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Hay,
Mark E.
Hay,
Mark E.
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ItemCan small rare prey be chemically defended? the case for marine larvae(Georgia Institute of Technology, 1995-06) Lindquist, Niels Lyle ; Hay, Mark E.Marine larvae are consumed by a wide variety of generalist fishes and particle—feeding invertebrates, but larvae of any particular species probably constitute a small and variable of the diet for these consumers. Because virtually all consumers can ingest small quantities of noxious compounds with minimal detrimental effects, it is uncertain that toxic chemicals in larvae could be consumed in quantities sufficient to select for predator recognition and avoidance. Despite this, chemically defended larvae do occur. We show that, at low doses, secondary metabolites (the didemnins) from adults and larvae of the Caribbean tunicate Trididemnum solidum induced vomiting in fish, resulting in rapid learned aversion of the didemnin—defended food. The particle—feeding anemone Aiptasia pallida did not learn to avoid the chemically defended food. When anemones ingested the chemical equivalent of 15 larvae/d, representing <2% of the mass of their total daily diet, the didemnins in the "larvae" significantly reduced: (1) growth of adults by 82%, (2) combined growth of adults and daughter clones by 76%, (3) production of daughter clones by 44%, and (4) average mass of individual daughter clones by 41%. At higher water temperatures, anemones cloned more rapidly, but the negative effects of consuming didemnins also occurred more rapidly. Significant differences in the number of daughter clones produced between treatment and control anemones occurred after only 4 d at seawater temperatures of 27°—29°C vs. 32 d at seawater temperatures of 18°—21°C. Thus consumption of even very small quantities of secondary metabolites can decrease consumer fitness substantially and select for predators that recognize and avoid chemically defended larvae, as do many consumers that co—occur with Trididemnum solidum larvae. This is the first rigorous demonstration that consumption of marine secondary metabolites can decrease consumer fitness when ingested at ecologically realistic doses.
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ItemDistribution, density, and sequestration of host chemical defenses by the specialist nudibranch Tritonia hamnerorum found at high densities on the sea fan Gorgonia ventalina(Georgia Institute of Technology, 1995-03-23) Cronin, Greg ; Hay, Mark E. ; Fenical, William ; Lindquist, Niels LyleThe dendronotid nudibranch Tritonia hamnerorum was observed on some reefs in the Florida Keys, USA, at very high densities during the summer of 1992. T. hamnerorum specializes on the sea fan Gorgonia ventalina and sequesters the furano-germacrene julieannafuran from its host; this compound effectively protects the nudibranch from consumption by the common predatory reef fish Thalassoma bifasciatum. T. hamnerorum densities were extremely high at some locations, with as many as 1700 nudibranchs found on a single G. ventalina colony. At high densities, nudibranch feeding killed large areas on some sea fan colonies by stripping all tissue from portions of the sea fan and allowing filamentous algae and other epibionts to colonize. The density of T. hamnerorum on G. ventalina varied greatly on scales of centimeters, meters and kilometers. High density patches of nudibranchs on individual sea fans were usually composed of equivalent-sized nudibranchs. These observations suggest that pelagic veligers have an incredible capability to find and settle synchronously on one portion of a sea fan or that the larvae or juveniles hatch from egg masses and develop without leaving the sea fan. This study adds to a growing number of marine examples suggesting that feeding specialization occurs primarily among small, sedentary consumers that deter or escape predators by associating with defended hosts.
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ItemEffects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis(Georgia Institute of Technology, 1995-03-23) Cronin, Greg ; Lindquist, Niels Lyle ; Hay, Mark E. ; Fenical, WilliamInvestigations focused on the ecological roles of marine secondary metabolites have become common, but marine ecologists have rarely assessed how methodologies used in sample preparation affect the extractability and stability of secondary metabolites and, thus, measurements of intraspecific and interspecific compound variance. We assessed various procedures for storing, drying, and extracting samples of 2 chemically defended brown seaweeds Dictyota ciliolata and D. menstrualis. These plants contain the diterpenoid alcohols pachydictyol A, dictyol B acetate, and dictyol E that are relatively stable under all test conditions. In contrast, the related diterpenoid dialdehyde, dictyodial, decomposed when plant tissues or crude extracts were stored at -25°C for 13 to 27 wk or when tissues or extracts were freeze-dried or subjected to high vacuum (<0.01 torr), methods that are commonly used in studies of marine chemical ecology. The stability of dictyodial was species-specific, degrading more in D. ciliolata than in D. menstrualis. During a few extractions, dictyodial reacted with methanol (MeOH) to yield an artifact resulting from the addition of 2 molecules of MeOH per molecule of dictyodial. A mixture of 2:1 dichloromethane (DCM) and MeOH tended to extract the lipophilic secondary metabolites better than MeOH or DCM alone. Metabolites were also afforded some protection against degradation when fresh tissue was submerged in 2:1 DCM:MeOH during storage at -25°C. Results of this investigation indicate that storage, extraction, and quantification methods need to be optimized for analyses of individual compounds and that even identical compounds can behave differently when they occur in different species.
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ItemConstraints on chemically-mediated coevolution: multiple functions for seaweed secondary metabolites.(Georgia Institute of Technology, 1995-01) Schmitt, Tim M. ; Hay, Mark E. ; Lindquist, Niels LyleDiterpene alcohols produced by the brown seaweed Dictyota menstrualis deter feeding by numerous species of abundant herbivores. Here we show that these same compound also may prevent fouling organisms from colonizing the surface of this alga. In the field, Dictyota menstrualis plants were less frequently and less heavily fouled than any of the other common seaweed species investigated. In laboratory assays, larvae of the common fouling bryozoan Bugula neritina failed to settle on Dictyota even though they contacted its surface as often as they contacted the surface of a preferred host alga. Rejection occurred only after direct contact with the alga's surface. Rejection of Dictyota was not mediated by water—borne chemical cues or by surface wettability (a physical property of the surface that can affect fouling). The lipid—soluble extract from surface rubbings of Dictyota inhibited larval settlement when placed on other surfaces and contained the diterpene alcohols pachydictyol A and dictyol E. Larvae exposed to these compounds experienced mortality, abnormal development, or reduced rates of development. Although the potential for chemically mediated coevolution between plants and herbivores has been the focus of scores of previous investigations, such coevolution will depend on selection altering the chemical defenses of the plant following the evolution of resistance by herbivores. Such a reciprocal response will be constrained if compounds play multiple roles that are ecologically important. Dictyota produces secondary metabolites that are broadly defensive against a wide variety of consumers and fouling organisms. Although certain consumers may evolve resistance to these metabolites, it is unclear that feeding by these consumers will result in reciprocal responses from the plant. We suggest that coevolved interactions may be uncommon, and that many interactions that appear to be coevolved may result from fortuitous and opportunistic preadaptations.
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ItemDefense of ascidians and their conspicuous larvae: adult vs. Larval chemical defenses(Georgia Institute of Technology, 1992-12) Lindquist, Niels Lyle ; Hay, Mark E. ; Fenical, WilliamPrevious 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.