Individual and non‐additive effects of exotic sap‐feeders on root functional and mycorrhizal traits of a shared conifer host

Abstract

Forest pests drive tree mortality through disruption of functional traits linked to nutrient acquisition, growth and reproduction. The impacts of attack by individual or multiple above‐ground herbivores on root functional traits critical to tree health have received little attention. This is especially true for exotic herbivores, organisms often found in disturbed forests. We excavated whole‐root systems from eastern hemlock (Tsuga canadensis) individuals experimentally infested with hemlock woolly adelgid (HWA: Adelges tsugae) and elongate hemlock scale (EHS: Fiorina externa) individually, or in combination, for periods of 2 and 4 years. Below‐ground root biomass, functional traits and storage nutrients were measured to assess impacts of herbivory. We also quantified ectomycorrhizal fungal (EMF) colonisation of fine roots and used culture‐independent methods to examine EMF diversity. Trees infested with HWA had a greater root mass fraction (root to total biomass ratio), although feeding had no observable effects on root functional traits (e.g. specific root length) or on resource allocation to roots. HWA feeding did significantly reduce EMF colonisation of hemlock fine roots, though surprisingly, EMF diversity and that of other fungal associates were unaffected. In contrast to HWA, EHS (alone or in conjunction with HWA) feeding had no observable effect on below‐ground traits or EMF colonisation alone; however, its presence mediated HWA effects when trees were co‐infested. Simultaneous infestation within the same year yielded significant reductions in EMF colonisation, whereas prior EHS attack weakened HWA effects. Our results collectively suggest that prior EHS attack dampens the impact of HWA on below‐ground functional traits. This highlights how the timing and sequence of herbivore arrival can alter plant‐mediated interactions between herbivores and their effects on above–below‐ground linkages and associated tree health. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12910/suppinfo is available for this article.

Chronic impacts of invasive herbivores on a foundational forest species: a whole‐tree perspective

“…Details regarding insect densities from 2011 to 2014 are presented elsewhere (Schaeffer et al 2017). Details regarding insect densities from 2011 to 2014 are presented elsewhere (Schaeffer et al 2017).…”

“…Insect densities were assessed twice yearly, in early spring and late fall, throughout the experiment. Details regarding insect densities from 2011 to 2014 are presented elsewhere (Schaeffer et al 2017). Because our focus is on cumulative treatment impacts, we report November 2014 insect densities solely as an indicator of whole-tree infestation levels.…”

“…Belowground harvest and processing protocols are detailed elsewhere (Schaeffer et al 2017). Each marked branch was then clipped at the base and placed on ice in a plastic bag.…”

“…Our results also confirm previous work (G omez et al 2012) showing that adelgids cause localized increases of N and the amino acid proline at their feeding sites. In Arabidopsis this pattern is associated with aphidinduced increases in the hormone abscisic acid (ABA; Hillwig et al 2016): adelgid also induces ABA production following attack (Schaeffer et al 2017). For instance, paralleling increases in proline, adelgid-infested tissues had lower levels of the amino acids isoleucine and tryptophan.…”

“…For instance, paralleling increases in proline, adelgid-infested tissues had lower levels of the amino acids isoleucine and tryptophan. We hypothesize that ABA induction following adelgid feeding aids its success through prevention of effective JA pathway signaling, which is known to deter HWA crawlers (Schaeffer et al 2017). In Arabidopsis this pattern is associated with aphidinduced increases in the hormone abscisic acid (ABA; Hillwig et al 2016): adelgid also induces ABA production following attack (Schaeffer et al 2017).…”