Mycorrhizal Fungal–Plant–Insect Interactions: The Importance of a Community Approach

Gehring, Catherine A.; Bennett, Alison E.

doi:10.1603/022.038.0111

Cited by 216 publications

(266 citation statements)

References 60 publications

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“…This foraging shift in response to perceived predation risk could explain why grasses, but not Solidago, became a carbon sink in the presence of carnivores. The higher level of fixed 13 C found in grass roots in the + carnivore treatment compared with the + herbivore treatment is consistent with the expectation that plants alter aboveground-belowground carbon allocation in response to foliar herbivory, with low levels of herbivory (i.e., the + carnivore treatment) promoting allocation belowground and higher levels (i.e., the + herbivore treatment) reducing it (15,16). This stimulation of belowground allocation with low levels of herbivory also may explain the greater 13 C retention in the + carnivore Fig.…”

Section: Discussionsupporting

confidence: 79%

Trophic cascade alters ecosystem carbon exchange

Hawlena

Reese

Bradford

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Trophic cascades-the indirect effects of carnivores on plants mediated by herbivores-are common across ecosystems, but their influence on biogeochemical cycles, particularly the terrestrial carbon cycle, are largely unexplored. Here, using a 13 C pulse-chase experiment, we demonstrate how trophic structure influences ecosystem carbon dynamics in a meadow system. By manipulating the presence of herbivores and predators, we show that even without an initial change in total plant or herbivore biomass, the cascading effects of predators in this system begin to affect carbon cycling through enhanced carbon fixation by plants. Prolonged cascading effects on plant biomass lead to slowing of carbon loss via ecosystem respiration and reallocation of carbon among plant aboveground and belowground tissues. Consequently, up to 1.4-fold more carbon is retained in plant biomass when carnivores are present compared with when they are absent, owing primarily to greater carbon storage in grass and belowground plant biomass driven largely by predator nonconsumptive (fear) effects on herbivores. Our data highlight the influence that the mere presence of predators, as opposed to direct consumption of herbivores, can have on carbon uptake, allocation, and retention in terrestrial ecosystems.experimental ecosystem ecology | animal-mediated carbon cycling | carbon tracer experiment | carbon retention T rophic downgrading-the disproportionate loss of species occupying top trophic levels of ecosystems-is a symptom of global biodiversity decline (1). Cutting short trophic chains in ecosystems causes significant changes in plant community biomass, composition, and diversity (2). These changes come about because loss of carnivores leads to increased impacts of herbivores on plant biomass through changes in herbivore density and foraging strategies (3).It is becoming increasingly recognized that the cascading effects of carnivores may affect ecosystem carbon dynamics as well. By altering the impact of herbivores on plants, carnivores may indirectly regulate the amount and type of plant biomass available for photosynthetic carbon fixation and storage (3-5). Moreover, herbivory can trigger physiological adjustments in the remaining damaged plants, including reduction in photosynthetic rates and increased respiration (6-8). Accordingly, we hypothesized that carnivores should increase plant community carbon fixation and reduce respiration, thereby increasing carbon retention, by causing herbivores to reduce their foraging impacts on plants. We tested this hypothesis with a 13 CO 2 pulse-chase field experiment in a grassland ecosystem in northeastern Connecticut.Using established methods to discern indirect effects of carnivores on plants in ecosystems (9), we applied three experimental treatments in replicated 0.25-m 2 fine-mesh enclosures (Fig. S1): (i) plants only (control), (ii) plants and herbivores (+ herbivore), and (iii) plants, herbivores, and carnivores (+ carnivore). The first treatment served as a control for animal effects, the + he...

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Section: Discussionsupporting

confidence: 79%

Trophic cascade alters ecosystem carbon exchange

Hawlena

Reese

Bradford

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…However, such studies of two-way interactions (e.g. between a plant and its herbivore or an insect herbivore and its symbionts) cannot always predict the responses of organisms in a community [7][8][9]. Here, we adopt a community approach and simultaneously examine the role of both plant -and insect -microbial interactions in modulating the plant -herbivore interaction.…”

Section: Introductionmentioning

confidence: 99%

Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids

2013

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Ecologically significant symbiotic associations are frequently studied in isolation, but such studies of two-way interactions cannot always predict the responses of organisms in a community setting. To explore this issue, we adopt a community approach to examine the role of plant-microbial and insect-microbial symbioses in modulating a plant-herbivore interaction. Potato plants were grown under glass in controlled conditions and subjected to feeding from the potato aphid Macrosiphum euphorbiae. By comparing plant growth in sterile, uncultivated and cultivated soils and the performance of M. euphorbiae clones with and without the facultative endosymbiont Hamiltonella defensa, we provide evidence for complex indirect interactions between insect-and plant-microbial systems. Plant biomass responded positively to the live soil treatments, on average increasing by 15% relative to sterile soil, while aphid feeding produced shifts (increases in stem biomass and reductions in stolon biomass) in plant resource allocation irrespective of soil treatment. Aphid fecundity also responded to soil treatment with aphids on sterile soil exhibiting higher fecundities than those in the uncultivated treatment. The relative allocation of biomass to roots was reduced in the presence of aphids harbouring H. defensa compared with plants inoculated with H. defensa-free aphids and aphid-free control plants. This study provides evidence for the potential of plant and insect symbionts to shift the dynamics of plant-herbivore interactions.

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“…Being a polyphagous defoliator, it feeds on hundreds of host plants, including black poplars. P. nigra L. is also a host plant for native defoliators, such as Lymantria dispar L. In a scenario where losses of above-ground biomass might impact mycorrhizal response as previously reported (Gehring & Whitham 2002, Gehring & Bennett 2009), the issue is whether invasive defoliators could play a role in affecting native ecosystem components such as AM fungi.…”

Section: Introductionmentioning

confidence: 99%

“…Over long-term, leaf herbivory (and clipping) may eventually result in reduced carbon accessibility for the host plant and fungal partners (Barto & Rillig 2010, Saravesi et al 2014, although, in spite of the re-growth of the above-ground tissue, carbon allocation to roots often increases immediately after defoliation, while allocation to shoots decreases (Dyer et al 1991, Holland et al 1996. Although the impact of leaf herbivory on colonization by mycorrhizal fungi has mainly been reported as negative, sometimes even positive or nil effects on fungal symbiosis have been detected (Gehring & Whitham 1994, 2002, Cullings et al 2001, Eom et al 2001, Hokka et al 2004, Kula et al 2005, Pietikäinen et al 2005, Walling & Zabinski 2006, Gehring & Bennett 2009, Saravesi et al 2014, Trocha et al 2015. It has been reported that the variability in responses might depend on the type and extent of defoliation, the duration of the experiment, the mycorrhizal type or plant species considered, the availability of soil nutrients or other not yet known factors (Gehring & Whitham 2002, Gehring & Bennett 2009).…”

Section: Introductionmentioning

confidence: 99%

“…Although the impact of leaf herbivory on colonization by mycorrhizal fungi has mainly been reported as negative, sometimes even positive or nil effects on fungal symbiosis have been detected (Gehring & Whitham 1994, 2002, Cullings et al 2001, Eom et al 2001, Hokka et al 2004, Kula et al 2005, Pietikäinen et al 2005, Walling & Zabinski 2006, Gehring & Bennett 2009, Saravesi et al 2014, Trocha et al 2015. It has been reported that the variability in responses might depend on the type and extent of defoliation, the duration of the experiment, the mycorrhizal type or plant species considered, the availability of soil nutrients or other not yet known factors (Gehring & Whitham 2002, Gehring & Bennett 2009). Barto & Rillig (2010) conducted a metaanalysis study, focusing on the sensitivity of AM and ectomycorrhizal (ECM) colonization of roots to the removal of leaves or shoots by herbivory or clipping.…”

Section: Introductionmentioning

confidence: 99%

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Arbuscular mycorrhizal colonization in black poplar roots after defoliation by a non-native and a native insect

Zampieri¹,

Toffolo²,

Mello³

et al. 2016

iForest

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A major goal in ecology is to understand how interactions among organisms influence ecosystem services. This work compares the effects of two Lepidoptera defoliators, one non-native (Hyphantria cunea) and one native (Lymantria dispar) to Europe, on the colonization of black poplar (the Populus nigra clone "Jean Pourtet") roots by an arbuscular mycorrhizal (AM) symbiotic fungus (Funneliformis mosseae) in a pot experiment. The effects of defoliation have also been assessed on the expression of fungal and plant genes playing a role during symbiosis. Both control and defoliated poplars have shown a low level of mycorrhization. Additionally, neither the non-native nor the native insect seem to strongly affect the AM colonization, at least at the time of observation (eight days from the end of the defoliation). Concerning the gene expression analysis, our results suggest that defoliation does not influence neither the expression of genes coding for a fungal and a plant phosphate transporter nor that of a gene coding for a fungal ATPase, and that there were no differences between defoliation carried out by the non-native and the native insect.

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Mycorrhizal Fungal–Plant–Insect Interactions: The Importance of a Community Approach

Cited by 216 publications

References 60 publications

Trophic cascade alters ecosystem carbon exchange

Trophic cascade alters ecosystem carbon exchange

Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids

Arbuscular mycorrhizal colonization in black poplar roots after defoliation by a non-native and a native insect

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