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Anthropogenic-Mediated Simplification of Marine Food Webs

2022-12-08 , Willert, Madison Shari

Anthropogenic-mediated stressors such as overexploitation, habitat destruction, climate change, and species introductions are changing food webs in marine ecosystems. In this dissertation, I first evaluate how these stressors are shifting trophic interactions via increased dietary overlap and interspecific competition within trophic levels, truncation of nutrient flow between trophic levels and ecosystems, and simplification and compression of entire food webs. Stable isotope analysis is a powerful tool to measure species’ trophic positions and thus, food web shifts over time and space. I show that δ15N values and δ13C values from formalin-preserved seaweeds are generally reliable, validating stable isotope analysis of herbarium specimens. Seaweeds are useful as nutrient baselines for trophic ecology studies, as well as for assessing nutrient runoff and pollution; this finding shows that preserved herbarium specimens can be used in these types of studies to reconstruct food webs of the past. I then use nitrogen stable isotope analysis of both herbarium specimens and museum fish specimens from New England, USA to show that the common piscivore Centropristis striata (black sea bass) and the common benthivore Stenotomus chrysops (scup) have experienced significant declines in trophic position in this area since pre-1950. Centropristis striata declined almost a full trophic level and Stenotomus chrysops declined half a trophic level, and these species are now converging on similar trophic positions coincident with the increase in destructive bottom fishing in New England. Next, I used nitrogen stable isotope analysis of >1000 museum fish specimens from coral reefs worldwide to assess dietary changes of common coral reef mesopredators since 1850 in regions of both the tropical Atlantic and the Indo-Pacific. I found that trophic instability has been common in the tropical Atlantic during the 20th century, with the trophic position of most Atlantic species decreasing further going into the 21st century. Unlike in the Atlantic, historically unstable species in the Indo-Pacific are now increasing in their trophic positions; this suggests that relatively higher levels of overfishing and coral loss in the tropical Atlantic are reflected in greater mesopredator trophic instability. Finally, I used nitrogen and carbon stable isotope analysis of vertebrae from Sphyrna mokarran (great hammerhead) and Sphyrna lewini (scalloped hammerhead) sharks to evaluate ontogenetic shifts in these two species in the U.S. South Atlantic and the eastern Gulf of Mexico. Sphyrna lewini occupies a high trophic position throughout its life, reaching peak predator status as a subadult and occupying more offshore pelagic habitats. Despite its larger body size, Sphyrna mokarran occupies a lower trophic position and relies more on benthic and inshore habitats, especially in the juvenile stage. I elucidated the nuances of these predators’ trophic ecology and found no evidence of within-species differences in sex or location with regards to dietary habits. A better understanding of individual species’ trophic ecology, as well as historic human impacts on marine food webs, is crucial to maintaining and promoting healthy ecosystems into the future.

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Developing appropriate methodology for assessing anti-pathogen properties of mucus-enriched water from corals

2019-05 , Jarvis, Simone

Global coral reef health is in rapid decline. A major contributor to this trend is warming ocean temperatures. As ocean temperature increases, corals become more susceptible to diseases that lead to bleaching and tissue mortality. Vibrio coralliilyticus is one of the few documented coral bleaching pathogens. Previous studies developed methods to quantify V. coralliilyticus metabolism and developed culturing procedures to test the anti-Vibrio potency of mucus-enriched water from numerous coral species. However, the best way to collect and process mucus-enriched water from corals was not determined. Previous efforts obtained mucus-enriched water via coral fragmentation and agitation in seawater. This methodology detected anti-Vibrio activity from several species, but required destructive sampling of the corals. This prevents collecting data over multiple time points without confounding time with previous damage. This study evaluates the effectiveness of less destructive methodologies for sampling mucus-enriched coral water. This study evaluated the effectiveness of the less destructive method of slowly sucking coral mucus from colonies in the field using a syringe. Tests using this method on mucus enriched water from 9 species of coral detected no anti-pathogen activity. In contrast, tests using the fragmentation and shaking method found significant anti-pathogen activity in 3 of the 4 species tested. the less destructive method assayed here, is ineffective at assessing the anti-pathogen potential of corals.

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Acclimating across healthy and degraded reefs

2016-05-31 , Dell, Claire Louise Alice

As a result of human activities, many environments are becoming fragmented into areas with different community compositions and selective regimes. The coral reefs of Fiji for example, are divided into ‘fished areas’ (fragments subjected to fishing and trampling) and ‘protected areas’ (fragments with little human pressure) that occur in close proximity and now have differing community compositions and selective regimes. Theory predicts that the species able to survive in such conditions should have highly plastic genotypes allowing them to acclimatise to diverse habitats without the time lag required for local adaptation. Here we use two species -Epinephelus merra (a small grouper) and Sargassum polycystum C. Agardh (a brown macroalga)- which are found in both fished and protected reefs, to investigate this plastic response and understand how these species cope in healthy versus degraded environments. We found that the fish E. merra exhibits plasticity in diet and feeds lower in the food chain in fished reefs than similarly sized conspecifics in protected reefs. The seaweed S. polycystum exhibits plasticity in defensive traits and is able to induce increased defenses in response to being partially consumed. In addition, we found that dense stands of S. polycystum increased the survival and growth of both recruit-sized and mature-sized S. polycystum ramets, suggesting that Sargassum beds protect conspecifics from grazing by herbivorous fishes and construct conditions that facilitate their growth. Implications for management are discussed.

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Chemically mediated competition, herbivory, and the structure of coral reefs

2012-07-03 , Rasher, Douglas B.

Corals, the foundation species of tropical reefs, are in rapid global decline as a result of anthropogenic disturbance. On many reefs, losses of coral have coincided with the over-harvesting of reef herbivores, resulting in ecosystem phase-shifts from coral to macroalgal dominance. It is hypothesized that abundant macroalgae inhibit coral recovery and recruitment, thereby generating ecological feedback processes that reinforce phase-shifts to macroalgae and further diminish reef function. Notwithstanding, the extent to which macroalgae directly outcompete coral, the mechanisms involved, and the species-specificity of algal-coral competition remains debated. Moreover the capacity for herbivores to prevent vs. reverse ecosystem phase-shifts to macroalgae and the roles of herbivore diversity in such phenomena remain poorly understood. Here I demonstrate with a series of field experiments in the tropical Pacific and Caribbean Sea that multiple macroalgae common to degraded reefs directly outcompete coral using chemical warfare, that these interactions are mediated by hydrophobic secondary metabolites transferred from algal to coral surfaces by direct contact, and that the outcomes of these allelopathic interactions are highly species-specific. Using field observations and experiments in the tropical Pacific, I also demonstrate that the process of herbivory attenuates the competitive effects of allelopathic algae on corals by controlling succession of algal communities, and that the herbivore species responsible for macroalgal removal possess complementary tolerances to the diversity of chemical defenses deployed among algae, creating an essential role for herbivore diversity in reversing ecosystem phase-shifts to macroalgae. Lastly, I demonstrate with field experiments in the tropical Pacific that algal-coral competition simultaneously induces allelochemicals and suppresses anti-herbivore deterrents in some algae, likely due to trade-offs in the productions of defense metabolites with differing ecological functions. Together, these studies provide strong evidence that chemically mediated competitive and consumer-prey interactions play principal roles in coral reef degradation and recovery, and should provide resource managers with vital information needed for effective management of these ecologically and economically important but threatened ecosystems.

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Impact of parrotfish predation on coral health: changes in microbiome and pathogen defense

2021-05 , Towner, Alexandra

Coral reefs are in rapid decline, and it is imperative to study reef community interactions in order to mitigate and reverse this trajectory. This study explores the relationship between corals and parrotfish, investigating how parrotfish bites on coral impact the composition of the coral’s microbiome and the corals suppression of a common bacterial pathogen. Fragments of Porites lobata coral colonies that were heavily predated by parrotfish or that showed no signs of parrotfish predation were shaken in seawater, and this seawater was bioassayed against the common coral pathogen Vibrio coralliilyticus to assess the effects of previous predation on the coral’s ability to suppress this ecologically relevant pathogen. Additionally, we sequenced the 16S rRNA gene from each coral sample to investigate possible alterations of the coral’s microbiome due to predation. Neither alpha diversity nor beta diversity of the microbiome was impacted by parrotfish predation. However, some bacteria were differentially abundant, such as those of the genus Endozoicomonas. Bioassays of water in which coral fragments were agitated detected no impact of previous parrotfish attack on the coral’s suppression of the pathogen Vibrio coralliilyticus. Overall, this speaks to the resistance and strength that corals demonstrate in the face of parrotfish predation.

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Effects of macroalgal versus coral reef dominance on coral survival, chemical defense, and microbiomes

2018-10-24 , Beatty, Deanna S.

Coral reefs are among the earth’s most biodiverse and productive ecosystems, but are undergoing precipitous decline due to coral bleaching and disease following thermal stress events, which are increasing in frequency and spatial scale. These effects are exacerbated by local stressors such as overfishing and pollution, collectively causing an increasing number of reefs to shift from coral to macroalgal dominance. These stressors can harm or kill corals through diverse mechanisms, including alterations in how corals interact with microorganisms. By employing a variety of field sampling and field experimental approaches, I investigated consequences of local protection from fishing and coral versus macroalgal dominance of the benthos on coral survival, chemical defense, and microbiomes within paired algal dominated fished areas and coral dominated marine protected areas (MPAs) in Fiji. I demonstrate that i) coral larvae from a macroalgal dominated area exhibited higher pre-settlement mortality and reduced settlement compared to those from a coral dominated area, ii) juveniles planted into a coral dominated MPA survived better than those planted into a macroalgal dominated fished area and differential survival depended on whether macroalgae were immediately adjacent to juvenile coral, iii) corals possess chemical defenses toward the thermally-regulated coral bleaching pathogen Vibrio coralliilyticus, but this defense is compromised by elevated temperature, iv) for a bleaching susceptible but ecologically important acroporid coral, anti-pathogen chemical defense is compromised when coral resides within macroalgal dominated reefs and this effect can be influenced by both the current and historic state of the reef. Effects on coral survival and chemical defense for individuals residing within coral versus macroalgal dominated areas largely coincided with nuanced differences in coral microbiomes (e.g., in microbiome variability and specific indicator bacterial taxa) but not with major shifts in microbiome composition. These findings have implications for reef conservation and for understanding how coral-microbe interactions will respond to the pressures of global change.

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Interactions between ecosystems and disease in the plankton of freshwater lakes

2013-11-18 , Penczykowski, Rachel M.

I investigated effects of environmental change on disease, and effects of disease on ecosystems, using a freshwater zooplankton host and its fungal parasite. This research involved lake surveys, manipulative experiments, and mathematical models. My results indicate that ecosystem characteristics such as habitat structure, nutrient availability, and quality of a host’s resources (here, phytoplankton) can affect the spread of disease. For example, a survey of epidemics in lakes revealed direct and indirect links between habitat structure and epidemic size, where indirect connections were mediated by non-host species. Then, in a mesocosm experiment in a lake, manipulations of habitat structure and nutrient availability interactively affected the spread of disease, and nutrient enrichment increased densities of infected hosts. In a separate laboratory experiment, poor quality resources were shown to decrease parasite transmission rate by altering host foraging behavior. My experimental results also suggest that disease can affect ecosystems through effects on host densities and host traits. In the mesocosm experiment, the parasite indirectly increased abundance of algal resources by decreasing densities of the zooplankton host. Disease in the experimental zooplankton populations also impacted nutrient stoichiometry of algae, which could entail a parasite-mediated shift in food quality for grazers such as the host. Additionally, I showed that infection dramatically reduces host feeding rate, and used a dynamic epidemiological model to illustrate how this parasite-mediated trait change could affect densities of resources and hosts, as well as the spread of disease. I discuss the implications of these ecosystem–disease interactions in light of ongoing changes to habitat and nutrient regimes in freshwater ecosystems.

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Climate change & the physiology, ecology, and behavior of coral reef organisms

2020-03-16 , Johnston, Nicole K.

The magnitude of ocean acidification (OA) and warming predicted to occur within the next century could have significant negative effects for organisms that inhabit coral reefs. Our understanding of how these stressors will impact coral reef organisms is complicated by the diverse behavioral and ecological interactions that exist on these reefs. In a series of experiments, I explored interactions between coral reef organisms, evaluated how some of these interactions may be affected by OA and warming, and then studied how environment may shape an organism’s response to a changing climate. First, through a sensory manipulated tank and a twochamber choice flume, I demonstrated that anemonefish respond to both chemical and visual conspecific cues, but they require a combination of these two cues to correctly identify conspecifics. Given that previous research indicates that fish behavioral responses to chemical cues are altered under conditions of future OA, this inability to compensate for the loss of one cue through a second cue could affect their ability to acclimate as climate changes. Second, I found that the common Caribbean mounding coral Porites astreoides, is unaffected by competition with Montastraea cavernosa and Orbicella faveolata under ambient environmental conditions, but exhibits significant reductions in photosynthetic efficiency in areas of direct contact with M. cavernosa and O. faveolata under conditions of elevated CO2 and temperature that are anticipated to occur by the year 2100. These results demonstrated that climate change can interact with competition to alter the rate and severity of coral-coral interactions on reefs of the future. Next, I compared the effects of OA and warming on the physiology of two congeneric coral species (Oculina arbuscula and Oculina diffusa) representing temperate (O. arbuscula) and tropical (O. diffusa) environments and found that, although both corals were negatively impacted by ocean acidification and warming, the temperate coral was slightly more resistant to these stressors. This suggests that temperate species may not be as disadvantaged by climate change as one might expect and may not be easily displaced by more tropical species moving poleward as global oceans warm. Finally, I evaluated the effect of elevated temperature on the well-being of the temperate coral, O. arbuscula when collected from deeper more physically stable environments versus shallower more physically variable environments. I found that corals from both deep and shallow sites were negatively impacted by elevated temperature, but that corals from deeper sites were more strongly impacted. These findings suggest that the physiologies, biotic interactions, and behaviors of reef organisms may all be affected by climate change and that outcomes of these interactions may not be simple to predict as global oceans warm and acidify and as tropical organisms shift poleward and intermix with temperate species to form novel communities.

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Predation, competition, and facilitation on tropical reefs: implications for corals as reefs degrade 

2017-11-13 , Clements, Cody Shane

Tropical coral reefs are among the most diverse and productive ecosystems on Earth, but reefs worldwide have experienced dramatic declines in coral and often transitioned from coral- to macroalgal dominance. As local and global threats to corals increase in severity and frequency, there is an urgent need to understand how reef degradation, as well as efforts to manage and restore corals, are reshaping ecological interactions that are critical to the function of coral reef ecosystems. Here, I utilize a range of experimental approaches to investigate how interactions between corals, competing macroalgae, and coral predators (i.e. corallivores) are being altered within mosaics of coral reef habitat characterized by different levels of degradation and local protection in the tropical Pacific. I first demonstrate, via a series of field observations and experiments, the direct negative effects of competition for corals competing with macroalgae that commonly dominate degraded reefs, including the spatial and temporal constraints of these competitive interactions, as well as the indirect positive effects that can arise due to the presence of a common coral predator, the crown-of-thorns sea star (Acanthaster cf. planci). I also provide observational and experimental evidence that protected reefs can help alleviate predation by corallivorous snails (Coralliophila violacea) for some stress-tolerant corals (Porites cylindrica), but that stark habitat contrasts between coral-dominated protected reefs and macroalgal-dominated fished reefs can simultaneously attract and concentrate feeding by other corallivores (Acanthaster cf. planci) – potentially contributing to coral demise and compromising the conservation value of small Marine Protected Areas. Lastly, I use a field-based manipulative experiment to explore the implications of coral species loss for ecosystem function on degraded reefs; demonstrating that greater coral species richness can enhance coral growth and survivorship, and reduced colonization by competing macroalgae. Together, these studies highlight the need to better understand the novel and context-dependent role of ecological interactions – both for fundamental ecology and effective management – in rapidly changing ecosystems subject to increasing disturbances.

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Seaweed allelopathy against coral: surface distribution of seaweed secondary metabolites by imaging mass sepctrometry

2012-08-16 , Andras, Tiffany D.

Coral reefs are in global decline, with seaweeds increasing as corals decrease. Though seaweeds have been shown to inhibit coral growth, recruitment, and survivorship, the mechanism of these interactions is poorly known. Here we use field experiments to show that contact with four common seaweeds induces bleaching on natural colonies of Porites rus. Controls in contact with inert, plastic mimics of seaweeds did not bleach, suggesting treatment effects resulted from allelopathy rather than shading, abrasion, or physical contact. Bioassay-guided fractionation of the hydrophobic extract from the red alga Phacelocarpus neurymenioides revealed a previously characterized antibacterial metabolite, Neurymenolide A, as the main allelopathic agent. For allelopathy of lipid soluble metabolites to be effective, the metabolites would need to be deployed on algal surfaces where they could transfer to corals on contact. We used desorption electrospray ionization mass spectrometry (DESI-MS) to visualize and quantify Neurymenolide A on the surface of P. neurymenioides and found the metabolite on all surfaces analyzed. The highest concentrations of Neurymenolide A were on basal portions of blades where the plant is most likely to contact other benthic competitors.

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