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Center for the Study of Systems Biology

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Now showing 1 - 10 of 13

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.
Chemical defense of hydrothermal vent and hydrocarbon seep organisms: a preliminary assessment using shallow-water consumers

(Georgia Institute of Technology, 2004-07-14) Kicklighter, Cynthia Ellen ; Fisher, C. R. ; Hay, Mark E.

Organisms at deep-sea hydrothermal vent or cold-seep communities represent oases of prey in an otherwise prey-poor desert. Why deep-sea consumers that remove other dense food patches do not rapidly remove the high biomass of prey from these communities is unclear. One potential explanation is that hydrogen sulfide, or other metabolites, in these chemoautotrophic prey could be serving as chemical defenses against generalist consumers; however, neither the palatability of these prey nor their potential defenses have been assessed. We fed tissues from 10 species of deep-sea polychaetes and 2 species of bivalves to shallow-water fishes Fundulus heteroclitus and Leiostomus xanthurus or crabs Callinectes similis and Pachygrapsus crassipes to assess their palatability to generalist consumers. Tissues from 4 polychaetes (Archinome rosacea, Lamellibrachia luymesi, Riftia pachyptila, and Seepiophila jonesi) and 1 bivalve (Calyptogena magnifica) were rejected by some consumers. Blood, which can be sulfide-rich, from R. pachyptila did not deter feeding. Sharp setae deterred feeding on the polychaete A. rosacea, while the other unpalatable species produced chemical extracts that deterred feeding. All of the chemically deterrent species contained chemoautotrophic endosymbiotic bacteria, suggesting that these microbial symbionts may produce metabolites that defend their host species. In several instances, consumers encountering novel, deep-sea prey consumed more on the first day of feeding than on later dates, or initially rejected the foods, but then consumed them after repeated encounters. Investigations with predators from the deep-sea are required to more fully understand the ecological role of prey defenses for deep-sea species.
Palatability and defense of some tropical infaunal worms: alkylpyrrole sulfamates as deterrents to fish feeding

(Georgia Institute of Technology, 2003-11-28) Kicklighter, Cynthia Ellen ; Kubanek, Julia ; Barsby, Todd ; Hay, Mark E.

Numerous studies have investigated chemical defenses among sessile species growing on hard substrates, but few have addressed this for mobile species in soft-sediment communities. We investigated the palatability and potential chemical defenses of 11 worm species from soft-sediment systems in southern Florida, USA. Three species were unpalatable to the bluehead wrasse Thalassoma bifasciatum. The polychaete Cirriformia tentaculata and the hemichordate Ptychodera bahamensis were uniformly unpalatable. For the polychaete Eupolymnia crassicornis, the exposed tentacles were unpalatable, but the body, which remains protected in a deeply buried tube, was palatable. These unpalatable worms were chemically defended; extracts of C. tentaculata, P. bahamensis, and the tentacles of E. crassicornis deterred fish feeding. For C. tentaculata, bioassay-guided fractionation demonstrated that a mixture of 3 closely related alkylpyrrole sulfamates deterred fish at naturally occurring concentrations (2-n-hexylpyrrole sulfamate [1.6% of worm dry mass], 2-n-heptylpyrrole sulfamate [3.1% dry mass], and 2-n-octylpyrrole sulfamate [0.8% dry mass]). This appears to be the first documentation of characterized natural products defending a marine worm from consumers. For P. bahamensis and the tentacles of E. crassicornis, deterrent effects of crude extracts decomposed before specific compounds could be identified
Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness

(Georgia Institute of Technology, 2003-08) Cruz-Rivera, Edwin ; Hay, Mark E.

Numerous studies have assessed the individual effects of prey nutritional quality or chemical defenses on consumer feeding behavior. However, little is known about how these traits interact to affect consumer feeding and performance. We tested the separate and interactive effects of prey chemical defenses and nutritional quality on the feeding behavior and fitness of six sympatric crustacean mesograzers. Natural concentrations of diterpene alcohols (dictyols) from the brown alga Dictyota menstrualis were incorporated, or not incorporated, into lower quality and higher quality foods to create artificial diets mimicking prey of variable value and defense. Five amphipods (Ampithoe longimana, A. valida, Cymadusa compta, Gammarus mucronatus, and Elasmopus levis) and one isopod (Paracerceis caudata), representing a continuum of closely to distantly related organisms, were fed intact algae or lower and higher quality diets containing or lacking dictyols. All six mesograzers preferred the green alga Enteromorpha intestinalis to the dictyol producing alga Dictyota menstrualis. In assays allowing consumers to choose between simultaneously available foods, dictyols deterred feeding by all five amphipods, but not the isopod; this occurred for both lower and higher quality foods. In no-choice assays, where consumers were confined with only one of our four treatment diets, effects on feeding became more complex. Nutritional quality alone affected feeding by five of the six species. These grazers compensated for lower quality by increasing consumption. Dictyols suppressed feeding for four of the six species. More interestingly, there were significant dictyol × quality interactions for three species. Dictyols decreased feeding more when placed in lower quality foods than higher quality foods. Two amphipods deterred by dictyols in the choice assays readily consumed dictyol-containing foods in no-choice situations and suffered few negative effects of doing so. Although all amphipods were deterred by dictyols in choice assays, dictyols decreased fitness (survivorship, growth, or reproduction) for only four of the five species. These effects included large and immediate decreases in survivorship, dramatic effects on reproduction, and modest effects on female growth. Dictyols enhanced survivorship of the isopod. Thus, the effects of secondary metabolites on feeding in choice situations vs. fitness in long-term assays were inconsistent. For three amphipods, certain effects of food quality, dictyols, or their interaction were detected only for females. In general, negative effects of dictyols on fitness were greater in lower than in higher quality foods, suggesting that prey nutritional value may counteract the effects of defensive metabolites. For example, when G. mucronatus consumed dictyols in lower quality foods, mortality was >80% by day 5; for dictyols in higher quality foods, 80% mortality took 28 days to develop. Lower quality foods alone significantly decreased growth for the isopod, three of the amphipods, and the females of a fourth amphipod, concomitantly reducing fecundity for four of the five amphipods studied. The effects of both chemical defenses and nutritional quality were unrelated to consumer phylogeny; responses of congeners varied as much, or more, than responses of more distantly related consumers. Understanding mechanisms and consequences of food selection requires that the interactive effects of both chemical defenses and prey nutritional characteristics be considered explicitly.
Selection of Estuarine Habitats by Juvenile Gags in Experimental Mesocosms

(Georgia Institute of Technology, 2003-01) Levin, Phillip S. ; Hay, Mark E.

The degradation and destruction of estuarine habitats threaten the organisms that depend on these habitats for food and shelter. Gags Mycteroperca microlepis reside on rocky reefs for most of their lives but initially settle and rear in estuarine habitats before moving to offshore reefs. Gag populations have declined to the point where some consider them vulnerable to extinction, and the recovery of the species requires an understanding of what habitats these fish use and why they use them. We examined the habitat selection of juvenile gags in North Carolina using experimental mesocosms.We manipulated the shelter characteristics of habitats and compared the foraging rates of gags to determine the specific attributes of habitats that influence habitat selection. Gags selected structured seagrass or oyster reefs over sand and shell hash habitats. While gags did not show a preference between eelgrass Zostera marina and oyster reefs, they did choose oyster reefs over shoal grass Halodule wrightii and selected seagrass habitats with high shoot densities over those with lower densities. The addition of a small shelter to the habitat that the gags did not choose dramatically increased their use of that habitat. Finally, when we provided pinfish Lagodon rhomboides as prey, gag foraging rate did not vary among seagrass habitats with different shoot densities. However, gags consumed penaeid shrimp at much lower rates in seagrass habitats of high shoot density. Our results agree with those of other studies suggesting that seagrass habitats are important to gags. However, our results also emphasize that gags select specific attributes within seagrass landscapes and suggest that oyster reefs may be important habitats for them.
Geographic variation among herbivore populations in tolerance for a chemically rich seaweed

(Georgia Institute of Technology, 2002-10) Sotka, Erik E. ; Hay, Mark E.

Previous investigations have shown that the sedentary amphipod Ampithoe longimana escapes consumers by selectively living on and eating chemically defended seaweeds in the genus Dictyota. However, A. longimana and Dictyota overlap only in the southern portion of the amphipod's range; Dictyota is not available to amphipods from more northerly regions. We used this disjunction in distribution to test the hypothesis that A. longimana populations co-occurring with Dictyota would have greater tolerance for the seaweed's chemical defenses and would display higher feeding preference for, and fitness on, the seaweed than would more northerly populations. We also evaluated the genetic vs. phenotypic basis of these patterns and attempted to detect trade-offs between tolerance for Dictyota and ability to use other plants as foods. Such geographic studies of herbivory have been conducted using terrestrial insects, but few studies have focused on other herbivores, and this is especially true for marine systems. In multiple-choice feeding assays with both field-collected and laboratory-reared adults, a North Carolina population of A. longimana sympatric with Dictyota more readily fed on Dictyota and was more resistant to Dictyota's deterrent chemistry than was a Connecticut population from outside of Dictyota's geographic range. When raised on Dictyota menstrualis and D. ciliolata, A. longimana juveniles from North Carolina grew faster, matured faster, and produced more reproductive females than did Connecticut juveniles. The differential tolerance for Dictyota has a genetic basis, as it was maintained through two generations grown to maturity in a common environment. When several northern and southern populations were assayed, they displayed similar regional differences in feeding preferences. Though southern juveniles had higher fitness on Dictyota than northern juveniles, southern juveniles performed as well as northern juveniles when raised on seven other seaweeds, including seaweeds (e.g., Fucus vesiculosus and Sargassum filipendula) that produce secondary metabolites in a different class from those found in Dictyota. Thus, tolerating Dictyota did not incur detectable performance trade-offs when juveniles were confined to feeding on alternative seaweeds. Our results suggest that the evolution of host preferences may depend more on the host value as a refuge from enemies than on minimizing the costs of tolerating plant secondary metabolites.
Fish-seaweed association on temperate reefs: do small-scale experiments predict large-scale patterns?

(Georgia Institute of Technology, 2002-05-03) Levin, Phillip S. ; Hay, Mark E.

Processes affecting reef fish populations are likely to vary with spatial scale, but there have been few attempts to determine whether predictions generated by small-scale experiments are manifested at larger spatial scales. Our goal in this study was to determine if patterns of microhabitat use measured in small-scale experimental manipulations scaled-up and allowed predictions of among-reef patterns of abundance across larger spatial scales. Manipulations of algal biomass in artificially created 1.5 m2 plots indicated that patches of Sargassum filipendula supported greater numbers of slippery dick Halichoeres bivittatus than those with an equal biomass of Zonaria tournefortii, or than patches with an equal mix of S. filipendula and Z. tournefortii. Scaling up and manipulating S. filipendula and Z. tournefortii abundance in 100 m2 sections of reef produced results qualitatively similar to the small-scale experiments; fish densities varied as a function of S. filipendula mass. Larger scale surveys of fish densities and algal biomass on large reefs separated by 1 to 30 km showed positive associations between fish density and S. filipendula biomass. For the reefs that we studied, our small-scale experiments scaled up and predicted large-scale patterns of abundance on reefs in the South Atlantic Bight.
Plankton tethering to assess spatial patterns of predation risk over a coral reef and seagrass bed

(Georgia Institute of Technology, 2002-01-11) Bullard, Stephan G. ; Hay, Mark E.

Difficulties associated with manipulating plankton in situ have limited the ability of investigators to assess among-habitat variation in predation risk for plankton. We used plankton tethering units (PTUs) to tether zooplankton in a variety of reef and seagrass habitats, and used field and laboratory assays to test PTUs for tethering artifacts. Tethering did not affect the survivorship of 5 species of plankton (sizes <1 to 6 mm), indicating that the method works with a range of planktonic organisms. We then used the reef mysid Mysidium columbiae in additional assays and found that: (1) mysids remained on PTUs unless they were attacked by predators; (2) PTUs did not prevent planktivorous fishes from consuming tethered mysids; (3) untethered mysids commonly evaded predators, while mysids on PTUs did not; (4) the same types of predators consumed untethered and tethered mysids in the field; and (5) fishes were neither attracted to nor repelled from PTUs. We used PTUs and mysids to assess predation risk for plankton over various coral reef or seagrass habitats. Risk of attack varied among habitats and was correlated with abundance of planktivorous fishes. On the reef, attack rates were most intense over a topographically complex reef ledge, less intense over the less structurally complex center of the reef, and least intense over a structurally simple sand plain. Within the seagrass bed, attack rates were highest at the edge of the bed and less intense to the center of the seagrass bed and over an adjacent sand plain. Thus, attack rates at these sites varied tremendously over small spatial scales (meters).
Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation

(Georgia Institute of Technology, 2001-08-20) Cruz-Rivera, Edwin ; Hay, Mark E.

Selective feeding, compensatory feeding, and diet mixing have all been proposed as adaptive strategies allowing herbivores to enhance nutrient intake from low quality plant and algal foods. However, little is known about the relative importance of these alternative feeding strategies for consumer fitness or about how these strategies are affected by prey nutritional traits. To address this, we studied the effects of algal nutritional value and toughness on feeding choices, feeding rates, and survival, growth and fecundity of the amphipod Ampithoe longimana. To assess the value of diet mixing, we compared fitness of amphipods cultured on each of 15 algal species or on 4 different mixtures of algae. We also quantified how sequentially switching between algae that supported higher and lower fitness affected fitness compared to monospecific diets of these algae and to a constant mixture of the algae. Protein, nitrogen, organic content, or toughness of algae did not correlate with food choice by A. longimana. In contrast, we found a strong inverse correlation between feeding rates and algal organic content [ash free dry mass/wet mass (AFDM:WM) and total organic carbon (TOC)], and, to a lesser extent, protein (but not nitrogen). Thus, when confined with algae having lower nutritional value, A. longimana used quantity to compensate for quality. This compensatory feeding was confirmed by feeding amphipods on artificial diets that varied only in their amount of AFDM:WM. Despite broad differences in algal nutrient content or other traits, compensatory feeding allowed this amphipod to maintain high fitness when cultured on most, but not all, algae. Access to algal mixtures did not enhance fitness compared to feeding on several algae offered alone, suggesting that A. longimana need not rely on a mixed diet. Even when significant differences in survivorship or growth occurred between a monospecific diet and a mixed diet, fecundity or size of eggs produced by egg-bearing survivors were generally unaffected. Furthermore, when amphipods were switched sequentially (every 24 h) between 2 different quality algae, only growth (but not survivorship, fecundity, or egg size) was affected, with growth determined primarily by the higher quality alga offered. Amphipods confined with the green alga Codium fragile ovulated significantly later than conspecifics on one mixed diet, but this effect was observed only in 1 of 2 long-term assays. Thus, dietary mixing offered only a moderate benefit to this amphipod under very restrictive conditions. For A. longimana, food selection is relatively unresponsive to algal nutritional quality, apparently because compensatory feeding allows this amphipod to successfully exploit a variety of algal foods. Compensatory feeding also may reduce the need to move among host algae in order to mix diets, thus decreasing the risk of movement-associated detection by predators.
Activated chemical defenses in tropical versus temperate seaweeds

(Georgia Institute of Technology, 2000-11-22) Cetrulo, Giancarlo L. ; Hay, Mark E.

Chemical defenses that are rapidly activated in response to injury have been reported in numerous species of vascular plants, but activated chemical defense has been demonstrated for only 1 genus of seaweed. To investigate the frequency of potential activated chemical defenses in seaweeds and to determine if there are geographic differences in the frequency of theses, we conducted urchin and fish feeding assays using chemical extracts from 42 species of temperate or tropical seaweeds that were damaged immediately before extraction in organic solvents (= the potentially activated extract) or placed in organic solvents before they were damaged (= the non-activated extract). Seven species exhibited changes in palatability consistent with activated defenses while 4 species became more, rather than less, palatable if they were damaged 30 s before extraction. Frequency of activation did not vary geographically. Seventeen percent of tropical species (4 of 24) and 17% of temperate species (3 of 18) exhibited changes in palatability that were consistent with activation of chemical defenses. Thin-layer chromatography of lipid-soluble extracts indicated that damaging the thallus prior to extraction caused noticeable chemical changes in 70% of the species evaluated. Investigations of algal chemical defenses thus need to consider the effects of injury during herbivore attacks and the effects of extraction methodology on the types of, and concentrations of, metabolites discovered in seaweeds.