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 (13C and 15N) 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.