title: Disease ecology across soil boundaries: effects of below-ground fungi on above-ground host-parasite interactions.
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.
authors.affiliation: Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA 30322, USA ltao@emory.edu.
authors.forename: Leiling
authors.initials: L
authors.lastname: Tao
authors.affiliation: Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA 30322, USA Department of Ecology and Evolutionary Biology, University of Michigan, 830 N University, Ann Arbor, MI 48109, USA.
authors.forename: Camden D
authors.initials: CD
authors.lastname: Gowler
authors.affiliation: Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA 30322, USA.
authors.forename: Aamina
authors.initials: A
authors.lastname: Ahmad
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Michigan, 830 N University, Ann Arbor, MI 48109, USA.
authors.forename: Mark D
authors.initials: MD
authors.lastname: Hunter
authors.affiliation: Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA 30322, USA.
authors.forename: Jacobus C
authors.initials: JC
authors.lastname: de Roode
mesh_terms: D000818:Animals; D016782:Apicomplexa / Q000472:pathogenicity / Q000502:physiology*; D031108:Asclepias / Q000737:chemistry* / Q000502:physiology*; D002080:Butterflies / Q000469:parasitology*; D002298:Cardenolides / Q000378:metabolism; D006790:Host-Parasite Interactions; D038821:Mycorrhizae / Q000378:metabolism*; D010758:Phosphorus / Q000378:metabolism; D018517:Plant Roots / Q000378:metabolism / Q000382:microbiology
chemical_list: D002298:Cardenolides; D010758:Phosphorus
keywords: below-ground–above-ground interaction; host–parasite interaction; trait-mediated indirect effects