413 publications from this institution
Red macroalgae are well-known for the production of brominated metabolites, including terpenoids and phenols, yet some taxa within the Rhodophyta remain relatively unstudied. Herein, we report the discovery of unusual diterpene-benzoate natural products representing three novel carbon skeletons, from the red alga Callophycus serratus collected in Fiji. Included among the new compounds were 15- and 16-membered macrolides as well as non-macrocyclic diterpene-benzoic acid structural motifs, all apparently sharing the same 27-carbon biosynthetic precursor. Biological activities of these compounds included moderate antibacterial, antiviral, and antineoplastic effects via specific apoptotic cell death.
Direct effects of predation have been widely recognized as important in affecting prey population dynamics and evolution. However, less attention has been devoted to the consequences of indirect effects of predators on prey behavior. For example, to avoid predation many animals restrict their activities to physical refugia and adopt low-mobility lifestyles, yet the consequences of these anti-predator behaviors for foraging and diet selection are relatively unknown. In this study we examine the relationships between mobility, feeding preferences, and compensatory feeding for 3 species of marine decapod crabs feeding on seaweeds in North Carolina, USA. Low mobility and high site fidelity of crabs were associated with a broad, non-selective diet and compensatory feeding. The majid Mithrax forceps exhibited the lowest mobility, highest site fidelity, and least selective diet of the 3 species, whereas another majid Libinia dubia was intermediate in both mobility and selectivity, and the xanthid Panopeus herbstii had the greatest mobility and narrowest diet. Of these 3 crabs, only M. forceps compensated for low food quality by increasing consumption rates in single food-species feeding assays. This may be because M. forceps is resistant to (or tolerant of) seaweed chemical defenses, while other crab species are not. The ability to consume, and presumably subsist on, a wide variety of potential foods including those defended from more mobile consumers may facilitate a low-mobility lifestyle, allowing the crab to minimize movement and reduce exposure to predators. Low mobility and high site-fidelity may thus facilitate the formation and use of associational refuges with sessile benthic organisms that are resistant to predators; these associations can have important community and ecosystem-wide consequences.
Grazing by the generalist amphipod Ampithoe longimana induced increased concentrations of defensive secondary metabolites in the brown alga Dictyota menstrualis and made the seaweed less susceptible to further attack by the amphipod. Although A. longimana preferentially consumes D. menstrualis, its feeding rates can be reduced significantly by high concentrations of diterpenoid dictyols produced by the alga. In 1991, D. menstrualis from sites with high numbers of A. longimana had higher levels of grazing scars, higher concentrations of dictyols, and were less palatable to A. longimana than plants from sites with few amphipods. Among—site differences in palatability to amphipods did not correlate with plant differences in protein, nitrogen, or carbon content. Within a site, plants that had apparent amphipod grazing scars were significantly less palatable to A. longimana than neighboring undamaged plants. Controlled field experiments manipulating A. longimana densities supported the hypothesis that feeding by this amphipod induced elevated chemical defenses in the alga. Compared to undamaged control plants, amphipod—damaged plants had 19—34% more of three diterpenoid secondary metabolites and were 50% less palatable to amphipods. Soluble protein and thallus toughness were unaffected by amphipod grazing and thus could not have caused the differences in palatability. High—pressure liquid chromatography evaluation of adventitious branches growing from blade margins at sites of amphipod grazing scars showed that these branches had significantly elevated levels of two diterpenoids relative to normal blade apices or middles. Thus, the amphipod—induced resistance to further attack occurs through an increase in chemical defenses, and these defenses are, to some extent, localized within the plant thallus. Among—site differences in amphipod densities, grazing scars, seaweed defensive chemistry, and plant palatability that we documented in 1991 varied considerably during 1992 and 1993, suggesting that these interrelationships may be complex. In 1992, A. longimana densities did not differ between sites, and there were no between—site differences in palatability or concentrations of deterrent secondary metabolites. In 1993, however, A. longimana densities did differ between sites, but between—site differences were less dramatic than in 1991. Some secondary metabolites were slightly, but significantly, increased at the site with higher densities of A. longimana, but this had no effect on A. longimana feeding. It has been long recognized that marine herbivores are active participants in seaweed—herbivore interactions and can greatly influence the structure of benthic algal communities. Our findings suggest that seaweeds are not passive participants in these interactions, but can actively alter their susceptibility to herbivores in ecological time. Induced responses to herbivory help explain both spatial (i.e., within—thallus, within—site, and among—site) and temporal variation in the chemical defenses of D. menstrualis.
Large brown seaweeds dominate coastal hard substrata throughout many of the world's oceans. In coastal North Carolina, USA, this dominance by brown seaweeds is facilitated by omnivorous fishes, which feed both on red and green algae and on herbivorous amphipods that graze brown algae. When fish are removed in the field, brown seaweeds are replaced by red seaweeds, and herbivorous amphipods are more abundant. Using an array of large (∼4000 L) outdoor mesocosms, we tested three mechanistic hypotheses for this pattern: fish feeding facilitates brown algal dominance (1) by removing red and green algal competitors, (2) by removing amphipods and reducing their feeding on brown seaweeds, or (3) through an interaction of these mechanisms. Our experiments revealed strong impacts of both fish and amphipods, and a key role for the interaction, in structuring this community. When both fish and amphipods were removed (the latter with dilute insecticide), space was rapidly dominated and held for 17 weeks by fast-growing, primarily filamentous green algae. In contrast, when either fish, amphipods, or both were present, green algae were cropped to a sparse turf, and space was more rapidly dominated by larger macroalgae. The impacts of amphipods and fish on late-successional macroalgal assemblages were comparable in magnitude, but different in sign: red seaweeds prevailed in the amphipod-dominated treatment, whereas browns dominated in the presence of fish. Laboratory feeding assays and amphipod densities in the tanks suggested that the significant effects of amphipods were attributable largely, if not exclusively, to the single amphipod species Ampithoe longimana, which fed heavily on brown macroalgae. Our experimental removal of red and green algae failed to enhance cover of brown algae significantly; however, the latter reached substantially lower cover in the grazer-removal treatment, where green algae were very abundant, than in the fish-only treatment, where green algae were sparse. Thus, our results support the third hypothesis: fish-mediated dominance of brown algae involves both suppression of grazing amphipods and removal of algal competitors. Although collective impacts of fish and amphipods on this benthic community were generally comparable in magnitude, impacts normalized to each grazer's aggregate biomass were consistently higher for amphipods than for fish, sometimes by 1–2 orders of magnitude. Thus, the impacts of grazing amphipods (specifically A. longimana) on the benthic community were both strong and disproportionate to their biomass. These experimental results imply that grazing amphipods, which are ubiquitous in marine vegetation but poorly understood ecologically, may play important roles in the organization of benthic communities, particularly where predation pressure is low.
Many reefs have shifted from coral and fish dominated habitats to less productive macroalgal dominated habitats, and current research is investigating means of reversing this phase shift. In the tropical Pacific, overfished reefs with inadequate herbivory can become dominated by the brown alga Sargassum polycystum. This alga suppresses recruitment and survival of corals and fishes, thus limiting the potential for reef recovery. Here we investigate the mechanisms that reinforce S. polycystum dominance and show that in addition to negatively affecting other species, this species acts in a self-reinforcing manner, positively promoting survival and growth of conspecifics. We found that survival and growth of both recruit-sized and mature S. polycystum fronds were higher within Sargassum beds than outside the beds and these results were found in both protected and fished reefs. Much of this benefit resulted from reduced herbivory within the Sargassum beds, but adult fronds also grew ~50% more within the beds even when herbivory did not appear to be occurring, suggesting some physiological advantage despite the intraspecific crowding. Thus via positive feedbacks, S. polycystum enhances its own growth and resistance to herbivores, facilitating its dominance (perhaps also expansion) and thus its resilience on degraded reefs. This may be a key feedback mechanism suppressing the recovery of coral communities in reefs dominated by macroalgal beds.
Because food and habitat are closely linked for small herbivores that live on plants, food choice in the field may be constrained by the need to choose plants that provide safe living sites. We investigated the importance of food value and refuge value in determining the plant utilization patterns of the herbivorous marine amphipod Ampithoe longimana. When offered a choice of five common seaweeds, this amphipod fed most readily on Dictyota and Hypnea and less readily on Sargassum, Chondria, and Calonitophyllum. Rates of feeding on the different seaweeds were unrelated to seaweed gross morphology, toughness, nitrogen, or protein content. When cultured on each of these seaweeds in the laboratory, amphipod survivorship was high on Dictyota (82%), intermediate (35 and 18%, respectively) on Sargassum and Hypnea, and low (0%) on the other seaweeds. Survivorship on the different diets was strongly correlated (r = 0.930) with algal protein content; however, neither protein content nor amphipod performance of the different diets was significantly related to feeding rates on those diets. Additionally, amphipods from the three seaweed species that produced some survivors did not differ in growth rate, fecundity, egg size, or age at first ovulation. Variance in survivorship, and related measures, among sibling groups of amphipods suggested that this amphipod population possessed heritable variation for performance on the different seaweed species. In the field, abunda
Increased herbivory at lower latitudes is hypothesized to select for more effective plant defenses. Feeding assays with seaweeds and salt marsh plants support this hypothesis, with low‐latitude plants experiencing greater damage in the field and being less palatable than higher‐latitude plants. We tested this hypothesis for freshwater macrophytes because they offered an independent plant lineage and habitat type for testing this general hypothesis and because the patchiness of consumer occupancy across isolated water bodies might produce local variance in herbivory that would override geographic variance and produce different results for this habitat type. When we fed eight congeneric pairs of live plants from four sites in Indiana vs. four sites in South Florida (∼215 and 0 frost days/yr respectively) to three species of crayfishes and one species of snail, three of the four herbivores significantly preferred high‐latitude to low‐latitude plants. For two crayfishes that differed in feeding on live plants (one favoring high‐latitude plants and one not), we retested feeding using foods composed of freeze‐dried and finely ground plants, thus removing structural characteristics while retaining most chemical/nutritional traits. In this assay, both herbivores strongly preferred high‐latitude plants, suggesting that lower‐latitude plants had been selected for more deterrent chemical traits. When we collected 22 pairs of congeneric plants from 9 sites throughout Indiana vs. 13 sites in Central Florida (∼215 and ∼95 frost days/yr respectively) and tested these in feeding assays with three crayfishes using dried, ground, and reconstituted plant material, we found a significant effect of latitude for only one of three species of herbivore. Overall, our results suggest a preference for high‐latitude plants, but the strength of this relationship varied considerably across small scales of latitude that differed considerably in numbers of frost‐free days. The difference in results suggests that large changes in frost frequency over small spatial scales may affect selection for plant defenses, that local variance in herbivory overrode differential selection at geographic scales, or that these possibilities interact when durations of cold weather periodically exclude herbivores from shallower habitats, producing heterogeneous selection for defenses at small spatial scales.
Physical stress to seaweeds and hunger stress of herbivores can influence the outcome of chemically mediated seaweed—herbivore interactions. The unpalatable brown seaweed Dictyota ciliolata produces the diterpenoid secondary metabolites pachydictyol A, dictyol B acetate, and dictyodial. At natural concentrations, pachydictyol A deterred the sea urchin Arbacia punctulata but did not inhibit feeding by the pinfish Lagodon rhomboides or the amphipod Ampithoe longimana until concentrations were 2.5—5 times natural levels. Dictyol B acetate deterred the urchin, amphipod, and pinfish at, or far below, natural concentrations. Dictyodial was too unstable to assay directly, but indirect experiments suggested that natural concentrations deterred the urchin, but not the pinfish or amphipod. Mild desiccation of D. ciliolata reduced concentrations of the different secondary metabolites by 7—38% and plants became 2.6—3.4 times more susceptible to urchin and amphipod grazing. The combined concentrations of pachydictyol A and dictyol B acetate found in undesiccated Dictyota ciliolata deterred feeding by urchins, but this deterrent effect was lost at concentrations found in the desiccated plants. Desiccated and undesiccated plants did not differ in nutritive value (as measured by protein and total N content) or toughness. Thus, desiccated plants became more palatable because chemical defenses were lost, not because nutritive value was increased. The stress of near—surface ultraviolet radiation also caused significant physiological changes in Dictyota ciliolata. UV—exposed blades bleached, senesced, and grew 84% less than blades protected from UV radiation. Tissue loss and minimal growth of UV—stressed plants constrained our sample sizes, but the limited assays that could be run suggested that UV stress may lower chemical defenses and increase plant susceptibility to herbivores. Because many previous investigations of herbivore feeding patterns used animals that had been starved for days before an assay, we tested the effects of this commonly used procedure on feeding discrimination. Recently fed urchins always avoided food containing natural concentrations of pachydictyol A during separate feeding trials performed on each of four consecutive days. In contrast, urchins deprived of food for 3 d before this assay did not avoid the treated food on days 1 and 2 of feeding trials, but did avoid it on days 3 and 4 after their hunger was reduced by feeding during days 1 and 2. If we had used only starved urchins (a common procedure in previous investigations), we could have concluded, with apparent justification, that urchins were unaffected by pachydictyol A (if the assays were run for only 1—2 d) or that they needed 2 d of exposure to the compound in order to learn to avoid it. Both of these conclusions would have been incorrect.
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