Effect of Plant Toughness, Calcification, and Chemistry on Herbivory by Dolabella Auricularia

Abstract

Most studies of feeding preferences of herbivores have focussed on the role of plant secondary metabolites; very few studies have experimentally tested the importance of plant toughness or calcification as feeding deterrents, although low preference has repeatedly been shown to correlate with these factors. Feeding preferences of the unusual generalist herbivore Dolabella auricularia, an opisthobranch gastropod which, like many other herbivores of that group, sequesters secondary metabolites from some algae, were consistent with our expectation that they might not feed on algae and seagrasses that were tough, calcified, or chemically rich. We experimentally examined the importance of each of these three features in deterring feeding by Dolabella. Consumption of plants by Dolabella was negatively correlated with plant toughness, as determined by penetrometer measurements. Given a choice between two species of plants, Dolabella always preferred the softer of the pair. However, when both species were ground up and incorporated into soft carrageenan cakes, Dolabella were significantly less selective in 3 of 4 cases where the tougher plant had no other known line of defense, and in 1 of 3 cases where the tougher plant also had chemical or CaCO 3 defenses. Frondose calcified algae on Guam are ≥50% CaCO 3 by dry mass. CaCO 3 deterred Dolabella feeding at concentrations of 28 and 50% of dry mass, but not at 16%. CaCO 3 occurs in algae in two crystal structures, calcite and aragonite; both deterred Dolabella feeding. CaCO 3 and chemical defenses of Halimeda macroloba did not interact synergistically to enhance effectiveness. Dolabella feeding was not deterred by organic extracts from most plants, even when offered at very high concentrations. Extracts from many of these plants had previously been shown to deter feeding by fishes at lower concentrations. Of the 12 plants tested, Dolabella feeding was deterred only by extracts from Caulerpa racemosa, Hormothamnion enteromorphoides, and Halimeda macroloba. We isolated and tested the two major metabolites of Caulerpa, caulerpenyne and caulerpin, and identified caulerpenyne as the deterrent agent. These results indicate that Dolabella are relatively unaffected by chemical defenses and yet are deterred by other plant defenses such as calcification and toughness. The fact that Dolabella can sequester algal secondary metabolities may explain Dolabella's relative indifference to chemically rich plant extracts.