in chemical plant defenses (Fürstenberg‐Hägg et al., 2013; Halitschke et al., 2008; Haukioja, 2005; Kessler et al, 2004) increase the decomposition time of the resulting litter (Chomel et al, 2016), although it is not clear to what extent these effects may be transient (Frost & Hunter, 2008b).…”

“…While less conspicuous than mammals, insect herbivores can exert a similar or even stronger control than mammals on ecosystem functioning (Hunter, 2001, Kristensen et al., 2020; Lovett et al., 2002; Risch et al., 2018; Silfver et al., 2020), particularly in forest ecosystems, where their impact is likely to intensify substantially with global change (Logan et al., 2003). Insect herbivory may cause early leaf abscission (Karban, 2007; Zvereva & Kozlov, 2014), leaf consumption (Galmán et al., 2018; Kozlov et al., 2015), alteration of aboveground versus belowground allocation of photosynthates (Ayres et al., 2004; Kristensen et al., 2020), and induction of plant defenses (Fürstenberg‐Hägg et al., 2013; Halitschke et al., 2008; Haukioja, 2005; Kessler et al, 2004). These effects alter the timing, quantities, and pathways of element fluxes, including the partitioning between fast‐ and slow‐cycle pathways through the decomposition foodweb (Frost & Hunter, 2004, 2007; Hunter et al., 2012; Kristensen et al., 2018).…”

Dynamic effects of insect herbivory and climate on tundra shrub growth: Roles of browsing and ramet age

“…There is thus a growing body of evidence that warmer conditions will lead to intensified insect herbivory, which could result in reduced growth of common woody plants at high latitudes. These growth reductions can result from direct losses of foliar area restricting photosynthetic gains (Björkman et al, 2000) but also via alterations in soil available resources and mycorrhizal status (Kristensen et al, 2020;Sandén et al, 2020).…”