Stable isotope labelling of earthworms can help deciphering belowground–aboveground interactions involving earthworms, mycorrhizal fungi, plants and aphids

Grabmaier, Andrea; Heigl, Florian; Eisenhauer, Nico; Heijden, Marcel G. A. van der; Zaller, Johann G.

doi:10.1016/j.pedobi.2014.10.002

Cited by 10 publications

(6 citation statements)

References 58 publications

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“…Aphids had the lowest per capita growth rates and individual masses on plants under medium AMF availability, yet had the highest per capita growth rates and masses on plants under high AMF availability (Figure 2). Thus, we found within a single study the range of aphid responses to AMF from the literature, from positive to negative (Pacovsky et al, 1985;Gange and West, 1994;Gange et al, 1999Gange et al, , 2002Gehring and Whitham, 2002;Wurst et al, 2004;Hempel et al, 2009;Koricheva et al, 2009;Abdelkarim et al, 2011;Babikova et al, 2014a;Colella et al, 2014;Grabmaier et al, 2014;Williams et al, 2014;Bennett et al, 2016;Simon et al, 2017;Tomczak and Müller, 2017). Our findings suggest that some of the previously found variation in aphid responses may result from differences in AMF inoculum availability among studies.…”

Section: Amf Abundance Alters Specialist Herbivore Performance and Susupporting

confidence: 65%

“…AMF-mediated increases in aphid performance under high AMF availability may also be a consequence of increased vascular bundle size; AMF colonization increases the size of vascular bundles in plants (Krishna et al, 1981), increasing aphid phloem feeding and reproductive success (Simon et al, 2017). Although aphids are often responsive to changes in amino acid content of phloem (Züst and Agrawal, 2016a), we think it unlikely that AMF influenced A. nerii performance by changing phloem soluble sugar or amino acid content because previous studies found no correlations among AMF-mediated changes in aphid performance and foliar or phloem nutrient content (Gange and West, 1994;Hempel et al, 2009;Grabmaier et al, 2014).…”

Section: Amf Abundance Alters Specialist Herbivore Performance and Sumentioning

confidence: 90%

“…For instance, aphids generally benefit from AMF colonization of their host plants; aphids are more attracted to plants colonized by AMF and have greater body masses, growth rates, and fecundity on host plants colonized by AMF (Gange and West, 1994;Gange et al, 1999Gange et al, , 2002Koricheva et al, 2009;Babikova et al, 2014a,b;Simon et al, 2017). However, aphids have also been found to not respond to AMF colonization of their host plants (Pacovsky et al, 1985;Wurst et al, 2004;Colella et al, 2014;Grabmaier et al, 2014;Williams et al, 2014;Bennett et al, 2016) or to have reduced population growth on plants colonized by AMF (Gehring and Whitham, 2002;Hempel et al, 2009;Abdelkarim et al, 2011). Similarly, while some specialist chewers benefit from AMF colonization of their host plants (Borowicz, 1997;Goverde et al, 2000;, others are unaffected (Laird and Addicott, 2008;Cosme et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Meier

Hunter

2018

Front. Ecol. Evol.

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Multitrophic species interactions are shaped by both top-down and bottom-up factors. Belowground symbionts of plants, such as arbuscular mycorrhizal fungi (AMF), can alter the strength of these forces by altering plant phenotype. For example, AMF-mediated changes in foliar toxin and nutrient concentrations may influence herbivore growth and fecundity. In addition, many specialist herbivores sequester toxins from their host plants to resist natural enemies, and the extent of sequestration varies with host plant secondary chemistry. Therefore, by altering plant phenotype, AMF may affect both herbivore performance and their resistance to natural enemies. We examined how inoculation of plants with AMF influences toxin sequestration and performance of two specialist herbivores feeding upon four milkweed species (Asclepias incarnata, A. curassavica, A. latifolia, A. syriaca). We raised aphids (Aphis nerii) and caterpillars (Danaus plexippus) on plants for 6 days in a fully factorial manipulation of milkweed species and level of AMF inoculation (zero, medium, and high). We then assessed aphid and caterpillar sequestration of toxins (cardenolides) and performance, and measured defensive and nutritive traits of control plants. Aphids and caterpillars sequestered higher concentrations of cardenolides from plants inoculated with AMF across all milkweed species. Aphid per capita growth rates and aphid body mass varied non-linearly with increasing AMF inoculum availability; across all milkweed species, aphids had the lowest performance under medium levels of AMF availability and highest performance under high AMF availability. In contrast, caterpillar survival varied strongly with AMF availability in a plant species-specific manner, and caterpillar growth was unaffected by AMF. Inoculation with AMF increased foliar cardenolide concentrations consistently among milkweed species, but altered aboveground biomasses and foliar phosphorous concentrations in a plant species-specific fashion. Increased herbivore sequestration of cardenolides followed AMF-mediated increases in foliar cardenolide concentrations. Aphid performance declined with increasing foliar cardenolide concentrations, while caterpillar survival increased with aboveground biomass. Our findings suggest that by altering plant phenotype, the availability of AMF in soil has the potential to influence both top-down (via sequestration) and bottom up (via plant defense and nutrition) forces that operate on herbivores.

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Section: Amf Abundance Alters Specialist Herbivore Performance and Susupporting

confidence: 65%

Section: Amf Abundance Alters Specialist Herbivore Performance and Sumentioning

confidence: 90%

Section: Introductionmentioning

confidence: 99%

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Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Meier

Hunter

2018

Front. Ecol. Evol.

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“…The mechanisms by which AM fungi influence aphid growth and life history traits are largely unknown. Aphids are often responsive to changes in amino acid content of phloem sap, but when such changes have been searched for in mycorrhizal experiments, they have been absent 27 33 34 . Instead, it has been suggested that it is more likely due to mycorrhizal-induced increases in leaf vascular bundle size 35 , leading to increased phloem feeding.…”

mentioning

confidence: 99%

Unravelling mycorrhiza-induced wheat susceptibility to the English grain aphid Sitobion avenae

Simon

Wellham

Aradottir

et al. 2017

Sci Rep

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Arbuscular mycorrhizal (AM) fungi are root symbionts that can increase or decrease aphid growth rates and reproduction, but the reason by which this happens is unknown. To investigate the underlying mechanisms of this interaction, we examined the effect of AM fungi on the English Grain aphid (Sitobion avenae) development, reproduction, attraction, settlement and feeding behaviour on two naturally susceptible varieties Triticum aestivum (L.) variety Solstice and T. monococcum MDR037, and two naturally resistant lines, T. monococcum MDR045 and MDR049. Mycorrhizal colonisation increased the attractiveness of T. aestivum var. Solstice to aphids, but there was no effect on aphid development on this variety. Using the Electrical Penetration Graph (EPG) technique, we found that mycorrhizal colonisation increased aphid phloem feeding on T. monococcum MDR037 and MDR045, colonisation also increased growth rate and reproductive success of S. avenae on these varieties. Mycorrhizas increased vascular bundle size, demonstrating that these fungi can influence plant anatomy. We discuss if and how this could be related to an enhanced success rate in phloem feeding in two varieties. Overall, we present and discuss how mycorrhizal fungi can affect the feeding behaviour of S. avenae in wheat, inducing susceptibility in a resistant variety.

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“…Via the conduit of a shared plant host, multitrophic interactions can occur amongst a wide range of below-and above-ground organisms including bacteria, fungi, invertebrates and vertebrates (Gehring & Bennett, 2009;Pineda, Zheng, Loon, & Dicke, 2012;van der Heyde, Bennett, Pither, & Hart, 2017). Due to the diverse organisms that exhibit interactions across the above-and below-ground interface, these interactions have large implications in key ecological processes such as nutrient cycling (Grabmaier, Heigl, Eisenhauer, Heijden, & Zaller, 2014;Hodge & Fitter, 2010;Lau, 2011), potent greenhouse gas emissions (Bender, Conen, & van der Heijden, 2015;Storer, Coggan, Ineson, & Hodge, 2018) and both population and community structure (Gehring & Bennett, 2009). Arbuscular mycorrhizal fungi (AMF) are obligate symbionts that form a mutualistic relationship with the roots of around two thirds of plant species (Hughes, Hodge, Fitter, & Atkin, 2008).…”

Section: Introductionmentioning

confidence: 99%

Aphids can acquire the nitrogen delivered to plants by arbuscular mycorrhizal fungi

et al. 2019

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Above‐ and below‐ground organisms can interact by altering the quality of shared host plants. Arbuscular mycorrhizal fungi (AMF) influence plant nutrient uptake, including nitrogen (N) acquisition. Under low N and phosphorus conditions, AMF delivery of N from organic sources not immediately available to the plant can have large impacts on plant N status, a limiting nutrient in the aphid diet. This study investigated the effect of AMF colonisation upon aphid number and determined the consequences of AMF directly accessing an organic nutrient patch that the plant cannot. We hypothesised that AMF colonisation of plants will increase plant and aphid N status, plant performance and aphid number, but only when the AMF had direct access to the added organic patch. Barley plants hosting the grain aphid Sitobion avenae were colonised by the AMF, Funneliformis mosseae, or no AMF. A two‐compartment microcosm was used to separate the plant roots from a 15N‐labelled organic patch in a second compartment. AMF‐colonised plants, but without access to the second compartment, were used to examine the effect of AMF colonisation on aphid number. In a separate treatment, and to determine whether AMF access to a plant inaccessible N source modified the effect of AMF colonisation on aphid number, AMF hyphae were permitted access to the second compartment containing an organic patch. As a control for AMF accessing a larger substrate volume, AMF were allowed access to a second compartment without an organic patch. When the AMF accessed the organic patch, more N from the patch was delivered to the plant resulting in a higher grain N concentration although plant growth was depressed. More N from the patch was also delivered to the aphids, but the N status of the aphid remained unchanged. Regardless of the level of access to the organic patch, AMF colonisation did not affect aphid number. Our data show that by accessing N sources not readily available to plants, AMF can indirectly deliver N to above‐ground organisms, a finding which has major implications for N‐transfer between higher trophic levels. A plain language summary is available for this article.

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Stable isotope labelling of earthworms can help deciphering belowground–aboveground interactions involving earthworms, mycorrhizal fungi, plants and aphids

Cited by 10 publications

References 58 publications

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Unravelling mycorrhiza-induced wheat susceptibility to the English grain aphid Sitobion avenae

Aphids can acquire the nitrogen delivered to plants by arbuscular mycorrhizal fungi

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