Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis.

Recent evidence suggests that competitive interactions among herbivores are mostly indirect and mediated by plant responses to herbivory. Most studies, however, emphasize chewing insects and secondary chemistry, thus ignoring the diverse group of vascular-parasites that may be more likely to compete through induced changes in phytonutrients. Using an aboveground phloem-feeding aphid (Myzus persicae) and a belowground gall-forming nematode (Meloidogyne incognita) on tobacco plants, we assessed the importance of competition via induced host-plant sinks. In a series of experimental trials, nematode root herbivory caused 55 and 72% declines in the growth and fecundity of aphids, respectively. Aphids, on the other hand, did not impact nematode performance. Therefore, we predicted that nematodes out-compete M. persicae by attenuating the magnitude of aphid-induced sinks. Through a combination of invertase enzyme measurements and stable isotope ((13)C and (15)N) enrichment, we found evidence that both herbivores act as mobilizing sinks. Aphids attracted photoassimilates to feeding aggregations on leaves and nematode galls accumulated resources in the roots. Levels of invertase enzymes, for example, were more than fourfold higher in nematode galls than in surrounding root tissue. Yet we found no evidence supporting a sink competition model for aphid-nematode interactions. The strength of aphid-induced leaf sinks was entirely unaffected by nematode presence, and vice versa. Thus, induced host-plant sinks appear to be a common strategy employed by vascular parasites to manipulate the physiology of their host, but multi-sink competition may be limited to herbivores that co-occur on the same tissue type and/or plants under growth-limited abiotic conditions.

Effects of plant vascular architecture on aboveground-belowground-induced responses to foliar and root herbivores on Nicotiana tabacum.

Herbivores induce systemic changes in plant traits, and the strength of these induced responses is often associated with the degree of vascular connectivity that links damaged and undamaged plant tissues. Although this phenomenon is known to occur aboveground in leaves, it is unknown whether or not leaf-root induction similarly follows the vascular architecture of plants. To test for this possibility, we manipulated foliar and root herbivory on tobacco (Nicotiana tabacum) by the leaf-chewing insect Spodoptera exigua and the root-galling nematode Meloidogyne incognita. Subsequent changes in secondary chemistry (alkaloids and phenolics) were measured in leaves and roots that were orthostichous (vertically aligned) and nonorthostichous (opposite) from the herbivore-damaged tissues. Aboveground caterpillar herbivory elicited stronger secondary chemical responses in orthostichous compared with nonorthostichous plant tissues, although the magnitude of this difference was greater in leaves than roots. However, belowground nematode herbivory did not affect the secondary chemistry of tobacco leaves, despite inducing strong local responses in roots. Thus, plant vascular architecture can mediate the magnitude of systemic induction in roots as well as in leaves, with stronger responses in tissues that are more closely aligned. As a result, herbivores that co-occur on the same sector of plant (both aboveground and belowground) may be more likely to affect one another via induced responses than herbivores that occur on plant tissues sharing fewer resources.

Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory.

Roots play a critical, but largely unappreciated, role in aboveground anti-herbivore plant defense (e.g. resistance and tolerance) and root-leaf connections may therefore result in unexpected coupling between above- and belowground consumers. Using the tobacco (Nicotiana tabacum) system we highlight two examples of this phenomenon. First, the secondary metabolite nicotine is produced in roots, yet translocated aboveground for use as a foliar resistance trait. We demonstrate that nematode root herbivory interferes with foliar nicotine dynamics, resulting in positive effects on aboveground phytophagous insects. Notably, nematode-induced facilitation only occurred on nicotine-producing plants, and not on nicotine-deficient mutants. In the second case, we use stable isotope and invertase enzyme analyses to demonstrate that foliar herbivory elicits a putative tolerance response whereby aboveground nutritional reserves are allocated to roots, resulting in facilitation of phytoparasitic nematodes. Thus, plants integrate roots in resistance and tolerance mechanisms for leaf defense, and such root-leaf connections inherently link the dynamics of above- and belowground consumers.

Constitutive and induced defenses to herbivory in above- and belowground plant tissues.

A recent surge in attention devoted to the ecology of soil biota has prompted interest in quantifying similarities and differences between interactions occurring in above- and belowground communities. Furthermore, linkages that interconnect the dynamics of these two spatially distinct ecosystems are increasingly documented. We use a similar approach in the context of understanding plant defenses to herbivory, including how they are allocated between leaves and roots (constitutive defenses), and potential cross-system linkages (induced defenses). To explore these issues we utilized three different empirical approaches. First, we manipulated foliar and root herbivory on tobacco (Nicotiana tabacum) and measured changes in the secondary chemistry of above- and belowground tissues. Second, we reviewed published studies that compared levels of secondary chemistry between leaves and roots to determine how plants distribute putative defense chemicals across the above- and belowground systems. Last, we used meta-analysis to quantify the impact of induced responses across plant tissue types. In the tobacco system, leaf-chewing insects strongly induced higher levels of secondary metabolites in leaves but had no impact on root chemistry. Nematode root herbivores, however, elicited changes in both leaves and roots. Virtually all secondary chemicals measured were elevated in nematode-induced galls, whereas the impact of root herbivory on foliar chemistry was highly variable and depended on where chemicals were produced within the plant. Importantly, nematodes interfered with aboveground metabolites that have biosynthetic sites located in roots (e.g., nicotine) but had the opposite effect (i.e., nematodes elevated foliar expression) on chemicals produced in shoots (e.g., phenolics and terpenoids). Results from our literature review suggest that, overall, constitutive defense levels are extremely similar when comparing leaves with roots, although certain chemical classes (e.g., alkaloids, glucosinolates) are differentially allocated between above- and belowground parts. Based on a meta-analysis of induced defense studies we conclude that: (1) foliar induction generates strong responses in leaves, but much weaker responses in roots, and (2) root induction elicits responses of equal magnitude in both leaves and roots. We discuss the importance of this asymmetry and the paradox of cross-system induction in relation to optimal defense theory and interactions between above- and belowground herbivory.