Parasite Removal, but Not Herbivory, Deters Future Parasite Attachment on Tomato

Abstract

Plants face many antagonistic interactions that occur sequentially. Often, plants employ defense strategies in response to the initial damage that are highly specific and can affect interactions with subsequent antagonists. In addition to herbivores and pathogens, plants face attacks by parasitic plants, but we know little about how prior herbivory compared to prior parasite attachment affects subsequent host interactions. If host plants can respond adaptively to these different damage types, we predict that prior parasitism would have a greater deterrent effect on subsequent parasites than would prior herbivory. To test the effects of prior parasitism and prior herbivory on subsequent parasitic dodder (Cuscuta spp.) preference, we conducted two separate greenhouse studies with tomato hosts (Solanum lycopersicum). In the first experiment, we tested the effects of previous dodder attachment on subsequent dodder preference on tomato hosts using three treatments: control plants that had no previous dodder attachment; dodder-removed plants that had an initial dodder seedling attached, removed and left in the same pot to simulate parasite death; and dodder-continuous plants with an initial dodder seedling that remained attached. In the second experiment, we tested the effects of previous caterpillar damage (Spodoptera exigua) and mechanical damage on future dodder attachment on tomato hosts. Dodder attached most slowly to tomato hosts that had dodder plants previously attached and then removed, compared to control plants or plants with continuous dodder attachment. In contrast, herbivory did not affect subsequent dodder attachment rate. These results indicate that dodder preference depended on the identity and the outcome of the initial attack, suggesting that early-season interactions have the potential for profound impacts on subsequent community dynamics.

Fig 1. Differences in attachment rate of the initial dodder seedlings on 6 tomato cultivars.

Lines shows proportion of dodder seedling attachment at each time point. Cultivar ‘H5608’ had significantly higher attachment rate compared to other cultivars (|Z| > 4.10, P < 0.001 for all).

Fig 2. Effects of prior dodder treatment on the attachment rate of a second dodder parasite across 3 tomato cultivars.

Lines indicate proportion of dodder seedling attachment at each time point. The ‘continuous attachment’ treatment line stops at day 4 because all dodder that did not attach by this point had died. Plants with the initial dodder removed had significantly lower attachment rate compared to control (Dodder-removed: hazard ratio vs control = 0.48, Z = -2.96, P = 0.0031) and plants with continuous dodder attachment (Dodder-continuous: hazard ratio vs control = 0.97, Z = -0.13, P = 0.900).

Fig 3. Effects of prior herbivory on the attachment rate of dodder plants on the ‘H5608’ tomato cultivar.

Lines indicate proportion of dodder seedling attachment at each time point. There were no significant differences between treatments (Herbivory: hazard ratio vs. control = 1.10, Z = 0.36, P = 0.72; Mechanical: hazard ratio vs. control = 1. 14, Z = 0.51, P = 0.62).