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School of Biological Sciences

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College of Sciences

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Center for the Study of Systems Biology

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Now showing 1 - 10 of 19

Propagule pressure of an invasive crab overwhelms native biotic resistance.

(Georgia Institute of Technology, 2007-07-24) Hollebone, Amanda L. ; Hay, Mark E.

Over the last decade, the porcelain crab Petrolisthes armatus invaded oyster reefs of Georgia, USA, at mean densities of up to 11 000 adults m–2. Interactions affecting the invasion are undocumented. We tested the effects of native species richness and composition on invasibility by constructing isolated reef communities with 0, 2, or 4 of the most common native species, by seeding adult P. armatus into a subset of the 4 native species communities and by constructing communities with and without native, predatory mud crabs. At 4 wk, recruitment of P. armatus juveniles to oyster shells lacking native species was 2.75 times greater than to the 2 native species treatment and 3.75 times greater than to the 4 native species treatment. The biotic resistance produced by 2 species of native filter feeders may have occurred due to competition with, or predation on, the settling juveniles of the filter feeding invasive crab. Adding adult porcelain crabs to communities with 4 native species enhanced recruitment by a significant 3-fold, and countered the effects of native biotic resistance. Differences in recruitment at Week 4 were lost by Weeks 8 and 12, when densities of recent recruits reached ~17 000 to 34 000 crabs m–2 across all treatments. Thus, native species richness slows initial invasion, but early colonists stimulate settlement by later ones and produce tremendous propagule pressure that overwhelms the effects of biotic resistance.
Population dynamics of the non-native crab Petrolisthes armatus invading the South Atlantic Bight at densities of thousands m⁻²

(Georgia Institute of Technology, 2007-04-27) Hay, Mark E. ; Hollebone, Amanda L.

The green porcelain crab Petrolisthes armatus recently invaded oyster reefs of the South Atlantic Bight. In 2 estuaries of coastal Georgia, USA, crab densities reached peak densities of 4000 to 11 000 crabs m–2 in some periods and locations. Densities generally were higher in the low versus the high intertidal and in the lower versus upper regions of the estuaries. In warmer months, 20 to 90% of adult females were gravid, recruits were dense, and population levels were high. In colder months, densities dropped by 64 to >99%. Male:female ratios were near 1:1 across times and locations. Maximum mean densities of P. armatus in Georgia were 37 times the highest densities recorded in the presumptive native range. Crabs in the new range reproduced at a smaller size, and the percentage of gravid females was similar between the old and new range. Thus, population fecundity in Georgia exceeds that of the native range by more than 1 order of magnitude. Densities of native mud crabs in the genera Panopeus and Eurypanopeus were unrelated to, or positively correlated with, densities of the exotic crabs; correlations were never significantly negative. The impact of Petrolisthes armatus on native communities is unclear, but could be considerable if this filter-feeding crab impacts oysters, which are the foundation species of inshore reefs.
Herbivore vs. nutrient control of marine primary producers: context-dependent effects

(Georgia Institute of Technology, 2006-12) Burkepile, Deron E. ; Hay, Mark E.

Pervasive overharvesting of consumers and anthropogenic nutrient loading are changing the strengths of top-down and bottom-up forces in ecosystems worldwide. Thus, identifying the relative and synergistic roles of these forces and how they differ across habitats, ecosystems, or primary-producer types is increasingly important for understanding how communities are structured. We used factorial meta-analysis of 54 field experiments that orthogonally manipulated herbivore pressure and nutrient loading to quantify consumer and nutrient effects on primary producers in benthic marine habitats. Across all experiments and producer types, herbivory and nutrient enrichment both significantly affected primary-producer abundance. They also interacted to create greater nutrient enrichment effects in the absence of herbivores, suggesting that loss of herbivores produces more dramatic effects of nutrient loading. Herbivores consistently had stronger effects than did nutrient enrichment for both tropical macroalgae and seagrasses. The strong effects of herbivory but limited effects of nutrient enrichment on tropical macroalgae suggest that suppression of herbivore populations has played a larger role than eutrophication in driving the phase shift from coral- to macroalgal-dominated reefs in many areas, especially the Caribbean. For temperate macroalgae and benthic microalgae, the effects of top-down and bottom-up forces varied as a function of the inherent productivity of the ecosystem. For these algal groups, nutrient enrichment appeared to have stronger effects in high- vs. low-productivity systems, while herbivores exerted a stronger top-down effect in low-productivity systems. Effects of herbivores vs. nutrients also varied among algal functional groups (crustose algae, upright macroalgae, and filamentous algae), within a functional group between temperate and tropical systems, and according to the metric used to measure producer abundance. These analyses suggest that human alteration of food webs and nutrient availability have significant effects on primary producers but that the effects vary among latitudes and primary producers, and with the inherent productivity of ecosystems.
Chemically mediated competition between microbes and animals: microbes as consumers in food webs

(Georgia Institute of Technology, 2006-11) Burkepile, Deron E. ; Parker, John D. ; Woodson, Clifton Brock ; Mills, Heath Jordan ; Kubanek, Julia ; Sobecky, Patricia A. ; Hay, Mark E.

Microbes are known to affect ecosystems and communities as decomposers, pathogens, and mutualists. However, they also may function as classic consumers and competitors with animals if they chemically deter larger consumers from using rich food-falls such as carrion, fruits, and seeds that can represent critical windfalls to both microbes and animals. Microbes often use chemicals (i.e., antibiotics) to compete against other microbes. Thus using chemicals against larger competitors might be expected and could redirect significant energy subsidies from upper trophic levels to the detrital pathway. When we baited traps in a coastal marine ecosystem with fresh vs. microbe-laden fish carrion, fresh carrion attracted 2.6 times as many animals per trap as microbe-laden carrion. This resulted from fresh carrion being found more frequently and from attracting more animals when found. Microbe-laden carrion was four times more likely to be uncolonized by large consumers than was fresh carrion. In the lab, the most common animal found in our traps (the stone crab Menippe mercenaria) ate fresh carrion 2.4 times more frequently than microbe-laden carrion. Bacteria-removal experiments and feeding bioassays using organic extracts of microbe-laden carrion showed that bacteria produced noxious chemicals that deterred animal consumers. Thus bacteria compete with large animal scavengers by rendering carcasses chemically repugnant. Because food-fall resources such as carrion are major food subsidies in many ecosystems, chemically mediated competition between microbes and animals could be an important, common, but underappreciated interaction within many communities.
Integrating prey defensive traits: contrasts of marine worms from temperate and tropical habitats

(Georgia Institute of Technology, 2006-05) Kicklighter, Cynthia Ellen ; Hay, Mark E.

Marine worms are speciose and numerically prominent members of marine communities where they play critical roles in trophic interactions and in affecting biogeochemical cycles. Despite the ecological importance of this group, little is known about their palatability to, and defenses against, consumers. In addition, most studies of prey defenses in marine organisms have focused on overt, sessile species: few studies have investigated more mobile and behaviorally complex species that could potentially be integrating predator deterrents with refuge use and other escape behaviors. To increase our understanding of consequences of defensive traits among mobile marine prey, we surveyed the palatability of 81 species of worms from the Caribbean and warm-temperate western Atlantic. Thirty-seven percent of the species were unpalatable. Worms with differentially exposed body portions commonly defended exposed feeding appendages with chemical or structural deterrents, while palatable and undefended bodies remained sheltered within structural refuges. Unpalatable worms tended to be brightly colored and sedentary, exposed to epibenthic predators, and to occupy hard substrates. Palatable worms tended to be drab, to live in structural refuges from consumers, to be mobile, and to inhabit unconsolidated sediments. Overall, taxonomy (Sabellidae and Terebellidae) and color were the traits most strongly associated with unpalatability. Unpalatable species appeared less constrained by predation and freer to forage for long periods on higher quality surface sediments or on other invertebrates at the sediment surface (thus, potentially influencing the distribution and abundance of other species). In contrast, palatable species appeared more constrained by predation risk. They fed on lower quality subsurface sediments and foraged at times or locations where consumers were less active. These ecological patterns may be generalized to other soft-bodied prey, such as caterpillars, which show similar trends regarding palatability and lifestyle.
Fishes learn aversions to a nudibranch’s chemical defense

(Georgia Institute of Technology, 2006-01-24) Long, Jeremy D. ; Hay, Mark E.

The nudibranch Doriopsilla pharpa was rejected as food when tethered in the field and when offered to 2 species of co-occurring crabs (the lesser blue crab Callinectes similus and the mud crab Panopeus herbstii) and 2 species of co-occurring fishes (the mummichog Fundulus heteroclitus and the striped blenny Chasmodes bosquianus) in the laboratory. When the fishes were offered squid-based artificial food containing nudibranch extracts (i.e. defended food), both species initially consumed this food, but rapidly developed aversions in subsequent feedings. Although both fishes rapidly learned to reject the food, they learned using different cues. The striped blenny Chasmodes bosquianus regurgitated following the initial feeding and then avoided all food made of squid regardless of whether or not it contained the extract. In contrast, the mummichog Fundulus heteroclitus did not regurgitate, and learned to avoid only food containing the extract; it still consumed squid-based food without the extract. Thus, the mummichog detected the deterrent chemical and avoided only defended food while the striped blenny was a less effective feeder, avoiding both defended and undefended food that tasted like squid. Bioassay-guided separation using the mummichog demonstrated that the sesquiterpene polygodial was responsible for the deterrent effects of the nudibranch extract. This metabolite also resulted in the striped blenny avoiding either squid- or tuna-based food treated with this metabolite.
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.