Abstract
Host-parasite interactions are subject to strong trait-mediated indirect effects from other species. However, it remains unexplored whether such indirect effects may occur across soil boundaries and connect spatially isolated organisms. Here, we demonstrate that, by changing plant (milkweed Asclepias sp.) traits, arbuscular mycorrhizal fungi (AMF) significantly affect interactions between a herbivore (the monarch butterfly Danaus plexippus) and its protozoan parasite (Ophryocystis elektroscirrha), which represents an interaction across four biological kingdoms. In our experiment, AMF affected parasite virulence, host resistance and host tolerance to the parasite. These effects were dependent on both the density of AMF and the identity of milkweed species: AMF indirectly increased disease in monarchs reared on some species, while alleviating disease in monarchs reared on other species. The species-specificity was driven largely by the effects of AMF on both plant primary (phosphorus) and secondary (cardenolides; toxins in milkweeds) traits. Our study demonstrates that trait-mediated indirect effects in disease ecology are extensive, such that below-ground interactions between AMF and plant roots can alter host-parasite interactions above ground. In general, soil biota may play an underappreciated role in the ecology of many terrestrial host-parasite systems.
Highlights
Interactions between hosts and their parasites depend on more than just two partners
We illustrate that interactions among members of four biological kingdoms link the fast growing fields of below-ground–above-ground species interactions and disease community ecology by showing complex interactions among plant symbiotic fungi, plants, herbivores and parasites
The relationship between a protozoan parasite and its herbivore host above ground depends upon the presence and the abundance of soil fungi that influence plant nutritional and defensive traits
Summary
Interactions between hosts and their parasites depend on more than just two partners. To analyse effects on parasite virulence, we used a linear model with adult monarch lifespan as the dependent variable, parasite treatment (uninfected versus infected), plant species (three species in the pilot experiment; six species in the main 3 experiment), AMF presence (absence/presence) or abundance (control, low and high) and their interactions as independent variables. To determine if AMF affect host tolerance to parasites, we used adult lifespan of butterflies as the dependent variable, AMF presence (absence/presence) or abundance (control, low and high), plant species (three in the pilot experiment; six in the main experiment), log transformed spore load and their interactions as independent variables. All statistical tests were performed using R v. 2.15.3 [42]
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