Watercress Allelochemical Defends High‐Nitrogen Foliage Against Consumption: Effects on Freshwater Invertebrate Herbivores

Abstract

Watercress (Nasturtium officina/e) 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' 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 heatedgreen 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.

Chemical Defense in Elodea nuttallii Reduces Feeding and Growth of Aquatic Herbivorous Lepidoptera

“…Omnivores or shredder herbivores accept various artificial diets (Lodge 1991;Newman et al 1996;. The specialized feeding habits of invertebrates challenges the design of suitable artificial diets .…”

“…In general, nitrogen content is considered the major nutrient determining food quality of plants, and many Lepidoptera prefer plants with the highest nitrogen content (White 1993;Newman et al 1996). Phosphorus may also limit the growth of Lepidoptera larvae (Perkins et al 2004).…”

“…Several aquatic angiosperms contain alkaloids (Ostrofsky and Zettler 1986), and watercress tissue is protected by glucosinolates (Newman et al 1996), both groups of secondary metabolites known as potent feeding deterrents in terrestrial plants. Hydrolyzable polyphenols present in M. spicatum possibly affect the growth of Acentria larvae Walenciak et al 2002), but larvae still develop into pupae and adults.…”

A Pharm-Ecological Perspective of Terrestrial and Aquatic Plant-Herbivore Interactions

“…As such, observations of temporal and spatial variation in feeding by herbivores could be a result of temporal and spatial variation in concentrations of PSMs. For example, mammalian herbivores select specific trees (Degabriel et al, 2009;Moore and Foley, 2005;Moore et al, 2010) and aquatic herbivorous invertebrates select specific tissue types (Newman et al, 1996) to avoid consequences of toxic PSMs. To add to dietary complexity, feeding by herbivores can influence the concentration and distribution of both chemicals and nutrients.…”

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“…Biomass loss of macrophytes (Lodge et al, 1998) and even changes in macrophyte community composition due to herbivory by both vertebrate and invertebrate (Johnson et al, 1998;Gross et al, 2001) herbivores have been reported. In the last decade, many studies have shown that chemical defenses of freshwater macrophytes are important, occurring as frequent as in marine or terrestrial macrophytes (Newman et al, 1996;Bolser et al, 1998;Wilson et al, 1999;Kubanek et al, 2000).…”