abstract: The oceans play an essential role in global biogeochemical cycles and in regulating climate. The biological carbon pump, the photosynthetic fixation of carbon dioxide by phytoplankton and subsequent sequestration of organic carbon into deep water, combined with the physical carbon pump, make the oceans the only long-term net sink for anthropogenic carbon dioxide. A full understanding of the workings of the biological carbon pump requires a knowledge of the role of different taxonomic groups of phytoplankton (protists and cyanobacteria) to organic carbon export. However, this has been difficult due to the degraded nature of particles sinking into particle traps, the main tools employed by oceanographers to collect sinking particulate matter in the ocean. In this study DNA-based molecular methods, including denaturing gradient gel electrophoresis, cloning and sequencing, and taxon-specific quantitative PCR, allowed for the first time for the identification of which protists and cyanobacteria contributed to the material collected by the traps in relation to their presence in the euphotic zone. I conducted this study at two time-series stations in the subtropical North Atlantic Ocean, one north of the Canary Islands, and one located south of Bermuda. The Bermuda study allowed me to investigate seasonal and interannual changes in the contribution of the plankton community to particle flux. I could also show that small unarmored taxa, including representatives of prasinophytes and cyanobacteria, constituted a significant fraction of sequences recovered from sediment trap material. Prasinophyte sequences alone could account for up to 13% of the clone library sequences of trap material during bloom periods. These observations contradict a long-standing paradigm in biological oceanography that only large taxa with mineral shells are capable of sinking while smaller, unarmored cells are recycled in the euphotic zone through the microbial loop. Climate change and a subsequent warming of the surface ocean may lead to a shift in the protist community toward smaller cell size in the future, but in light of these findings these changes may not necessarily lead to a reduction in the strength of the biological carbon pump. / Dissertation/Thesis / Ph.D. Biology 2011

abstract: The ocean sequesters more than 25% of the carbon released by anthropogenic action every year, and oligotrophic oceans, such as the Sargasso Sea, are responsible for about 50% of the global carbon export. Pico- and nano-phytoplankton (cells < 5 µm), mostly unicellular eukaryotes (protists) and cyanobacteria, dominate the primary production in the Sargasso Sea; however, little is known about their contribution to the export of carbon into the deep ocean via sinking particles. The overall goal of this study is to examine the link between growth and grazing rates of pico- and nano-phytoplankton and the carbon export in the Sargasso Sea. I investigate three aspects: 1) how microzooplankton grazing and physical forcing affect taxon-specific primary productivity in this region, 2) how these microbial trophic dynamics impact their contribution to the export of particulate matter, and 3) how much pico-phytoplankton, specifically the pico-cyanobacteria Synechococcus and Prochlorococcus, contribute to the carbon export. I collected seawater samples within the sunlit (euphotic) zone, and sinking particles at 150 m depth using particle traps in the Sargasso Sea during the winter and summer seasons of 2011 and 2012. I conducted dilution experiments to determine the growth and grazing rates of the pico- and nano-phytoplankton community, and used 454 pyrosequencing and quantitative Polymerase Chain Reaction to measure the relative and absolute contribution of these primary producers to the plankton community within the euphotic zone and in the sinking particles. I found that micrograzing controls taxon-specific primary production, and that microbial trophic dynamics impact directly the taxonomical composition of the sinking particles. For the first time, I was able to quantify clade-specific carbon export of pico-cyanobacteria and found that, despite their small size, these tiny primary producers are capable of sinking from the surface to the deeper oceans. However, their contribution to the carbon flux is often less than one tenth of their biomass contribution in the euphotic zone. Our study provides a comprehensive approach to better understand the role of pico- and nano-phytoplankton in the carbon cycle of oligotrophic oceans, and a baseline to study changes in the carbon export in future warmer oceans. / Dissertation/Thesis / Doctoral Dissertation Natural Science 2016

abstract: Microzooplankton, mainly heterotrophic unicellular eukaryotes (protists), play an important role in the cycling of nutrients and carbon in the sunlit (euphotic) zone of the world’s oceans. Few studies have investigated the microzooplankton communities in oligotrophic (low-nutrient) oceans, such as the Sargasso Sea. In this study, I investigate the seasonal and interannual dynamics of the heterotrophic protists, particularly the nanoflagellate, dinoflagellate, and ciliate communities, at the Bermuda Atlantic Time Series site and surrounding areas in the Sargasso Sea. In addition, I test the hypotheses that the community is controlled though bottom-up and top-down processes. To evaluate the bottom-up hypothesis, that the protists are controlled by prey availability, I test whether the protist abundance co-varies with the abundance of potential prey groups. Predation experiments with zooplankton were conducted and analyzed to test top-down control on the protists. I found distinguishable trends in biomass of the different protist groups between years and seasons. Nanoflagellates and dinoflagellates had higher biomass during the summer (28 ± 5 mgC/m2 and 44 ± 21 mgC/m2) than during the winter (17 ± 8 mgC/m2 and 30 ± 11 mgC/m2). Ciliates displayed the opposite trend with a higher average biomass in the winter (15 ± 9 mgC/m2) than in summer (5 ± 2 mgC/m2). In testing my bottom-up hypothesis, I found weak but significant positive grazer/prey relationships that indicate that nanoflagellates graze on picophytoplankton in winter and on the pico-cyanobacterium Prochlorococcus in summer. I found evidence that ciliates graze on Synechococcus in winter. I found weak but significant negative correlation between dinoflagellates and Prochlorococcus in summer. The predation experiments testing the top-down hypothesis did not show a clear top-down control, yet other studies in the region carried out during our investigation period support predation of the protists by the zooplankton. Overall, my results suggest a combination of bottom-up and top-down controls on these heterotrophic protists, however, further investigation is necessary to reveal the detailed trophic dynamics of these communities. / Dissertation/Thesis / Masters Thesis Biology 2016

<p> The work in this dissertation represents an attempt to investigate multiple temporal and spatial scales of inquiry relating to the variability of marine resources throughout the Gulf of Mexico large marine ecosystem (Gulf LME). This effort was undertaken over two spatial extents within the greater Gulf LME using two different time-series of fisheries monitoring data. Case studies demonstrating simple frameworks and best practices are presented with the aim of aiding researchers seeking to reduce errors and biases in scientific decision making. Two of the studies focused on three years of groundfish survey data collected across the West Florida Shelf (WFS), an ecosystem that occupies the eastern portion of the Gulf LME and which spans the entire latitudinal extent of the state of Florida. A third study was related to the entire area covered by the Gulf LME, and explored a 30-year dataset containing over 100 long-term monitoring time-series of indicators representing (1) fisheries resource status and structure, (2) human use patterns and resource extractions, and (3) large- and small-scale environmental and climatological characteristics. Finally, a fourth project involved testing the reliability of a popular new clustering algorithm in ecology using data simulation techniques.</p><p> The work in Chapter Two, focused on the WFS, describes a quantitatively defensible technique to define daytime and nighttime groundfish assemblages, based on the nautical twilight starting and ending times at a sampling station. It also describes the differences between these two unique diel communities, the indicator species that comprise them, and environmental drivers that organize them at daily and inter-annual time scales. Finally, the differential responses in the diel, and inter-annual communities were used to provide evidence for a large-scale event that began to show an environmental signal in 2010 and subsided in 2011 and beyond. The event was manifested in the organization of the benthic fishes beginning weakly in 2010, peaking in 2011, and fully dissipating by 2012. The biotic effects of the event appeared to disproportionately affect the nighttime assemblage of fishes sampled on the WFS.</p><p> Chapter Three explores the same WFS ecosystem, using the same fisheries-independent dataset, but also includes explicit modeling of the spatial variability captured by the sampling program undertaking the annual monitoring effort. The results also provided evidence of a disturbance that largely affected the nighttime fish community, and which was operating at spatial scales of variability that were larger than the extent of the shelf system itself. Like the previous study, the timing of this event is coincident with the 2010 <i>Deepwater Horizon</i> oil spill, the subsequent sub-marine dispersal of pollutants, and the cessation of spillage. Furthermore, the spatial models uncovered the influence of known spatial-abiotic gradients within the Gulf LME related to (1) depth, (2) temperature, and (3) salinity on the organization of daytime groundfish communities. Finally, the models developed also described which non-spatially structured abiotic variables were important to the observed beta-diversity. The ultimate results were the decomposition of the biotic response, within years and divided by diel classification, into the (1) pure-spatial, (2) pure-abiotic, (3) spatial-abiotic, and (4) unexplained fractions of variation. </p><p> Chapter Five employs a clustering technique to identify regime states that relies on hypothesis testing and the use of resemblance profiles as decision criteria. This clustering method avoids some of the arbitrary nature of common clustering solutions seen in ecology, however, it had never been rigorously subjected to numerical data simulation studies. Therefore, a formal investigation of the functional limits of the clustering method was undertaken prior to its use on real fisheries monitoring data, and is presented in Chapter Four. The results of this study are a set of recommendations for researchers seeking to utilize the new method, and the advice is applied in a case study in Chapter Five.</p><p> Chapter Five presents the ecosystem-level fisheries indicator selection heuristic (EL-FISH) framework for examining long-term time-series data based on ecological monitoring for resources management. The focus of this study is the Gulf LME, encompassing the period of 1980-2011, and it specifically sought to determine to what extent the natural and anthropogenic induced environmental variability, including fishing extractions, affected the structure, function, and status of marine fisheries resources. The methods encompassed by EL-FISH, and the resulting ecosystem model that accounted for ~73% of the variability in biotic resources, allowed for (1) the identification and description of three fisheries resource regime state phase shifts in time, (2) the determination of the effects of fishing and environmental pressures on resources, and (3) providing context and evidence for trade-offs to be considered by managers and stakeholders when addressing fisheries management concerns. The EL-FISH method is fully transferrable and readily adapts to any set of continuous monitoring data. (Abstract shortened by ProQuest.)</p><p>

<p> Burial is an important life history strategy employed by benthic fishes that has not been fully explored in its diversity by the biomechanical literature. This thesis explores the mechanism by which the Pacific sandfish buries as well as the physical limitations of the behavior. We first investigate the role of the ventilatory pump in the burial behavior of sandfish by using high-speed videography, dye, and digital particle image velocimetry (DPIV). We determined that sandfish employ a modification of the ventilatory pump, which is used repeatedly to fluidize the substrate ventral to the head. This modification of the ventilatory pump should reduce the energetic costs associated with burial as it decreases the cost of transport typically associated with &lsquo;shoveling&rsquo; substrate. Second, we investigate the physical limitations that are caused by the reliance on the ventilatory pump to fluidize substrate. We used sand beds of varying grain sizes, and therefore varied the minimum velocities of fluidization, to determine how sandfish respond variation in substrata. We determined that sandfish can bury in grains smaller than 1.00mm in diameter but were unable to bury in any substrate larger than 1.00mm. We also determined that there was an increase in the time it took sandfish to bury in those substrates smaller than 1.00mm as grain size increased. There was no change in the frequency of the behavior, however, suggesting that sandfish have very little ability to bury in larger substrates. We also determined that it is probably not the absolute velocity produced by the opercular jet that determines burial success, but the ability burying behavior to maintain the sand&rsquo;s momentum during the expansive phase that occurs between bouts of opercular jetting.</p>

<p> SEM observations have revealed unknown and previously undetected stages of the bloom-forming dinoflagellate Prorocentrum growing inside calcium carbonate-encrusted perithallial cells of the rhodolith-forming Lithothamnion sp. (Hapalidiaceae, Hapalidiales, Rhodophyta) in the NW Gulf of Mexico. Roundish structures inside the coralline cells were clustered together, surrounded by a thin membrane. Organized blebs, projections of the cytoplasm into the plasma membrane, as well as a suite of varying extracellular ornamentation patterns, were observed. Openings on the surface of some of the structures looked like characteristic thecal pores found in thecal plates of some dinoflagellates. DNA was extracted from inside the rhodolith and sequenced using dinoflagellate-specific cob1-primers. When blasting the resulting DNA sequences, it proved to be an exact match for Prorocentrum lima. Cells were isolated from inside the rhodoliths and cultured, revealing the presence of another set of endolithic life stages identified as Haptophyta (Prymnesiophyta), confirmed by single cell 18S rDNA sequencing. This research illustrates and illuminates newly found benthic life history stages of two ecologically important taxa of primary producers that also cause harmful algal blooms, such as the formation of red tides, fish kills, or shellfish poisoning events in the Gulf of Mexico. </p>

<p> Shallow subtidal epibenthic communities worldwide are under threat from exploitation, pollution, eutrophication, acidification, climate change, and invasive species, with implications for ecosystem diversity, productivity, function, and services. Subtidal ecosystems in the Gulf of Maine are particularly impacted, making it crucial to understand these habitats so that our impacts can be predicted and mitigated. I investigated the basic ecological forces that structure shallow subtidal epibenthic communities in this region, and how invasive species integrate themselves into these communities. I used community phylogenetic and functional trait analyses to investigate if invertebrate communities in the rocky subtidal are assembled via deterministic or random forces, experimental manipulations to quantify how macroalgae might influence sessile invertebrates on subtidal surfaces, and measurements of life history traits of <i>Botrylloides violaceus</i>, an invasive colonial ascidian, to estimate whether growth of this species differs among man-made versus natural habitats. Based on community phylogenetic analyses, rocky subtidal invertebrate communities appear to be structured by deterministic forces, with evidence for both competitive exclusion and environmental filtering operating at different spatial scales. These findings support existing studies that show that competition structures communities at local scales, and also expand our knowledge of the processes that act regionally, i.e. environmental filtering. On shallow sunlit experimental surfaces suspended from floating docks, macroalgae had little effect on invertebrate abundance or diversity, contrary to findings from experiments in the rocky subtidal. Macroalgae did influence composition as well as enhance invertebrate colonization in the early stages of community assembly. Different factors appear to influence the balance between heterotrophs and autotrophs in floating dock and rocky subtidal systems with implications for community structure, function and productivity. In different habitats, colonies of the invasive ascidian B. violaceus exhibited differences in life history traits. It grew faster and attained larger sizes in man-made floating dock versus natural rocky subtidal and eelgrass bed habitats. Again, differences among habitats appear to influence invasion success. In conclusion, competitive exclusion, facilitation, and environmental filtering play key roles in controlling the structure, composition, and function of shallow subtidal communities. Invasive species have the potential to disrupt these forces as they integrate themselves into man-made and subsequently natural habitats.</p>

<p>Most of the seafloor is soft sediment, so hard substrata are isolated and island-like. In this dissertation, I explore how species distribution patterns on isolated marine hard substrata resemble terrestrial island communities, drawing on classical island biogeography theory and assembly rules, and describe how benthic invertebrate communities assemble in these island-like habitats. Higher species richness occurred on larger substrata (dropstones and shipwrecks), paralleling terrestrial island communities. However, while larger islands have greater habitat diversity and primary productivity, marine hard substrata are simpler habitats. Greater elevation in the benthic boundary layer may expose fauna to faster current, higher food supply and larval flux. Substrata located closer together had more similar communities, another pattern that resembles terrestrial islands. Dropstone fauna had a clumped distribution, indicating that larvae may disperse among substrata located close together, resulting in similar communities. In Svalbard fjords, benthic megafaunal communities were significantly different between Arctic- and Atlantic-influenced fjords. Depth and temperature had the greatest influence, with the highest diversity occurring in cold Rijpfjorden and on the north Svalbard shelf. Recruitment in Svalbard fjords was spatially and temporally variable, with lower recruitment in Rijpfjorden than in Atlantic-influenced fjords and lower recruitment at greater depth. Most of the recruits in Svalbard fjords were fast-growing, poor-competitive opportunists. On shipwrecks, communities showed two mechanisms of colonization: mobile fauna with long-dispersing planktotrophic larvae, and encrusting fauna with lecithotrophic larvae. Encrusting species reproduce asexually to cover the wreck surface, and philopatry may build up dense populations, leading to uneven communities. On terrestrial islands, non-random co-occurrence is attributed to interspecific competition, but for marine substrata, there may not be a relationship. Fauna were distributed randomly on settlement plates in Svalbard fjords, even when interspecific competition was observed. On dropstones, some morphotypes co-occurred non-randomly in the absence of overgrowth competition. Non-random co-occurrence on isolated marine hard substrata may be a result of restricted larval dispersal (for pairs co-occurring less than by chance) or epibiontism (for pairs co-occurring more often than by chance). While species distribution patterns on island-like marine hard substrata resemble terrestrial islands, the mechanisms are not necessarily the same.

<p> Recruitment of marine fishes is largely determined by biological and oceanographic factors acting on early life stages. Coastal upwelling has long been recognized as a critical factor influencing the survival of larvae and recruitment to adult populations. Dynamics in regional upwelling influence the magnitude and timing of primary productivity, affecting the availability of critical food sources for larval fish. In addition, upwelling-relaxation cycles affect the dispersal of marine larvae and their onshore delivery prior to settlement. Challenges with tracking larvae, however, have limited our understanding of how oceanography influences the early life stages of fishes. The objective of this dissertation is to evaluate the biological and oceanographic drivers of larval growth, settlement, and recruitment, using rockfishes (<i> Sebastes</i> spp.) as model organisms. </p><p> Overlap of larval production and favorable feeding conditions may drive recruitment for many temperate marine fishes, as small changes in larval growth can result in order-of-magnitude differences in year-class-strength. In Chapter 1, I assess the influence of regional productivity, temperature, and larval condition in explaining growth in rockfishes. I employ a combination of otolith microstructure and satellite imagery to measure initial larval growth and estimate the productivity and temperature experienced by individuals to determine their relative importance in subsequent growth at metamorphosis. I compare model performance using indexed environmental conditions scaled over three different regions. In both years of study, net primary productivity explained the most variation in pre-metamorphic growth relative to temperature and initial growth. This relationship was consistent across spatial regions. Recent settlement, juvenile recruitment, and individual growth were significantly higher in a year when productivity bloomed earlier and individual larvae experienced higher levels of productivity. These results support the hypothesis that large-scale oceanographic processes that stimulate upwelling and secondary production are primary drivers of larval growth and subsequent year-class strength in rockfishes.</p><p> Characterizing the behavior of larvae prior to settlement is integral to understanding population dynamics because coastal oceanography may facilitate or limit settlement. Otolith microchemistry can be used to determine patterns of fish movement, although there is a limited understanding of how this tool can be applied in coastal marine systems. My goal in Chapter 2 is to evaluate the application of otolith microchemistry to characterize water mass associations of settlement-stage marine fish in a coastal upwelling region using a three-step approach. First, I characterize seawater chemistry of coastal water masses across multiple years, finding significant differences in the chemical signatures of strong upwelling, weak upwelling, and relaxation. Second, I experimentally determine the effect of temperature on the partitioning of trace elements in otoliths for two rockfishes to find that the effect of temperature on otolith partition coefficients was element- and species-specific. Finally, I compare the synchrony in seawater and otolith chemistry of settlement-stage rockfishes that were exposed to naturally variable conditions over an upwelling-relaxation cycle. I subsequently evaluate whether laser ablation inductively coupled plasma mass spectrometry effectively measures otolith chemistry over ecologically relevant time scales. I discovered that elemental concentrations in otoliths respond rapidly to changes in seawater chemistry and reflect equivalent proportional changes. This study provides evidence that elemental signatures are valuable tools for reconstructing larval histories of marine fish.</p><p> In Chapter 3, I use otolith chemistry to examine water mass associations of two juvenile rockfishes during onshore transport and settlement in an upwelling region. I develop a chemical proxy for upwelling and relaxation by characterizing Sr/Ca and Ba/Ca signatures of otoliths collected during these oceanographic conditions. Otolith chemistry differed between rockfishes collected during upwelling and relaxation, with signatures unique to each year. I subsequently compare otolith signatures of rockfishes collected during high and low settlement periods to determine whether specific water masses affect settlement. I provide evidence that copper rockfish associate with upwelling currents during periods of high settlement, suggesting that upwelling may facilitate settlement for these species. Conversely, I found evidence that the closely related gopher rockfish associate with relaxation events during peak settlement periods. This research takes an important first step at in evaluating the utility of trace element signatures to characterize larval fish movement during onshore delivery and settlement in marine systems. Together, these studies improve our understanding of how coastal upwelling impacts larval growth, settlement, and recruitment, which provides important information for understanding population dynamics in marine ecosystems.</p>

<p> Ocean acidification can reduce survival and growth of marine larvae. However, if populations have the genetic capacity to adapt and increase their tolerance to low pH levels, then such genetic changes may offset the harmful effects of ocean acidification. I used methods in quantitative genetics to measure the genetic variance and project the potential rate of evolution for low pH tolerance in a nearshore forage-fish: the California grunion (<i> Leuresthes tenuis</i>). I raised grunion larvae across an experimental pH gradient and measured their mortality and growth rates over a 14-day interval during the early larval stage. My results indicated that low pH levels significantly decreased the survival rates of grunion larvae overall. Surprisingly, low pH levels did not significantly affect larval growth rates. However, families varied widely with respect to pH tolerance, and many families had similar mortality and growth rates in high and low pH treatments. Quantitative genetic analyses indicated that low pH tolerance had a substantial genetic basis and is highly heritable within grunion populations. These results suggest that populations of California grunion, and possibly other nearshore fishes, may adapt relatively quickly to long-term changes in ocean pH.</p><p>