Herbivory reduces plant interactions with above‐ and belowground antagonists and mutualists

Abstract

Abstract. Herbivores affect plants through direct effects, such as tissue damage, and through indirect effects that alter species interactions. Interactions may be positive or negative, so indirect effects have the potential to enhance or lessen the net impacts of herbivores. Despite the ubiquity of these interactions, the indirect pathways are considerably less understood than the direct effects of herbivores, and multiple indirect pathways are rarely studied simultaneously. We placed herbivore effects in a comprehensive community context by studying how herbivory influences plant interactions with antagonists and mutualists both aboveground and belowground. We manipulated early-season aboveground herbivore damage to Cucumis sativus (cucumber, Cucurbitaceae) and measured interactions with subsequent aboveground herbivores, root-feeding herbivores, pollinators, and arbuscular mycorrhizal fungi (AMF). We quantified plant growth and reproduction and used an enhanced pollination treatment to determine if plants were pollen limited. Increased herbivory reduced interactions with both antagonists and mutualists. Plants with high levels of early herbivory were significantly less likely to suffer leaf damage later in the summer and tended to be less attacked by root herbivores. Herbivory also reduced pollinator visitation, likely due to fewer and smaller flowers, and reduced AMF colonization. The net effect of herbivory on plant growth and reproduction was strongly negative, but lower fruit and seed production were not due to reduced pollinator visits, because reproduction was not pollen limited. Although herbivores influenced interactions between plants and other organisms, these effects appear to be weaker than the direct negative effects of early-season tissue loss.

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

“…(b) Plants attacked by an aboveground herbivore induce systemic defense responses [herbivore-induced resistance (HIR)] in roots, which have a negative impact on arbuscular mycorrhizal fungi (AMF), reducing the scope for ISR (6,9,28). In addition, systemic induced changes in root exudates can either facilitate or inhibit infection by belowground phytophages.…”

Attracting mutualists and antagonists: Plant trait variation explains the distribution of specialist floral herbivores and pollinators on crops and wild gourds

“…Generalists such as honeybees and bumblebees can also be effective pollinators ( Artz and Nault, 2011 ). Cucumber beetles ( Diabrotica spp., Acalymma vittatum ) can reduce yield in cucurbits through direct damage ( Barber et al, 2011 ;Barber et al, 2012 ) and indirectly by reducing pollinator attraction ) and acting as a vector of pathogens ( Sasu et al, 2010 ). Cucumber beetle adults damage leaves and fl owers early in the season and lay eggs in the soil.…”

Herbivore-Induced DNA Demethylation Changes Floral Signalling and Attractiveness to Pollinators in Brassica rapa

“…In the case of insect-pollinated plants, there is a strong trade-off in resource investment as the two processes are often competing—not only on a metabolic, but also on an ecological level [1–3]: plant defence measures can deter pollinators [4, 5], and signals attractive to pollinators can also attract herbivores [6, 7], a phenomenon known as the defence-apparency dilemma [8]. Since herbivore and pollinator compositions can fluctuate in time and space, plants need a system to quickly react to alterations of the surrounding insect community [9].…”