Prey Nutritional Quality Interacts With Chemical Defenses to Affect Consumer Feeding and Fitness

Abstract

Numerous studies have assessed the individual effects of prey nutritional quality or chemical defenses on consumer feeding behavior. However, little is known about how these traits interact to affect consumer feeding and performance. We tested the separate and interactive effects of prey chemical defenses and nutritional quality on the feeding behavior and fitness of six sympatric crustacean mesograzers. Natural concentrations of diterpene alcohols (dictyols) from the brown alga Dictyota menstrualis were incorporated, or not incorporated, into lower quality and higher quality foods to create artificial diets mimicking prey of variable value and defense. Five amphipods (Ampithoe longimana, A. valida, Cymadusa compta, Gammarus mucronatus, and Elasmopus levis) and one isopod (Paracerceis caudata), representing a continuum of closely to distantly related organisms, were fed intact algae or lower and higher quality diets containing or lacking dictyols. All six mesograzers preferred the green alga Enteromorpha intestinalis to the dictyol producing alga Dictyota menstrualis. In assays allowing consumers to choose between simultaneously available foods, dictyols deterred feeding by all five amphipods, but not the isopod; this occurred for both lower and higher quality foods. In no-choice assays, where consumers were confined with only one of our four treatment diets, effects on feeding became more complex. Nutritional quality alone affected feeding by five of the six species. These grazers compensated for lower quality by increasing consumption. Dictyols suppressed feeding for four of the six species. More interestingly, there were significant dictyol ϫ quality interactions for three species. Dictyols decreased feeding more when placed in lower quality foods than higher quality foods. Two amphipods deterred by dictyols in the choice assays readily consumed dictyolcontaining foods in no-choice situations and suffered few negative effects of doing so. Although all amphipods were deterred by dictyols in choice assays, dictyols decreased fitness (survivorship, growth, or reproduction) for only four of the five species. These effects included large and immediate decreases in survivorship, dramatic effects on reproduction, and modest effects on female growth. Dictyols enhanced survivorship of the isopod. Thus, the effects of secondary metabolites on feeding in choice situations vs. fitness in long-term assays were inconsistent. For three amphipods, certain effects of food quality, dictyols, or their interaction were detected only for females. In general, negative effects of dictyols on fitness were greater in lower than in higher quality foods, suggesting that prey nutritional value may counteract the effects of defensive metabolites. For example, when G. mucronatus consumed dictyols in lower quality foods, mortality was Ͼ80% by day 5; for dictyols in higher quality foods, 80% mortality took 28 days to develop. Lower quality foods alone significantly decreased growth for the isopod, three of the amphipods, and the females of a...

Chemical mediation of interactions among marine organisms

“…Targett and Arnold 171 review the effects of secondary metabolites on digestion in marine herbivores. A recent study by Cruz-Rivera and Hay 70 examined the separate and interactive effects of prey nutritional quality and chemical defenses on feeding behavior and overall performance of six different crustacean consumers (5 amphipods, 1 isopod). The chemical defenses tested were the dictyol diterpenes, pachydictyol A 13 and dictyol E 14, of Dictyota menstrualis.…”

“…Low nutritional quality alone negatively influenced fecundity and growth of most species of consumers. Cruz-Rivera and Hay 70 stress the importance of studying the interactive effects of chemical defenses and prey nutritional characteristics for understanding food selection by consumers.…”

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

“…Are aquatic herbivores more likely to experience synergistic chemical consequences when they than terrestrial herbivores? Have ecologists overlooked the consequences of inadvertently consuming cryptic toxins from small epiphytes living on larger plants (Cruz-Rivera and Hay, 2003;Sotka et al, 2009) by focusing only on host plant traits (Porras-Alfaro and Bayman, 2011)?…”

“…Although both nutrients and secondary metabolites influence foraging behavior, there is a general lack of ability to a priori predict diet selection even when the nutritional and chemical profiles of available plants are well documented (Clements et al, 2009;Cruz-Rivera and Hay, 2003;Kool, 1992;Sotka et al, 2009;Yeager et al, 1997).…”

“…Another reason is that researchers tend to regard nutrients as "therapeutic" components that always result in positive consequences whereas PSMs are considered "toxic" components with inevitable negative repercussions. As such, PSMs (Cruz-Rivera and Hay, 2003;Duffy and Paul, 1992;Felton et al, 2009;Van Alstyne et al, 2009), in others, PSMs are more important (Dearing et al, 2000;Erhard et al, 2007), and in still other cases, these factors are equally important or act synergistically to influence foraging behavior (Duffy and Paul, 1992;Frye et al in press, Simpson and Raubenheimer, 2001). While approaches, such as the geometric framework, have helped researchers study how herbivores regulate nutrient needs in variable nutritional and PSM environments (Behmer, 2009), what remains poorly understood is why certain species respond to specific thresholds of PSMs or nutrients and others do not.…”