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Hay, Mark E.

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https://hdl.handle.net/1853/71334

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School of Biological Sciences

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Ambiguous role of phlorotannins as chemical defenses in the brown alga Fucus vesiculosus

(Georgia Institute of Technology, 2004-08-16) Kubanek, Julia ; Lester, Sarah E. ; Fenical, William ; Hay, Mark E.

Brown seaweeds (Fucales) produce phlorotannins that are often considered chemical defenses against herbivores. The many correlative and fewer direct tests conducted have shown effects of phlorotannins on herbivore feeding behavior to be variable. In an attempt to clarify the roles of phlorotannins versus other metabolites in defending brown algae, we conducted bioassay-guided fractionation of herbivore-deterrent extracts from the commonly studied brown alga Fucus vesiculosus. Feeding by the amphipods Ampithoe valida and A. longimana and the sea urchin Arbacia punctulata was suppressed by crude and water-soluble extracts of F. vesiculosus, but this deterrence was lost following storage or fractionation of the active, water-soluble extract. Phlorotannins in these extracts did not decompose in parallel with the loss of feeding deterrence. F. vesiculosus phlorotannins were fed to herbivores at 3 to 12× the isolated yield (or 4.2 to 16.8% of plant dry mass). No herbivore was deterred from feeding by concentrations of 3 or 6×, but A. valida (the only test herbivore that readily consumes F. vesiculosus in the field) was deterred at 12× isolated yield. When juvenile A. valida were raised on an artificial diet containing F. vesiculosus phlorotannins at 3× isolated yield, the phlorotannin-rich diet significantly enhanced, rather than reduced, amphipod survivorship and growth relative to an equivalent diet without phlorotannins. Females ovulated only on the phlorotannin-rich diet. Compounds other than phlorotannins appear to defend the F. vesiculosus populations we investigated, but we were unable to identify these unstable compounds.
Distribution, 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 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.
Effects 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, 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.
Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality

(Georgia Institute of Technology, 1994) Hay, Mark E. ; Kappel, Quaker E. ; Fenical, William

Many tropical seaweeds and benthic invertebrates produce both secondary metabolites and calcium carbonate (CaC03) particles or spicules that serve as possible defenses against consumers. To evaluate the relative defensive value ofCaC03 , secondary metabolites, and the potential synergistic or additive effects of the two, we made artificial agar-based "seaweeds" in which we manipulated algal organic content, CaC03 , and the secondary metabolites produced by the calcified green seaweeds Rhipocephalus phoenix, Udotea cyathiformis, and Halimeda goreauii, all of which are relatively resistant to herbivores. The effects ofthese manipulations on herbivore feeding were evaluated using three different types of herbivores, the sea urchin Diadema antillarum, the amphipod Cymadusa filosa, and a mixed-species group of small parrotfishes. Addition of finely powdered CaC03 as 69% of food dry mass had no effect on feeding by parrotfishes, deterred feeding by Cymadusa, and deterred Diadema when food organic content was low but not when it was higher. Although calcification of algal tissues has generally been considered a structural defense that hardens seaweed thalli and makes them more resistant to attack, the decreased feeding on CaC03-containing foods in our assays occurred without any measurable alteration of food toughness. At natural concentrations, semi purified secondary metabolites from Rhipocephalus or Udotea deterred feeding by all three herbivores. In most assays, feeding was depressed more by the addition of metabolites from Rhipocephalus or Udotea than by the addition of CaC03 even though CaC03 was added at 1.3-2,2 times the natural concentration for these plants. In contrast, the major metabolite from Halimeda goreauii, when tested alone, did not affect feeding by any of the herbivores. In two of our nine assays, the synchronous combination ofCaC03 and secondary metabolites acted synergistically and deterred feeding significantly more than the sum of the effects of each tested separately. Mechanisms producing these synergisms are unknown, but it is possible that calcification could also be acting as a chemical defense by altering gut pH in ways that increase the potency of the secondary metabolites. It is common for chemical, structural, morphological, and nutritional deterrents to co-occur in individual prey species. For some plant-herbivore interactions, the combined effects of these characteristics can be much more than the sum of their separate effects.
Defense of ascidians and their conspicuous larvae: adult vs. Larval chemical defenses

(Georgia Institute of Technology, 1992-12) Lindquist, Niels Lyle ; Hay, Mark E. ; Fenical, William

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.
Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing

(Georgia Institute of Technology, 1990) Hay, Mark E. ; Duffy, J. Emmett ; Fenical, William

We investigated the factors selecting for host-plant specialization and the roles that plant defensive chemistry may play in this process. We studied marine organisms because marine communities contain fewer specialized herbivores than terrestrial communities and, therefore, provide a simplified system for investigating certain aspects of host-plant specialization. Our study focused on the unusual domicile-building and feeding behavior of the amphipod Pseudamphithoides incurvaria, which is the only herbivorous marine amphipod known to specialize on a few closely related seaweeds. P. incurvaria lives in a portable, bivalved domicile that it constructs from the chemically defended brown alga Dictyota bartayresii. Chemical assays indicate that natural populations of Pseudamphithoides construct their domiciles from D. bartayresii even when this alga is rare compared to other Dictyota species and to other related genera in the family Dictyotaceae. In both choice and no-choice tests in the laboratory, Pseudamphithoides built domiciles from and selectively consumed species of Dictyota that produced dictyol-class diterpenes that deter feeding by reef fishes. Other brown seaweeds in the family Dictyotaceae, including a Dictyota species, that did not produce these fish-feeding deterrents were avoided by the amphipod. Amphipods removed from their domiciles were rapidly eaten when presented to predatory fish; amphipods in their normal domiciles were consistently rejected by fish. The defensive value of the domicile appeared to result from specific characteristics of the Dictyota from which it was built, since amphipods forced to build domiciles from the palatable green seaweed Viva were rapidly eaten when these amphipods, in their domiciles, were exposed to predatory fish. Algal defensive chemistry directly cued domicile building. When the green alga VIva was treated with pachydictyol-A (the major secondary metabolite produced by Dictyota bartayresiz), domicile building by Pseudamphithoides increased in proportion to the concentration of pachydictyol-A. All data collected during this study are consistent with the hypothesis that predator escape and deterrence are primary factors selecting for host specialization by Pseudamphithoides incurvaria. Similar conclusions can be drawn for the limited number of other marine herbivores that are relatively specialized.
Chemical defense in the seaweed Dictyopteris delicatula: differential effects against reef fishes and amphipods

(Georgia Institute of Technology, 1988-09-21) Hay, Mark E. ; Duffy, J. Emmett ; Fenical, William ; Gustafson, Kirk

Many seaweeds produce chemicals that deter feedlng by fishes and sea urchins. A growing body of evidence suggests that small, relatively immobile herbivores (mesograzers) such as amphpods, polychaetes, and ascoglossan gastropods are often unaffected by these compounds and may preferentially consume seaweeds that are chemically defended from fishes. We tested this hypothesis by examining the responses of reef fishes and amphipods to a mutture of 2 C,, hydrocarbons, &ctyopterenes A and B, produced by the Canbbean brown alga D~ctyopteris delicatula. This alga was intermediate in preference for reef fishes, and the dictyopterenes reduced fish grazing by a significant 40 %. In contrast, D. delicatula was highly preferred by a muted-species group of amphipods and the dlctyopterenes had no effect on their feeding Despite the tendency for mesograzers to selectively consume some seaweeds that are chemically deterrent to fishes, true specialization by these or other marine herbivores appears to be rare in companson with terrestnal systems. Plant-dwelling amphipods at our study site in the Grenadine Islands were found on, and consumed a variety of, macrophytes; they were not restrict~velys pecialized to D. delicatula. Many terrestnal insects are very specialized feeders, sequester toxins from theu food plants, and use these as duect defenses against predation. In contrast, sequestenng of seaweed toxlns by marine mesograzers appears to be relahvely rare. However, the indirect advantage of llving on seaweeds that are not eaten by fishes may be considerable. We hypothesize that mesograzers living on plants chemically defended from fishes wlll experience less predation than those living on plants preferred by fishes.
Chemical defense against different marine herbivores: are amphipods insect equivalents?

(Georgia Institute of Technology, 1987) Hay, Mark E. ; Duffy, J. Emmett ; Pfister, Catherine A. ; Fenical, William

The structurally similar diterpenoid alcohols pachydictyol-A and dictyol-E are produced by the brown seaweed Dictyota dichotoma. This seaweed and several related species that also produce these compounds are known to be relatively low preference foods for tropical fishes and urchins. We evaluated the effect of various concentrations of these compounds on feeding by the three common types of herbivores that co-occur with Dictyota in coastal North Carolina. Fish (Diplodus holbrooki), sea urchins (Arbacia punctulata), and a mixed species group of gammarid amphipods were offered pieces ofthe palatable seaweed Graci/aria tikvahiae coated with either (1) dictyol-E or pachydictyol-A dissolved in diethyl ether or (2) diethyl ether alone. Dictyol-E significantly reduced consumption by fish and urchins at concentrations of 0.5 and 1.0% of algal dry mass, but had no effect on amphipod grazing. Pachydictyol-A significantly reduced fish grazing at the relatively high concentrations of 1.0 and 1.3% of plant dry mass; at 0.5% it tended to decrease grazing, but the effect was not significant (P = .07). Pachydictyol-A had no effect on urchin grazing and significantly increased amphipod grazing. When Pachydictyol-A was fed to fish as 1.0% of food dry mass, their growth rate was reduced by a significant 48%. In feeding preference experiments with several seaweeds, Dictyota ranks low for fish and urchins but high for amphipods. This is consistent with the hypothesis that the secondary metabolites produced by Dictyota playa major role in determining its susceptibility to herbivores. The ability of amphipods to circumvent the chemical defenses of Dictyota, and the fact that the two species of algae most readily consumed by amphipods (Codium and Dictyota) were the two species least readily consumed by fish, suggest that predation and herbivory by fishes may be major factors selecting for amphipods that can live on, and eat, seaweeds that are unpalatable to fishes. Amphipods that fed on Dictyota did not appear to sequester the Dictyota metabolites; when exposed to fish predation, Dictyota-fed amphipods were eaten as readily as amphipods that had fed on an alga with no defensive chemistry. Tubicolous amphipods and other small marine herbivores that may spend significant portions of their lives on only a few plants may be under very different evolutionary constraints than the larger, more mobile herbivores that commonly move between many plants. Several characteristics of these smaller, less mobile, and much less studied, marine herbivores suggest that they may be ecologically similar to terrestrial insects and may play a large, but presently unappreciated, role in structuring marine plant communities.
Chemical defense against diverse coral reef herbivores

(Georgia Institute of Technology, 1987) Hay, Mark E. ; Fenical, William ; Gustafson, Kirk

Five secondary metabolites from tropical marine algae and one related compound from an herbivorous sea-hare (Aplysidae) were coated, at approximately natural concentrations, onto the palatable seagrass Thalassia testudinum and placed on coral reefs where they could be eaten by the diverse group of herbivorous fishes that occur there. Laboratory feeding assays with the herbivorous sea urchin Diadema antillarum were also conducted. When compared to appropriate controls, the following terpenoid compounds significantly reduced the amount of Thalassia eaten by both Diadema and reef fishes: stypotriol, from the brown seaweed Stypopodium zonale; pachydictyol-A, which is produced by several genera of tropical (Dictyota and Dilophus) and warm-temperate (Paehydiet yon and Glossophora) brown seaweeds; elatol, from the tropical red alga Laureneia obtusa; and isolaurinterol, which is produced by several tropical and warm-temperate species of Laureneia, Under very mild acid conditions, isolaurinterol is converted to a structurally similar compound, aplysin, found in high concentrations in sea-hares that feed on isolaurinterol-containing Laureneia species. Aplysin did not deter feeding by either type of herbivore. Cymopol, a terpenoid bromohydroquinone from the green alga Cymopolia barbata, significantly reduced feeding by reef fishes but significantly stimulated feeding by Diadema, Pharmacological and crude bioactivity tests suggest that several of these compounds function as generalized toxins. However, these generalized laboratory assays are not necessarily good predictors of how compounds will affect feeding by herbivores. For example, pachydictyol-A and stypotriol were equally effective at deterring fishes and Diadema, even though pachydictyol-A shows almost no bioactivity in laboratory assays while stypotriol and its oxidation product, stypoldione, are very bioactive. Herbivory on coral reefs is more intense than in any other habitat studied and the diversity of herbivore types is high. It appears that this intense grazing has provided strong selection for seaweeds that synthesize unique secondary metabolites that significantly reduce the consumption of plants exposed to attack by a diverse group of reef herbivores.