Invader disruption of belowground plant mutualisms reduces carbon acquisition and alters allocation patterns in a native forest herb

Abstract

SummaryInvasive plants impose novel selection pressures on na€ ıve mutualistic interactions between native plants and their partners. As most plants critically rely on root fungal symbionts (RFSs) for soil resources, invaders that disrupt plant-RFS mutualisms can significantly depress native plant fitness. Here, we investigate the consequences of RFS mutualism disruption on native plant fitness in a glasshouse experiment with a forest invader that produces known antifungal allelochemicals.Over 5 months, we regularly applied either green leaves of the allelopathic invader Alliaria petiolata, a nonsystemic fungicide to simulate A. petiolata's effects, or green leaves of nonallelopathic Hesperis matronalis (control) to pots containing the native Maianthemum racemosum and its RFSs. We repeatedly measured M. racemosum physiology and harvested plants periodically to assess carbon allocation.Alliaria petiolata and fungicide treatment effects were indistinguishable: we observed inhibition of the RFS soil hyphal network and significant reductions in M. racemosum physiology (photosynthesis, transpiration and conductance) and allocation (carbon storage, root biomass and asexual reproduction) in both treatments relative to the control.Our findings suggest a general mechanistic hypothesis for local extinction of native species in ecosystems challenged by allelopathic invaders: RFS mutualism disruption drives carbon stress, subsequent declines in native plant vigor, and, if chronic, declines in RFS-dependent species abundance.

Herbaceous invaders in temperate forests: a systematic review of their ecology and proposed mechanisms of invasion

“…Since the majority of native understory herbs rely on mutualisms with mycorrhizae, the potential impact of allelopathic chemicals that disrupt these mutualisms are significant. For example, the allelochemicals of A. petiolata (Cantor et al 2011;Hale and Kalisz 2012) have been found to affect carbon storage and photosynthesis (Hale et al 2016), demographic performance (Brouwer et al 2015b) of native understory perennial herbs, and have long-term legacy affects (Lankau et al 2014). Further, the impacts of these allelopathic or other invader effects on the soil ecosystem, microbial community structure, nutrient cycling and the native community can be long-term and also show legacy effects (Elgersma et al 2011).…”

Effects of deer on the photosynthetic performance of invasive and native forest herbs

“…Comparable trends in abundance have been reported for additional invaders in other deciduous forests (Eschtruth and Battles 2009; Dávalos et al 2015 a ; Shen et al 2016). While other studies have investigated potential physiological impacts of Alliaria on native species (Hale et al 2011, 2016) and Alliaria photosynthetic physiology in general (Dhillion and Anderson 1999; Anderson and Cipollini 2013; Stinson and Seidler 2014), the physiological basis for deer-mediated plant invasions remains unexplained.…”

A novel mechanism to explain success of invasive herbaceous species at the expense of natives in eastern hardwood forests

“…To test their model, Hale et al . carried out a five‐month field study wherein they added various materials to growth pots of feathery false lily of the valley ( Maianthemum racemosum ), a native forest herb which supports mycorrhizas and which is an important component in herbaceous layer communities throughout eastern deciduous forests (Gilliam, ). Materials included (1) green leaves of garlic mustard, (2) a non‐systemic fungicide, and (3) green leaves of dames rocket ( Hesperis matronalis ), another member of the Brassicaceae.…”

“…Notably, the effects of additions of fresh foliar material of garlic mustard and fungicide were essentially identical. Not only were there the expected reductions in mycorrhizal network biomass (Cantor et al ., ; Brouwer et al ., ), but there were also reductions in all ecophysiological and C allocation measurements in treated pots relative to controls receiving fresh, non‐allelopathic foliar material (Hale et al .).…”

“…Hale et al . provide evidence that quite clearly supports their general mechanistic hypothesis (their fig. 1) for local extinction of native species in forests invaded by species with allelopathic properties.…”