The Influence of Mutualisms Below Ground on Multitrophic Interactions Above Ground

[摘要] Multitrophic species interactions are shaped by a combination of top-down and bottom-up forces. Mutualisms, by altering partner phenotype, may directly and indirectly alter the strength of these forces. However, the ecological consequences of mutualisms on multitrophic interactions, and the mechanisms by which this may occur, are just beginning to be understood. In this dissertation, I combine a series of manipulative experiments to assess the effects of ubiquitous mutualists of plants belowground, arbuscular mycorrhizal fungi (AMF), on multitrophic interactions. First, in Chapter II, I investigated the effects of the availability of AMF on the induction of milkweed (Asclepias) defenses by herbivores above and belowground, and how herbivore damage influenced AMF colonization of roots. I found that the relative induction or suppression of foliar cardenolides (chemical defenses) and leaf toughness by herbivores was altered by the level of AMF inoculum available to plants, but AMF did not influence herbivore-induction of root cardenolides. Furthermore, I showed that herbivore feeding altered levels of AMF colonization substantially, completing a feedback loop between above and belowground organisms. Next, in Chapter III, I evaluated how AMF-mediated changes in plant traits affect toxin sequestration and performance of oleander aphids (Aphis nerii) and monarch caterpillars (Danaus plexippus). Following AMF-mediated increases in cardenolide concentrations, herbivores sequestered higher concentrations of cardenolides from plants inoculated with AMF across all milkweed species; greater sequestration may help to protect herbivores from natural enemies. In addition, aphid per capita growth rates and individual masses varied with AMF availability, consistently among milkweed species. Aphid performance was greatest on plants under high AMF availability, least on plants under medium AMF availability, and intermediate on plants without AMF. In contrast, caterpillar survival varied strongly with AMF availability in a species-specific manner, highlighting the importance of herbivore identity in their responses to AMF. In Chapter IV, I examined how AMF influence constitutive and aphid-induced volatile organic compound (VOC) emissions in two milkweed species, A. curassavica and A. incarnata. I found that AMF had species-specific effects on VOC emissions; AMF increased total VOC emissions, green leafy volatiles, and methyl salicylate in A. curassavica but decreased these compounds in A. incarnata. In contrast, AMF suppressed emissions of individual terpenes that are also suppressed by aphid feeding in both plant species. As these compounds are important to herbivore and natural enemy attraction, these findings suggest that AMF may alter herbivore-natural enemy interactions in the field. In Chapter V, I examined how AMF affect multitrophic interactions in the field. I found that AMF increased the probability of aphid colonization consistently among plant species but altered aphid abundances differentially among plant species. Following AMF-mediated increases in aphid colonization and abundance, total predator abundances were greatest on plants under high AMF availability, consistently among plant species. However, effects of AMF on individual predators varied; colonization by spiders varied with AMF availability differentially among plant species, irrespective of aphid density. In contrast, aphid midge fly oviposition and predation of aphids varied strongly with aphid density and the amount of AMF available to plants. Most notably, the per capita mortality rate imposed by midge flies on aphids varied with AMF availability. Taken together, my research shows that AMF affect strongly both top-down (via toxin sequestration and natural enemy attraction) and bottom-up (via plant defense and nutrition) forces, indicating that AMF may have pervasive effects on multitrophic interactions.

[发布机构] University of Michigan

[效力级别] chemical ecology

[关键词] plant-herbivore interactions;chemical ecology;Asclepias;arbuscular mycorrhizal fungi;plant-microbe-insect interactions;Aphis nerii;Ecology and Evolutionary Biology;Science;Ecology and Evolutionary Biology