Preliminary evidence that the feeding rates of generalist marine herbivores are limited by detoxification rates

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CHEMOECOLOGY

RESEARCH PAPER

Preliminary evidence that the feeding rates of generalist marine herbivores are limited by detoxification rates Erik E. Sotka • Jacob Gantz

Received: 5 March 2013 / Accepted: 23 May 2013 Ó Springer Basel 2013

Abstract Herbivores tend to increase feeding rate and fitness when consuming a mixed diet relative to a single diet. According to the detoxification limitation hypothesis (DLH), feeding choices and rates when confronted with chemically rich plants are determined by herbivore physiology, and specifically by the metabolic pathways that herbivores use to manipulate secondary metabolites. We tested two predictions of the DLH using two generalist herbivores, the urchin Arbacia punctulata and amphipod Ampithoe longimana. These herbivores have geographic ranges which overlap with brown seaweeds that produce diterpenes (Dictyota menstrualis, D. ciliolata) and a green seaweed that produces sesquiterpenes and diterpenes (Caulerpa sertularioides). As predicted by the DLH, herbivore consumption rates in no-choice feeding assays were limited by extract intake rates. This suggests an upper limit in the herbivores’ abilities to physiologically manipulate seaweed metabolites. Contrary to a second prediction of the DLH, urchins consumed equal amounts of foods coated with limiting concentrations of two seaweed extracts offered singly, as a mixture, or as a pairwise choice. This result suggests that secondary metabolites of these seaweeds are manipulated by a linked set of detoxification pathways. Improving our understanding of the mechanisms that underlie diet mixing depends on greater attention to the physiology of herbivore resistance to secondary metabolites.

E. E. Sotka (&)  J. Gantz Department of Biology and the Grice Marine Laboratory, College of Charleston, 205 Fort Johnson Road, Charleston, SC 29412, USA e-mail: [email protected]

Keywords Marine seaweed–herbivore interactions  Plant secondary metabolites  Generalist diets  Foraging

Introduction Generalist herbivores play central roles in regulating and structuring ecosystems, determining spatial patterns of biodiversity, and the cycling of nutrients and materials through ecosystems (Stachowicz et al. 2007; Stephens et al. 2007). Many terrestrial (Novotny et al. 2002) and most marine herbivores (Poore et al. 2008) are generalists, and several studies demonstrate that generalist herbivores actively seek a mixed diet (e.g., Horn 1983; Kitting 1980; Lyons and Scheibling 2007; Pennings et al. 1993). Consumption of a mixed diet tends to increase overall feeding rates and can increase overall herbivore performance (growth, survival or fecundity) relative to single-species diets, although performance on the best single-species diet can match performance on mixed diets (see review by Stachowicz et al. 2007; Cruz-Rivera and Hay 2000; Hemmi and Jormalainen 2004; Lobel and Ogden 1981; Pennings et al. 1993; Scheibling and Anthony 2001; Steinberg and van Altena 1992). Marine and terrestrial plants produce secondary metabolites (Sotka et al. 2009)