Watercress allelochemical defends high-nitrogen foliage against consumption: Effects on freshwater invertebrate herbivores

Watercress (Nasturtium officinale) is a spring-stream macrophyte that possesses glucosinolates, which are hydrolyzed to feeding deterrent isothiocyanates when the enzyme myrosinase is released by tissue damage. Previous studies indicated that frequently associated aquatic shredders strongly prefer yellowed-senescent leaves over fresh-green foliage, because the latter releases much more isothiocyanate than senescent watercress. When the action of myrosinase was blocked by heating the tissue, the shredders\u27 preference shifted to heated-green tissue, which contains much more nitrogen than that found in senescent tissue. Here we report a series of no-choice experiments on various tissue types designed to determine intermediate and long-term consumption rates and associated impacts on growth and survival of shredders associated with watercress. The amphipod Gammarus pseudolimnaeus, the caddisflies Pycnopsyche sp., Hesperophylax designatus, and Limnephilus sp., and the snail Physella gyrina, all consumed much more senescent than fresh-green tissue. In long-term tests with G. pseudolimnaeus, H. designatus, and Limnephilus sp., growth was negative or zero on the defended fresh-green tissue and often highest on heated-green tissue. Reaction to glucosinolates differed among shredders. For the caddisflies, growth and survival were positively correlated with bulk tissue and nitrogen consumption, which were highest for heated-green tissue. However, amphipod survival was significantly lowered on heated-green watercress, although it was readily consumed. Therefore, consumption of high-glucosinolate tissue was detrimental to the amphipods but not to caddisflies. Our results indicate that the glucosinolate-myrosinase system defends live green watercress against herbivory by an array of aquatic invertebrates. These generalist herbivores forgo eating high-quality fresh-green leaves because of plant defenses and instead settle for lower quality senescent leaves. When the defense system was experimentally shut down, these herbivores readily consumed young green tissue and frequently showed higher growth rates than those achieved on the senescent, but undefended, leaves they typically consume. Evidently, these shredders face a trade-off of high nitrogen and high defense vs. low nitrogen and low defense