Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Abstract

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.

Arbuscular mycorrhizal fungi mediate herbivore‐induction of plant defenses differently above and belowground

“…The commercial AMF mix was purported to consist of four AMF species, and AMF species vary in nutrient trading and resulting effects on plant phenotype , Thonar et al 2014, Argüello et al 2016). However, we consider this explanation to be unlikely; cloning and Sanger sequencing of the AMF mix, and of milkweed roots from plants grown under the same experimental conditions, revealed that the AMF mix consisted only of Funneliformis mosseae (Meier and Hunter 2018a). Therefore, the differential effects of medium and high AMF inoculum availability on herbivore-induction of defenses are more likely due to plant suppression of AMF colonization under high AMF inoculum availability than to differential colonization by AMF species.…”

“…We describe key results in more detail below. Note that we have reported the effects of AMF on the traits of the undamaged (control) milkweeds previously in a manuscript on herbivore performance (Meier and Hunter 2018a). Here, we use data from the control plants only to measure the magnitude of induction in treatment (herbivore-damaged) plants.…”

“…We obtained fungal inoculum from Mycorrhizal Applications (Grants Pass, OR, USA), which was comprised of cosmopolitan AMF species, including Rhizophagus intraradices, Funneliformis mosseae, Glomus aggregatum and Claroideoglomus etunicatum (33 spores of each AMF species per gram of inoculum, < www.plant-success.com >). However, cloning and Sanger sequencing of the inoculum revealed that the inoculum consisted only of Funneliformis mosseae (Meier and Hunter 2018a). Milkweeds grow in habitats that host a diversity of AMF taxa (Öpik et al 2006), and can form associations with these cosmopolitan AMF species in natural and experimental populations (Landis et al 2004, Vannette and Hunter 2011, Tao et al 2015.…”

High levels of arbuscular mycorrhizal fungus colonization on Medicago truncatula reduces plant suitability as a host for pea aphids (Acyrthosiphon pisum)

“…To the extent of our knowledge, this is the first report studying the outcome of insect–plant–microbe interactions with a focus on phloem feeders’ probing and feeding behavior on a leguminous plant with different levels of root colonization by AM fungi. In general, positive effects of the AM symbiosis on phloem feeders have been documented (Gange et al ., ; Hempel et al ., ; Koricheva et al ., ; Babikova et al ., ; Simon et al ., ; Maurya et al ., ; Meier & Hunter, ). In previous studies, the extent of root colonization by AM fungi ranged between 15% and 55% RLC.…”

“…The indirect effects of AM fungi on plant interactions with aphids has resulted in beneficial (Gange et al, 2002;Babikova et al, 2014a;Maurya et al, 2018;Meier & Hunter, 2018), detrimental (Guerrieri et al, 2004;Babikova et al, 2013;Maurya et al, 2018;Meier & Hunter, 2018), or no effects on aphids (Gehring & Bennett, 2009;Hartley & Gange, 2009;Karley et al, 2017). Previous research found a positive effect of the AM symbiosis on aphid adult weight (Gange & West, 1994;Gange et al, 1999), percent growth (Gange et al, 2002), and aphid abundance (Babikova et al, 2014a).…”