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Author: Hay, Mark E. × Author: Lindquist, Niels Lyle × End date: 1996 × Start date: 1995 × Has files: Yes × Type: Text ×

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Palatability and chemical defenses of marine invertebrate larvae

1996-11 , Lindquist, Niels Lyle , Hay, Mark E.

Risk of larval mortality is a critical component of models and debates concerning the ecology and evolution of the differing reproductive characteristics exhibited by marine invertebrates. In these discussions, predation often is assumed to be a major source of larval mortality. Despite limited empirical support, most marine larvae are thought to be palatable and broadly susceptible to generalist predators. Previous studies of larval—planktivore interactions have focused primarily on larvae that typically feed, grow, and develop for weeks to months in the plankton. Such planktotrophic species commonly produce large numbers of small larvae that disperse over vast distances. In contrast, the nonfeeding lecithotrophic larvae from sessile invertebrates that brood are often large and conspicuous, lack morphological defenses, and have limited dispersal distances because they typically are competent to settle minutes to hours after spawning. Interactions between lecithotrophic larvae and consumers are not well studied. This has limited the ability of previous authors to test broad generalities about marine larvae. We show that brooded larvae of Caribbean sponges (11 species) and gorgonians (three species) as well as brooded larvae of temperate hydroids (two species) and a bryozoan are unpalatable to co—occurring fishes. In contrast, brooded larvae of temperate ascidians (three species), a temperate sponge, and Caribbean hard corals (three species) are readily consumed by fishes, as are larvae from four of six species of synchronous broadcast—spawning gorgonians from the Florida Keys. Frequencies of survivorship for larvae attacked and rejected by fishes were high and statistically indistinguishable from frequencies for unattacked control larvae. Frequency of metamorphosis (when it occurred) of rejected larvae never differed significantly from that of unattacked control larvae. Assays testing for larval vs. adult chemical defenses for five species with distasteful larvae showed that larvae of all five species were chemically distasteful to fishes, whereas only three of five adult extracts deterred fish feeding. A comparison of larval palatability among chemically rich taxa showed that brooded larvae were significantly more likely to be unpalatable (86% of the species tested) than larvae of broadcasters (33%), and that palatable larvae were rarely released during the day (23%) while unpalatable larvae usually were (89%). Additionally, the frequency of bright coloration was high (60%) for unpalatable larvae and low (0%) for palatable larvae, suggesting that unpalatable larvae often may be aposematically colored. Results of this broad survey cast doubt on the widely accepted notion that virtually all marine larvae are suitable prey for most generalized planktivores. Among species that do not chemically or physically protect larvae against fishes, selection appears to favor the release of larvae at night, or the production of smaller more numerous offspring that grow and develop at sea as a way of escaping consumer—rich benthic habitats. Because distasteful larvae are not similarly constrained, distasteful species should exhibit reproductive and larval characteristics selected more by the fitness—related consequences of larval development mode and dispersal distance than by the necessity of avoiding benthic predators. Production of large larvae and retention of offspring in parental habitats that have proved to be suitable for growth and reproduction have both been proposed as advantageous, but these advantages often were assumed to be offset by losses due to increased larval apparency to fishes. This assumed trade—off is not mandatory because larvae can be defended chemically. Distasteful larvae tend to be conspicuous, localized dispersers that can co—occur with benthic fishes, and yet not be consumed.

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Effects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis

1995-03-23 , Cronin, Greg , Lindquist, Niels Lyle , Hay, Mark E. , Fenical, William

Investigations 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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Can small rare prey be chemically defended? the case for marine larvae

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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Constraints on chemically-mediated coevolution: multiple functions for seaweed secondary metabolites.

1995-01 , Schmitt, Tim M. , Hay, Mark E. , Lindquist, Niels Lyle

Diterpene 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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Distribution, density, and sequestration of host chemical defenses by the specialist nudibranch Tritonia hamnerorum found at high densities on the sea fan Gorgonia ventalina

1995-03-23 , Cronin, Greg , Hay, Mark E. , Fenical, William , Lindquist, Niels Lyle

The 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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