Complex Consequences of Herbivory and Interplant Cues in Three Annual Plants

Abstract

Information exchange (or signaling) between plants following herbivore damage has recently been shown to affect plant responses to herbivory in relatively simple natural systems. In a large, manipulative field study using three annual plant species (Achyrachaena mollis, Lupinus nanus, and Sinapis arvensis), we tested whether experimental damage to a neighboring conspecific affected a plant's lifetime fitness and interactions with herbivores. By manipulating relatedness between plants, we assessed whether genetic relatedness of neighboring individuals influenced the outcome of having a damaged neighbor. Additionally, in laboratory feeding assays, we assessed whether damage to a neighboring plant specifically affected palatability to a generalist herbivore and, for S. arvensis, a specialist herbivore. Our study suggested a high level of contingency in the outcomes of plant signaling. For example, in the field, damaging a neighbor resulted in greater herbivory to A. mollis, but only when the damaged neighbor was a close relative. Similarly, in laboratory trials, the palatability of S. arvensis to a generalist herbivore increased after the plant was exposed to a damaged neighbor, while palatability to a specialist herbivore decreased. Across all species, damage to a neighbor resulted in decreased lifetime fitness, but only if neighbors were closely related. These results suggest that the outcomes of plant signaling within multi-species neighborhoods may be far more context-specific than has been previously shown. In particular, our study shows that herbivore interactions and signaling between plants are contingent on the genetic relationship between neighboring plants. Many factors affect the outcomes of plant signaling, and studies that clarify these factors will be necessary in order to assess the role of plant information exchange about herbivory in natural systems.

Do plant–plant signals mediate herbivory consistently in multiple taxa and ecological contexts?

“…In a recent study (Pearse et al 2012), damage to a neighboring plant appeared to induce susceptibility in a focal plant. In a large field experiment with three grassland forbs (Sinapis arvensis, Lupinus nanus, and Achyrachaena mollis), one species (A. mollis) experienced greater damage when next to a wounded conspecific neighbor, and this led to a delayed flower production, lower biomass accumulation, and ultimately a lower fruit set (Pearse et al 2012).…”

“…There is good reason to expect that the effects of plantÁplant signaling should be varied across plant groups and ecological settings ( Figures 1 and 2 following Pearse et al 2012). Much of the current evidence suggests a fairly simple link between damage experienced by a neighboring (emitter) plant and the potential fitness consequences for its neighbor (receiver) plants (Figure 1).…”

“…Ecological studies have shown that plantÁplant signals can affect rates of herbivory (Karban et al 2006;Heil & Silva Bueno 2007) as well as plant fitness (Karban & Maron 2002;Karban et al 2012). At the same time, plausible evolutionary scenarios that might lead to plantÁplant signaling have been explored (Heil & Karban 2010), such as the possibility of self-induction (Heil & Silva Bueno 2007;Karban & Shiojiri 2009) or protection of close relatives (Pearse et al 2012).…”

“…While the number of taxa examined has been few, they represent multiple plant growth forms including trees, shrubs, vines, grasses, and forbs (Heil & Karban 2010). On the flip side, there have been very few reports from studies that find no effect (Fowler & Lawton 1985;Julkunen-Tiitto et al 1995) or counterintuitive effects (Pearse et al 2012) of neighbor induction on defensive traits or herbivory. The lack of null or complicated results about herbivore-induced plantÁplant signaling may either indicate that there is little variation in the effect of neighbor induction or may simply represent a publication bias in which studies that find results that fit the current model of herbivore-induced plantÁ plant signaling are reported, but those that do not are discarded Á an issue that would be similar to trends that arose in studies of inducible resistance (Nykanen & Koricheva 2004).…”

Genotypic recognition and spatial responses by rice roots

“…Aboveground tissues may identify volatile cues that provide information about their neighbors (3,4) and detect irradiance, directional light, and light quality (5), whereas belowground tissues, such as roots, can detect changes in soil moisture, nutrient availability, and physical obstacles (6)(7)(8). Plants not only detect but also respond to changes in their environment, exhibiting adaptation in their morphology and physiology in response to environmental stimuli (9)(10)(11)(12)(13)(14), such as alteration in total root length, root system volume, and root depth (15,16).…”