Title:
Defense of ascidians and their conspicuous larvae: adult vs. Larval chemical defenses
Defense of ascidians and their conspicuous larvae: adult vs. Larval chemical defenses
Author(s)
Lindquist, Niels Lyle
Hay, Mark E.
Fenical, William
Hay, Mark E.
Fenical, William
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Abstract
Previous investigations, focused primarily on vertebrates, have noted substantial losses of eggs and embryos to predators and questioned why selection has not more commonly resulted in the evolution of chemically defended eggs or embryos. Hypotheses regarding the apparent rarity of such defenses have emphasized the potential incompatibility of actively developing tissues and toxic metabolites. Alternatively, this apparent pattern could be an artifact of our greater knowledge of vertebrates, which in general show few tendencies for synthesizing defensive metabolites in either juvenile or adult stages. In this study, we investigated adult and larval chemical defenses of a group of benthic marine invertebrates, the ascidians, in which the adults are often chemically rich, and we contrast our findings with what is known about chemical defenses of eggs and embryos from terrestrial and aquatic organisms. Our findings suggest that there is no fundamental incompatibility of rapidly developing juvenile tissues and bioactive metabolites, and that chemically defended eggs and larval stages may be common among some taxonomic groups. Ascidians are benthic invertebrates that often lack apparent physical defenses against predation, yet are common on coral reefs where predation by fishes is intense. In contrast to most co—occurring invertebrates, many ascidians also release large, conspicuous larvae during daylight hours when exposure to fish predation would be highest. Thus selection by predators might favor the evolution of distasteful larvae. In situ observations indicate that many conspicuous ascidian larvae are distasteful to potential consumers. We investigated the ability of secondary metabolites produced by taxonomically diverse ascidians from geographically distant locales to deter predation on both adults and larvae. Larvae from the Caribbean ascidian Trididemnum solidum were distasteful to reef fishes, and when organic extracts of individual larvae were transferred onto eyes of freeze—dried krill (a good larval mimic in terms of size and color), these eyes were rejected by fishes while control eyes (solvent only) were readily eaten. Larvae of the Indo—Pacific ascidian Sigillina cf. signifera were also distasteful to coral—reef fishes and contained the unpalatable bipyrrole alkaloid tambjamine C. When added to artificial foods at or below their natural mean concentrations and offered to consumers in field and laboratory feeding assays, the secondary metabolites produced by Trididemnum solidum (Caribbean Sea), Sigillina cf. signifera (Indo—Pacific), and Polyandrocarpa sp. (Gulf of California) significantly deterred feeding by co—occurring fishes and invertebrates. Secondary metabolites produced by Trididemnum cf. cyanophorum from the Caribbean Sea, Lissoclinum patella from the Indo—Pacific, and Aplidium californicum from the temperate Pacific, and the small stellate spicules common to many tropical didemnid ascidians did not significantly affect fish feeding. High—pressure liquid chromatography (HPLC) analyses of six didemnin cyclic peptides in individual colonies of Trididemnum solidum from one patch reef at Little San Salvador, Bahamas found large inter—colony differences in their concentrations. The mean concentration of didemnin B was more than double the concentration needed to significantly deter fish feeding in our field assays, and feeding tests with nordidemnin B showed that it deterred fish feeding across the entire range of natural concentrations. HPLC analysis of the extract from a combined collection of T. solidum larvae found adequate concentrations of didemnin B and nordidemnin B to account for their rejection by foraging fishes. We demonstrate that taxonomically diverse ascidians from habitats characterized by intense predation pressure produce secondary metabolites that significantly reduce predation on both adults and larvae, and suggest that this defensive chemistry may be crucial in allowing the release of large, well—provisioned larvae during daylight periods when larvae have the greatest probability of using photic cues to select physically appropriate settlement sites. Production of defensive secondary metabolites appears widespread among certain groups of ascidians, some of which are also known to concentrate acid and heavy metals as additional defensive strategies.
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Date Issued
1992-12
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