Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits

Gange, Alan C.; Bower, Erica; Brown, V. K.

doi:10.1007/s004420050840

Cited by 117 publications

(88 citation statements)

References 28 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 Sumentioning

confidence: 51%

“…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).…”

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 Sumentioning

confidence: 51%

Section: Introductionmentioning

confidence: 99%

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Meier

Hunter

2018

Front. Ecol. Evol.

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“…For example, it has been shown that reproductive traits of aboveground herbivorous arthropods can be positively or negatively affected by belowground arbuscular mycorrhizal fungi (Gange et al 1999;Goverde et al 2000).…”

Section: Discussionmentioning

confidence: 99%

“…For example, Gange et al (1999) reported that the fecundity of two species of aphids (Myzus persicae and M. ascalonicus) was enhanced when the aphids fed on mycorrhiza-infected Plantago. Likewise, spider mites (T. urticae) fed on mycorrhiza-infected plants showed increased egg production (Hoffmann et al 2009) although this pattern was in contrast to the findings Koricheva et al (2009).…”

Section: Discussionmentioning

confidence: 99%

Belowground microbial symbiont enhances plant susceptibility to a spider mite through change in soybean leaf quality

et al. 2010

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To examine how rhizobia affect the chemical and nutrient status in leaves of soybean (Glycine max L.), and how rhizobia change plant susceptibility to a generalist spider mite (Tetranycus urticae), we cultivated root-nodulating soybeans (R?) and their non-nodulating mutant (R-) in a common garden. We experimentally fertilized the plants with nitrogen to examine effects of rhizobia on the plant traits and plant susceptibility to spider mites at different nitrogen levels. R? plants produced more leaves containing greater nitrogen and less total phenolics than R-plants. Spider mites fed on R? leaves produced more eggs than those fed on R-leaves. The positive effect of rhizobia on spider mite fecundity could be due to an increase in foliar N content and/or to a decrease in concentration of phenolics. Although root nodule mass did not differ among different nitrogen levels, ureide-N, an indicator of nitrogen provided by rhizobia, in xylem sap decreased at moderate and high soil nitrogen levels. Therefore, we expected that rhizobia effects on egg production of the spider mite would decrease in high soil nitrogen conditions. However, the effect of rhizobia was still maintained even at high soil nitrogen levels. Thus, soil nitrogen and rhizobia may independently affect the reproductive performance of the spider mite.

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“…A cursory examination of the literature provides support for these predictions. In all of the annual species examined-Plantago lanceolata (Gange et al 1999(Gange et al , 2002b, soybean (Borowicz 1997), and Abutilon theophrasti (Sanders et al 1993)-herbivore fitness increased on host plants associated with mycorrhizal fungi as predicted by the nutritional hypotheses. However, additional studies with two of these species-Plantago lanceolata (Gange and West 1994) and soybean (Rabin and Pacovsky 1985)-demonstrated a decline in herbivore fitness on host plants associated with mycorrhizal fungi, suggesting a need for further study.…”

Section: Plant Successional Statusmentioning

confidence: 96%

Three-Way Interactions among Mutualistic Mycorrhizal Fungi, Plants, and Plant Enemies: Hypotheses and Synthesis

Bennett¹,

Alers-Garcia²,

Bever³

2006

The American Naturalist

101

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A number of studies have shown that an association with mycorrhizal fungi can alter the outcome of interactions between plants and their enemies. While the directions of these effects vary, their strength suggests the need for greater attention to multispecies interactions among plant enemies, plants, and mycorrhizal fungi. We recognize that mycorrhizal fungi could effect plant enemies by improving plant nutrition, modifying plant tolerance, or modifying plant defenses. In addition, mycorrhizal fungi could directly interfere with pathogen infection, herbivory, or parasitism by occupying root space. We formalize these alternative outcomes of multispecies interactions and explore the long-term dynamics of the plant-enemy interactions based on these different scenarios using a general model of interactions between plants and plant enemies. We then review the literature in terms of the assumptions of the alternative mechanisms and the predictions of these models. Through this effort, we identify new directions in the study of tritrophic interactions between enemies, plants, and soil mutualists.

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Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits

Cited by 117 publications

References 28 publications

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Belowground microbial symbiont enhances plant susceptibility to a spider mite through change in soybean leaf quality

Three-Way Interactions among Mutualistic Mycorrhizal Fungi, Plants, and Plant Enemies: Hypotheses and Synthesis

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