Ph.D. - Marine Biology

Permanent URI for this collectionhttps://hdl.handle.net/10125/61892

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Phylogeography, dispersal, and invasion pathways of marine Rhodophyta in Hawai‘i and the Pacific
(University of Hawai'i at Manoa, 2025) Fumo, James T.; Sherwood, Alison R.; Marine Biology
Dispersal capacity of organisms in marine ecosystems explains population structure, biogeography, and phylogeography, and should be considered in ecosystem management. Understanding dispersal is particularly important for marine macroalgae, which are the foundation of marine ecosystems and provide numerous ecosystem services. Red algae, however, face numerous biological constraints limiting dispersal by propagules, which are negatively buoyant, non-flagellated, and attach rapidly to substrates. As such, dispersal to and within the remote Hawaiian archipelago may be difficult. Though long-distance dispersal by propagules is limited, it can be achieved by rafting on flotsam, which is increasingly abundant in the oceans. Hawai‘i’s marine algal biogeography, phylogeography, and dispersal capacities remain poorly understood, particularly in relation to dispersal barriers and the transport of nuisance taxa. Here I show through phylogeographic analyses that there are dispersal barriers for the red alga Amansia glomerata between the islands of Hawai‘i and Maui Nui (Maui, Moloka‘i, Lāna‘i), Maui Nui and O‘ahu, as well as between Kaua‘i and the remote and protected Papahānaumokuākea Marine National Monument (PMNM). These barriers largely match those found in similar studies on marine animals in the archipelago. Further, A. glomerata in Hawai‘i is split into four lineages which overlap in certain parts of their ranges and display a high level of molecular diversity. Assessments of population differentiation between islands yield relatively high values in comparison to animal groups. Comparisons between mesophotic and shallow collections revealed shared haplotypes. These shared haplotypes may provide support for ongoing connectivity between these environments with implications for mesophotic refugia and the habitat persistence of deep reefs. Additionally, through a modeling approach I show that dispersal of the putative non-native red alga Chondria tumulosa is likely aided by marine debris in PMNM. This is concerning as there is an abundance of large, floating, abandoned, lost, or discarded fishing gear in PMNM which acts as a habitat substitute in the open ocean. I also identify the oceanographic conditions and particle properties most likely to transport the species from Manawai (Pearl and Hermes Atoll), the first known location of the species, and show that rafting fragments are more likely to transit between atolls than tetraspores. This aligns with genetic assessments of population connectivity in C. tumulosa, which indicate high rates of asexual fragmentation. This result also helps guide early detection of the species on the atolls and islands to the southeast of Manawai. Finally, I use a backtracking connectivity model to show that the highest likelihood source locations for C. tumulosa are Japan’s Cape Inubo and Izu Islands, Johnston Atoll and the Line Islands, including Palmyra in the central Pacific, and the Galápagos Islands and Clipperton Atoll in the Eastern Tropical Pacific. While the macroalgal flora of PMNM is broadly composed of species that share affinities with Japanese and Indo-Polynesian regions, the model highlights specific source locations which should be targeted in the search for the species outside of the Hawaiian archipelago. I propose a framework for searching within these model-guided potential source locations for C. tumulosa, beginning with eDNA surveys, followed by in-water surveys and DNA barcoding. This method utilizes a recently developed eDNA assay for C. tumulosa, minimizing costs and improving efficiency. An accompanying search for C. tumulosa in global herbaria is presented and identifies 12 species of Chondria which previously lacked genetic information and have distributions overlapping with the model-guided search regions. Collectively, this dissertation focuses on connectivity of macroalgal populations between the islands of the Hawaiian archipelago and beyond using both genetic and modeling approaches. This approach provides a more comprehensive understanding of the biogeography and phylogeography of macroalgae in Hawai‘i and the Pacific. Furthermore, it has broad utility and applicability for the inclusion of algae in inter-island connectivity indices and the assessment of the spread and origin of nuisance species.
Underwater soundscapes and false killer whale acoustic ecology across the Hawaiian archipelago
(University of Hawai'i at Manoa, 2025) Madrigal, Brijonnay Chanel; Pacini, Aude; Marine Biology
Passive acoustic monitoring (PAM) is an effective technique for long-term monitoring of the soundscape in marine protected areas (MPAs). This study leverages long-term PAM data sets from recorders deployed in the Hawaiian Islands Humpback Whale National Marine Sanctuary, Papahānaumokuākea Marine National Monument, and island-associated sites outside the sanctuary to investigate soundscapes and odontocete presence. This dissertation implements a multi-scale PAM approach to large-scale monitoring of MPAs, validates cross-platform detection/classification techniques for lesser-known species in biologically relevant areas, and highlights the importance of representative individual insights to inform our knowledge of animal behavior of an endangered population. In Chapter 1, the underwater soundscape was characterized and compared across multiple sites within the sanctuary. Generally, soundscapes were dominated by biological sources, most prominently the seasonal detection of humpback whale chorusing. Overall, we reported relatively low vessel detection rates. No COVID-19 impact could be observed acoustically using soundscape metrics which was likely due to the dominance of humpback whale chorusing. In order to better understand the habitat use of blackfish within the sanctuary boundaries, in Chapter 2, automated detectors were used on the full repertoire (whistles, clicks, and burst pulses) to determine the presence of these species on the same SanctSound datasets. Our findings revealed diel patterns in detections with relative presence of blackfish being significantly higher at night within the sanctuary. Additional more in-depth analyses were conducted to detect the presence of the false killer whales (Pseudorca crassidens) within the monument and sites outside the sanctuary. Results revealed that false killer whales were detected across all sites with some geographical variation. In Chapter 3, the acoustic behavior of Main Hawaiian Islands insular false killer whales was investigated using non-invasive animal borne tags. Greater repertoire diversity and signal complexity than previously described were observed with 52 stereotyped call types characterized. Predominant call types and call rates across dive states varied by individual. Most calls contained acoustically complex, nonlinear phenomena indicating potential functionality as contact calls when spatially distant. Call rates decreased as swim speed increased, indicating potential behavioral changes in response to conspecifics.
The energetic cost of reproduction and growth in humpback whales
(University of Hawai'i at Manoa, 2025) van Aswegen, Martin; Bejder, Lars; Marine Biology
Recent declines in reproductive output and calf survival among North Pacific humpback whales (Megaptera novaeangliae) underscore the critical need to quantify the energy requirements of mothers and their offspring. This dissertation examines energy allocation to reproduction and growth in humpback whales across their Hawaiian breeding and Southeast Alaskan feeding grounds. Using a comparative framework, I modeled pre- and post-natal energetic demands, incorporating key external and internal factors such as migration, maternal size and body condition, sex, and age. In Chapter 2, I estimated the energetic cost of gestation in humpback whales, encompassing both direct (tissue growth) and indirect costs (metabolic load). I incorporated multiple data streams, including morphometric measurements from historical whaling records (678 mother-fetus pairs) and non-invasive unoccupied aerial system (UAS) photogrammetry (987 mother-calf pairs), and tissue samples from an opportunistically collected placenta and a post-mortem specimen. I demonstrated that energetic costs increase exponentially over gestation, with over 95% of total costs incurred in the final 100 days. This illuminates a critical time period during which pregnant females endure extreme energetic demands while fasting on their southbound migration to the breeding grounds. In Chapter 3, I analyzed 2,410 UAS measurements of 1,659 individual whales, including 803 repeat measurements of 275 individuals, to assess the influence of maternal size and body condition on postnatal offspring investment. Larger females not only produced larger calves at birth, as found in Chapter 2, but their calves also gained body volume faster. Together, findings from Chapters 2 and 3 highlight the critical role of maternal size and condition in mitigating the energetic demands of reproduction, with mass-specific costs decreasing as maternal size increases. Consequently, smaller females face greater energetic trade-offs, potentially reducing maternal investment and leaving both mothers and their offspring more vulnerable to stressors. In Chapter 4, I estimated the energetic cost of growth from birth to 50 years of age by modeling the body length and mass of 1,503 known-age whales. I estimated that postnatal somatic growth requires 38 times more energy compared to prenatal growth, with calves allocating 6-8 times more energy to growth than mature adults. Notably, nearly 30% of a calf’s lifetime somatic growth costs occur within less than 2% of its lifespan. This necessitates that mothers draw extensively on their energy reserves to sustain both their metabolic demands and those of their rapidly growing offspring. These findings advance our understanding of energy allocation around parturition, highlighting the extreme energetic demands on reproductive females and their offspring. By quantifying these costs, this work sheds light on their vulnerability to energy imbalances during migration and enhances our ability to assess the impacts of anthropogenic disturbances and changing ocean ecosystems on life history strategies.
The effects of dissolved inorganic nutrients on thermal responses and recovery of Hawaiian corals
(University of Hawai'i at Manoa, 2025) Han, Ji Hoon Justin; Hunter, Cynthia L.; Marine Biology
My dissertation interest stems from a study in which I participated in 2017 which revisited the thermal thresholds of Hawaiian scleractinian corals first established by Drs. Paul Jokiel and Steven Coles in the 1970s (Jokiel & Coles 1977). This comparative analysis revealed not only an enhanced tolerance of corals to temperature stress but also prompted further inquiry into the role of environmental factors particularly nutrients. Conducted under conditions replicated from the original experiments, the 2017 study (Coles et al. 2018) demonstrated differences in coral survivorship, bleaching severity, and onset of bleaching. These findings suggest that corals have been acclimatizing or adapting to temperatures over the last 47 years, offering a hopeful perspective amidst the current crisis of global coral reef degradation. However, a notable difference in the levels of dissolved inorganic nutrients between the two periods, influenced by unique historical events in Kāne‘ohe Bay, triggered a need for a deeper investigation into how these factors affect the shifted temperature responses.The significance of coral reef ecosystems is often attributed to their limited spatial extent, they cover less than 1% of the ocean floor yet harbor tremendous biodiversity. However, the primary reason these small areas can act as biodiversity hotspots is the coral’s ability to create habitats under nutrient-poor conditions, an environmental scenario often referred to as a 'blue desert' (Dubinsky & Jokiel 1994). Nutrients, while essential for organisms to grow, survive, and reproduce, are considered detrimental to coral reef ecosystems when present in excessive amounts, disrupting the finely tuned balance of these ecosystems. Furthermore, over the past two decades, studies have found that excessive nutrients can synergistically increase the impacts of thermal stress and exacerbate coral bleaching, further underscoring the importance of maintaining stable nutrient levels, especially as ocean temperatures continue to rise due to climate change (Wooldridge 2009; Cunning & Baker 2013; Morris et al., 2019; Done & Wooldridge 2013; D’Angelo & Wiedenmann 2019; Rädecker et al., 2021). Yet, past studies have often focused on the extreme effects of nutrients and a fine-scale, naturally representative regime has not been thoroughly investigated, necessitating further research to better inform management strategies amid this urgent reef crisis. Therefore, my dissertation research seeks to elucidate the complex role of nutrients in scleractinian coral biology, specifically focusing on:I. Exploring changes in nutrient effects on thermal bleaching across time by comparing thermal responses of corals with simulated nutrient conditions from the 1970’s until present. II. Investigating the synergistic effects between the naturally occurring enrichment levels and thermal stress to determine threshold concentrations of ambiguous aspects of the nutrient and coral relationships under thermal stress. III. Testing the effects of mild nutrient enrichment of different nutrient types during postbleaching coral recovery. This research addresses critical aspects of reef stability that are often overshadowed by temperature stress, the impact of changing nutrient regimes in a warming climate. Clarifying the long-debated role of nutrients, which are essential yet potentially harmful, will contribute significantly to our understanding of coral biology and inform conservation efforts aimed at sustaining coral reef ecosystems in the face of ongoing environmental changes.
Data-limited approaches to coral reef fishery management
(University of Hawai'i at Manoa, 2024) Matthews, Toby; Donahue, Megan; Marine Biology
Coral reef fisheries provide vital sustenance and employment to hundreds of millions of humans across small coastal communities. Due to the relatively low value of individual reef fisheries and large number of species caught, common management approaches designed for large-scale fisheries are rarely applicable to reef fisheries. As a result, reef fisheries are consistently data-limited and most lack any form of management. Meta-analyses indicate that the majority of reef fisheries are overfished, so we must identify cost-effective surveys, assessments, and control rules that are appropriate for these diverse fisheries. This research employs a simulation approach with a novel reef fishery model to evaluate the expected performance of a range of management approaches, each employing length-based assessment and minimum size limits. First, three survey types to collect length data are compared, revealing that even low-cost surveys can provide the information for management to dramatically improve the population health and catch of a common target species. Next, the model is expanded to include over 100 species of varying life history. Management still performs well at the fishery level, but species-level recovery depends on data availability and permanent closures are required to sustain rare species. Finally, temporary species closures are evaluated as a simpler control rule that is well-received by fishers. These closures perform only marginally worse at the fishery level than size limits, providing a compelling option for most species. Taken together, these investigations identify promising management approaches for reef fisheries. Real-world applications should focus on efficient methods to collect large quantities of length data, and partner directly with communities to integrate multiple control rules to effectively manage the large number of reef species with a minimum of complex restrictions.
Reproductive Ecology of Hawaiian Intertidal Invertebrates, Hāʻukeʻuke and ʻOpihi: Drivers, Seasonal Patterns, and the Impacts of Temperature, Wave Energy, Limu, and Habitat Structure
(University of Hawai'i at Manoa, 2014) Morishige, Kanoeʻulalani; Moran, Amy; Marine Biology
This dissertation examines the reproductive ecology of Hawaiian intertidal invertebrates, focusing on hāʻukeʻuke (Colobocentrotus atratus) and three endemic ʻopihi (Cellana spp.) species—makaiauli, ʻālinalina, and kōʻele. Using field surveys, laboratory analyses, and statistical modeling, the study investigates how biophysical factors such as sea surface temperature (SST), wave energy flux, chlorophyll-a biomass, habitat zonation, and algal diversity shape reproductive traits and strategies across spatial and temporal scales. Reproductive metrics—including gonad-somatic index (GSI), gonad maturity, egg size, and fecundity—were analyzed alongside environmental variables and habitat features such as crustose coralline algae (CCA) and limu diversity. Generalized additive models (GAMs) revealed nonlinear relationships between reproductive output and environmental drivers, highlighting site-specific and seasonal patterns. Chapter 1 serves as a foundational biocultural framework and positionality statement weaving community engagement, Kānaka ʻŌiwi knowledge systems, and intertidal monitoring to support thriving communities. Chapter 2 identified distinct reproductive seasonality among three endemic Hawaiian limpets, with makaiauli and ʻālinalina exhibiting seasonal reproductive peaks influenced by temperature and wave energy, while kōʻele displayed more stable patterns, highlighting the role of habitat-specific environmental drivers in shaping reproductive strategies along an intertidal-to-subtidal gradient. Chapter 3 found that hāʻukeʻuke exhibit a seasonal reproductive cycle with gametogenesis beginning in the fall, a major spawning peak in winter, and quiescence in summer, driven by nonlinear relationships with temperature, wave energy, and chlorophyll-a, emphasizing the need for ecosystem-based management strategies. Chapter 4 revealed significant site-specific variation in hāʻukeʻuke reproductive traits, highlighting trade-offs between egg size and fecundity, larger individuals’ disproportionate contributions to reproductive output, and strong correlations between these traits and environmental factors such as SST and wave energy, emphasizing the need for adaptive, site-specific management to sustain population resilience and ecosystem health. This research emphasizes the need for adaptive, habitat-specific management strategies, such as size limits, rotational closures, and the integration of Kānaka ʻŌiwi knowledge systems. By addressing climate-driven variability and habitat-specific challenges, it provides critical insights to support the resilience and sustainability of Hawaiʻi’s intertidal ecosystems.
WINTER PICOPLANKTON DISTRIBUTIONS AND DIVERSITY OVER A THREE-YEAR STUDY OFF THE NORTHWESTERN ANTARCTIC PENINSULA
(University of Hawai'i at Manoa, 2024) Gimpel, Carla; DeLong, Edward F.; Marine Biology
High latitude-driven seasonal shifts govern the northwestern Antarctic Peninsula (NAP), which is experiencing some of the most rapid climatic warming trends on Earth. The ecological seascape faced by picoplankton has transitioned to a shorter and milder sea ice season. Among the microbiological consequences reported in the NAP is the shift in dominant phytoplankton populations, benefiting smaller sized species during the spring. Scarce Antarctic winter studies have suggested that low chlorophyll a levels correlate with pico and nanoplankton but these observations have been restricted to surface waters and have been limited in geographical scope. A picoplankton-focused survey was conducted off the NAP during three consecutive winters (2012 − 2014). The water column (15 − 750 m) featured Winter Water, Transitional Weddell Water and Upper Circumpolar Deep Water. Interannual variability in sea ice conditions influenced shallowing of the mixed layer over the period studied (104 ± 28 to 79 ± 49 m). Flow cytometry was used to quantify phototrophic picoeukaryotes (PPE) and bacterioplankton abundances and distribution from 300 hydrographic samples. A metabarcoding analysis accompanied 230 samples, to investigate the taxonomic composition of picoeukaryotes, including heterotrophic picoeukaryote taxa (HPE). The low chlorophyll a levels observed each winter correlated with persistent populations of pelagic PPE (R20122 = 0.86, R20132 = 0.63, R20142 = 0.62), regardless of sea ice cover (ROW2 = 0.48, RSI2 = 0.65). PPE abundances were in the 0.5 − 3.9 x 103 cell·mL-1 range, while observed bacterioplankton estimates were two orders of magnitude higher (0.8 − 3.5 x 105 cell·mL-1), both consistent with previous polar reports. PPE concentrations decreased with depth − nevertheless they were regularly detected beyond the mixed layer, in the upper 100 m and rarely even at 200 m. Bacterioplankton abundances were more stable in the upper 100 m in years with higher sea ice while a decreasing depth gradient was more abrupt in 2014 (i.e., in 2012 the bacterioplankton levels only decreased 4% from surface to 100 m, compared to 14% in 2013). This last year of the winter study (2014) showed a subsurface (50 m) maximum in mean prokaryoplankton abundance with a decrease of 25% at 100 m. Total picoplankton abundance increased each winter, coincident with diminished sea ice cover during the same time period. The co-occurrence of PPE and bacterioplankton varied and was positively influenced by sea ice. The taxonomic identities of the picoeuaryote populations focused on the 0.22 - 3.0 μm seawater fraction. The 18S rRNA amplicon metabarcoding results revealed the winter picoeukaryote community to be more diverse under conditions of lower sea ice. Obligate phototrophic taxa included Mamiellophyceae and Pelagophyceae. Among mixotrophic taxa, Dinoflagellata and Ciliophora were observed regardless of sea ice cover/open water conditions, while heterotrophic taxa were heavily biased towards parasitic picoeukaryotes, previously reported to be abundant in the Gerlache Strait in the west Antarctic Peninsula mesopelagic during winter and present at surface and in summer. Across the three winters surveyed, a single Bathycoccus-affiliated operational taxonomic unit (OTU) was observed to be the most abundant PPE in the upper mixed layer, even in sea ice-covered waters. The dominance of this prasinophyte coincided with seasonal patterns reported for Mamiellales in Arctic waters. Micromonas spp. have been regularly detected in spring and summer Antarctic Peninsula molecular and pigment-based surveys, nevertheless, Micromonas spp. appear to be outcompeted by Bathycoccus sp. in Southern Ocean winter waters, suggesting the prasinophyte seasonal pattern could occur in both polar ocean systems. Syndiniales-affiliated OTUs dominated the HPE community throughout the water column and the surveyed area. From the 3043 OTUs of the amplicon library, 37% were affiliated to parasitic groups. The prevalence of the parasitic Syndiniales spp. was evident throughout the water column and across the regional survey. All together, these findings substantiate the importance of picoeukaryotes to the late winter ecology of the NAP, and open questions regarding the role of phototrophic picoeukaryotes and parasitic Syndiniales in the nutrient and energy transfer of a rapidly changing winter environment.
Asymmetrical trophic release: Moray eels inconspicuously predominate heavily fished reefs
(University of Hawai'i at Manoa, 2024) Zill, Julie; Donahue, Megan J.; Marine Biology
Populations of marine apex predators have declined globally due to human activities. Without sufficient top-down control, mid-trophic level predator abundance can increase, termed ‘mesopredator release’. In the Hawaiian Archipelago, moray eels are consumed by large, transient predators that are scarce on densely populated coastlines of the Main Hawaiian Islands, indicating the potential for mesopredator release of moray eels. Additionally, human fishers have functionally replaced apex piscivores in heavily fished systems, but human prey selectivity differs from that of the natural predator assemblage, resulting in strong top-down control on targeted fishes of all trophic levels and, I hypothesize, the asymmetrical trophic release of non-targeted moray eels. Morays are generally excluded from fish biomass analyses because standard visual survey methods are unreliable for cryptic predators. Therefore, we conducted a novel, eel-specific baited camera survey on shallow reef habitats in the near-pristine Northwestern Hawaiian Islands (NWHI), where large carangids and reef-associated sharks are abundant, and in the populated Main Hawaiian Islands (MHI) where they are relatively rare. In the MHI, morays constituted the majority of piscivore biomass and, unlike most fish families, had a higher average biomass density in the fished MHI compared to the unfished NWHI, a result of both greater eel abundance and body size. Analysis of eel behavior in survey footage revealed that eels spent more time in risk-prone activities and degree of body exposure when large, transient predators were not present in video surveys. Due to their cryptic nature, changes in eel behavioral patterns and size frequency distribution may result in unique non-consumptive effects on the reef fish community. Morays specialize in hunting in the physical reef structures that would otherwise provide a size-dependent refuge to many benthic fishes. In a mesocosm experiment, eel presence decreased the shelter usage time and feeding patterns of a prey surgeonfish, and disrupted its refuge-seeking response during a simulated threat of a transient predator; these responses depended on both the relative size of predator and prey as well as shelter availability. Abundant, many-sized morays may reduce the ability of prey fish to achieve a spatial or body size refuge, and may shift community structure if they unevenly impact shelter-dependent fishes. The underdetection or exclusion of moray eels in spatial analyses of reef fish biomass patterns has led to the paradigm that native piscivorous fish are nearly absent from fished MHI reefs. Rather than a near extirpation of predatory fishes in areas of high human pressures, my data suggest a relative shift in biomass predominance from large roving predators to untargeted, cryptic mesopredators, which are emboldened in the absence of their natural predators—a phenomenon that may also occur outside of Hawaiʻi.
IMPLEMENTING A NOVEL APPROACH TO QUANTIFY THE AGE-STRUCTURE OF FREE-RANGING DELPHINID POPULATIONS USING UNOCCUPIED AERIAL SYSTEM PHOTOGRAMMETRY
(University of Hawai'i at Manoa, 2024) Vivier, Fabien Jeremy; Bejder, Lars PhD; Marine Biology
Evaluating the status of free-ranging wildlife populations is crucial for developing effective conservation and management strategies. Traditional monitoring approaches for cetaceans, are often costly, time-consuming, and lack the statistical power to detect changes in population trajectory. Therefore, alternative monitoring approaches are necessary to evaluate population stability and future trends. Stable populations typically maintain a consistent proportion of calves, juveniles, and adults, whereas deviations from this structure may indicate population growth or decline. Changes in age-structure can influence vital rates, offering insights into future population trends. In this thesis, I used Unoccupied Aerial System (UAS) photogrammetry to develop and implement a novel approach for quantifying the age-structure of free-ranging delphinid populations. I applied this method to two case studies representing extreme scenarios of group living in delphinids: one with average group sizes of <10 individuals and another with groups often reaching hundreds. In Chapter 2, I evaluated the accuracy of UAS-photogrammetry for estimating total body length (TL) of trained dolphins (Tursiops truncatus) using the blowhole-to-dorsal fin distance (BHDF) during surfacing events. I assessed its performance for age classification by simulating UAS-derived BHDF estimates using a 35-year age-length dataset from a free-ranging bottlenose dolphin community in Sarasota Bay, USA. The results showed that the TL of surfacing dolphins was overestimated by 3.3% (±3.1 SE), with 72% accuracy in age-class assignment. In Chapter 3, I combined UAS-photogrammetry data with long-term (>20 years) photo-identification data to assess the age-structure of the critically endangered sub-population of common bottlenose dolphins in the Gulf of Ambracia, Greece. I obtained a representative population age-structure estimate in five days of annual UAS-sampling. Subsequently, I compared the age-structure of the Greek population with two extensively studied non-endangered bottlenose dolphin populations: Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Australia, and common bottlenose dolphins in Sarasota Bay, USA. The results suggest careful consideration is needed when interpreting age-structure estimates across populations. In Chapter 4, I quantified the age-structure of a spinner dolphin (Stenella longirostris) stock in Hawaiʻi, the world’s most exposed dolphin population to human disturbances. This stock faces long-term viability concerns amid rising human activities and has been a NOAA management priority since 2005. My findings highlight concerns about a low calf proportion, indicating the need for ongoing monitoring and management by NOAA. In conclusion, this thesis demonstrates the use of UAS-photogrammetry as a promising and reliable tool for monitoring the age-structure of free-ranging delphinid species. UAS-photogrammetry has the potential to inform management more rapidly than traditional survey methods, particularly for large pelagic stocks.
Corallivory on Hawaiian Reefs
(University of Hawai'i at Manoa, 2024) Escontrela Dieguez, Daniela; Hixon, Mark A.; Marine Biology
Corallivores, predators of coral, span a wide range of taxa on tropical reefs. Corallivores can affect coral fitness, leading to reduced growth and reproduction, and at high densities, can cause mass coral mortality. As human-made threats to corals escalate and compound the effects of corallivory, coral reef managers increasingly need monitoring tools to track changes in corallivory. Historically, corallivory has been monitored with in situ visual surveys or post-hoc estimates derived from photoquadrats, both methods of which have limitations. Structure from Motion (SfM) photogrammetry, an imagery-based methodology, has emerged as a potential alternative. I counted bite marks by reef fishes on colonies of 16 coral species in paired in situ visual and SfM surveys at sites around Oʻahu to evaluate the accuracy of SfM as corallivory monitoring tool. I found significant differences in bite counts between methods, with SfM detecting higher counts. This disparity was more pronounced at deep sites and locations with high coral cover, reflecting the limitations of SCUBA diving inherent during in situ surveys. However, despite differences in absolute counts, both methods were consistent in qualitative patterns across sites, indicating that SfM is a viable tool to quantify corallivory, with potential for enhanced accuracy. Given the success of this tool, I leveraged the same data to investigate patterns and drivers of corallivory. My analysis revealed consistent consumption of only six coral species by reef fishes. There was also a positive relationship between species-specific coral cover and predation intensity for the preferred coral species of each corallivore, shedding light on common predator-prey interactions. Considering the heightened vulnerability of recently outplanted corals to predation, this information can inform coral restoration methodologies, ultimately yielding more favorable outcomes. Lastly, I studied the feeding ecology of a common corallivore around Oʻahu, the cushion sea star (Culcita novaeguineae), which may be increasing in abundance at some sites, representing a potential local stressor. I tested prey choice by running pairwise comparisons of corals of opportunity from different species and tracking the order of consumption. I used three methods to construct a feeding hierarchy, and across all methods, stars overwhelmingly preferred Pocillopora spp. and rarely consumed Porites spp. These findings indicate which coral species may face increased predation as seastar populations increase, which has implications for local coral restoration efforts and coral community trajectory under future conditions.
Microbial assemblage dynamics of disturbed, tropical, high-island estuarine systems
(University of Hawai'i at Manoa, 2024) Lensing, Becca Rae; Alegado, Rosanna; Marine Biology
Marine microbes exhibit characteristic distributions both temporally and across physiochemical gradients that drive biogeochemical cycling. Understanding how the taxonomic and functional diversity of microbial assemblages change in response to disturbances is critical for identifying vulnerabilities or critical tipping points toward alternative stable states to an ecosystem’s microbe-dependent biogeochemical cycling. Environmental conditions, trophic interactions, immigration from adjacent ecosystems, and the history and evolution of community members underlie microbial assemblage shifts, and the relative contribution of these factors varies across ecosystems. Better characterization of how these factors drive microbial assemblage dynamics is necessary to build robust assemblage models, improve our understanding of microbial function and resilience in ecosystems, and can provide insight into the functions of individual clades within distinct ecological niches. While several temperate estuaries serve as systems for studying the effects of anthropogenic and climatic impacts on the coastal environment, few cognate systems have been thoroughly examined in the tropics. We set out to provide a baseline understanding of microbial responses to a variety of disturbances faced by Pacific, high-island communities. We took a genomic approach to characterize planktonic microbial assemblages from Hawaiʻi [RA1] and American Samoa estuaries and embayments. At Heʻeia Fishpond (HFP) on the island of Oʻahu, we used 16S V4 and 18S V9 amplicon sequencing to characterize microbial resistance, resilience, and recovery in response to diverse external disturbances during a year-long sampling campaign (Chapters 2 and 4). In HFP, we found that prokaryotic diversity recovered following a tropical storm to pre-storm levels within two weeks and were lowly resistant but highly resilient to multiple tropical storms and a SSTA. A marked shift in the dominant primary producers from cyanobacteria-dominated assemblages to diatom-dominated assemblages occurred immediately following and up to at least one week following the largest tropical storm. Eukaryotic assemblages did not immediately recover within two weeks of a tropical storm. However, we observed strong successional shifts in these groups, possibly driven by seasonal changes, that contributed to microbial recovery on longer time scales. In this manner, seasonal forcing may serve as a stabilizing mechanism for disturbed microbial assemblages. Notably, we characterized a marked shift in the most dominant microeukaryote group from Cyclotella to Chaetoceros in the last quarter of our rigorous sampling campaign. We hypothesize that this shift is the result of increased freshwater input and mixing achieved through intensive biocultural restoration efforts, with potentially profound implications to fishpond food-web dynamics. We also investigated disturbed plankton and biofilm microbial assemblages using 16S V4 amplicon sequencing and quantitative polymerase chain reaction (qPCR) across four watersheds on the island of Tutuila, American Samoa[RA2] . How does nitrogen loading, at different scales, alter reef microbial assemblages? And how does the capacity of reef microbial assemblages to cycle nitrogen respond to altered nitrogen input (Chapter 3)? [RA3] In Tutuila watersheds, we found that both plankton and biofilm assemblages were differentiated between nitrogen concentrations but with distinct patterns. We detected areas of higher-than-expected nitrogen contamination and microbial metabolisms supporting nitrogen loss at two of the more impacted sites, one of which was also identified as a potential hotspot for algal blooms. We identified novel microbial indicators with metabolisms directly linked to the consumption and cycling of NH3, the concentration and cycling ability of which was found to be critically elevated in Tutuila’s more urbanized watersheds. These analyses support the findings of mesocosm experiments approximating biofilm development of coastal reefs experiencing nutrient enrichment and provide in-situ evidence that biofilms are strongly influenced by nutrient pollution and the composition of DOM altered by anthropogenic activities in coral reef ecosystems. Taken together, my work provides a foundational understanding of important food-web and nutrient cycling contributors in tropical estuarine environments undergoing different types of disturbances. This research establishes HFP as an ecosystem model for tropical, high-island estuaries. Finally, my work was co-produced and co-published with the local community stakeholders and stewards that care for these remarkable places and demonstrates how ʻōiwi methodologies support and empower communities to protect their natural and cultural resources.
POPULATION GENOMIC TOOLS AND APPLICATIONS OF POOLED SEQUENCING DATA
(University of Hawai'i at Manoa, 2024) Freel, Evan Barba; Toonen, Robert J.; Marine Biology
Population genetic studies use a diverse toolkit to better understand the mechanisms affecting the exchange of genetic information between populations. A frequently used metric of genetic variation used to characterize populations is allele frequency, or the relative frequency of a genetic variant at a particular locus in a population. High throughput sequencing has vastly increased the capacity to generate sequence data at the genomic scale, resulting in the ability to obtain allele frequency data at many loci across the genome. However, when dozens of individuals are needed per population in order to differentiate populations, sequencing costs can be cost-prohibitive when many populations are in the study system. Thankfully, allele frequency can still be reliably estimated at the population level when individuals from the same population are pooled prior to sequencing (pool-seq), making cost relative to the total number of pools instead of the total number of individuals sequenced. However, the data analysis of pool-seq data has not caught up in terms of accessibility and pipelines are needed to alleviate the burden of bioinformatic expertise. In this dissertation, a novel bioinformatic pipeline, asessPool, is presented as a tool to analyze pool-seq data. asessPool is entirely contained in the free and widely used R language, with ease of operation in an RStudio environment. The tool’s utility is then demonstrated in a multispecies population genetic analysis of seven species, across the Hawaiian Archipelago. Using pool-seq data from 625,215 SNP loci differentiation was observed at a finer scale than previously detected, with nearly 70 percent of island pairs having significant differentiation, exchanging the equivalent of less than 100 migrant per generation. assessPool was then also used to identify regions of the genome with high degrees of differentiation, outlier loci, in tilapia which had undergone acclimation to freshwater or seawater treatments in an evolve-and-resequence approach. In this application of assessPool, we are able to extract information about observed allele frequency differences that occur in just a few generations, with the potential to be related to salinity tolerance or adaptive processes related to salinity. The approach taken highlights a cost-effective method to scan the genome for candidate loci that may be further confirmed or denied using targeted approaches. 86 outlier loci were identified, with 26 of them receiving gene ontology assignments. Overall, the work presented in this dissertation provides a new tool which increases the accessibility of cost-effective population genetic approaches and demonstrates two distinct applications of assessPool, highlighting the broad diversity of its use.
SELECTING HEAT TOLERANT CORALS FOR RESILIENT REEF RESTORATION
(University of Hawai'i at Manoa, 2023) Caruso, Carlo; Madin, Joshua; Marine Biology
As coral reefs face increasing threats from warming oceans, there is burgeoning interest in reef restoration as an intervention to retain living coral cover. Given that thermal stress is inevitable in the near term, selecting putatively resilient coral stocks for restoration projects may improve efficiency and success. Understanding the level and range of heat tolerance available in coral populations is critical to determining their viability and for choosing corals for outplanting. Whether breeding to produce novel genotypes or asexually propagating fragments, determining if selection criteria translate into long-term success is critical. In this study, we sampled a model population of a dominant reef-building coral (Montipora capitata), subjected fragments to an artificial heat-stress, and subsequently revisited and assessed source colonies at the height of a moderate natural bleaching event. We also exposed asexually propagated fragments of known bleaching phenotypes and sexually derived juvenile samples selected via acute heat exposure to realistic long-term temperature profiles simulating past, contemporary, and future climate conditions. We measured a range of performance outcomes including survival, growth, and bleaching performance. Selection criteria broadly translated to improved subsequent performance across experiments. There was substantial response variation in the population during exposure to increasingly detrimental future temperature conditions suggesting extant adaptive potential. These results align with the view of heat tolerance as a complex, heritable trait. While the only tenable solution to the cascading problems of warming oceans is drastic reduction in fossil fuel emissions, utilizing corals picked for thermal resilience might help reef restoration projects buy time for climate change mitigation to occur.
Prokaryotes and Partners: Exploring How Microbe – Organic Matter Interactions Inform Carbon Cycling in Healthy and Degraded Coral Reefs
(University of Hawaii at Manoa, 2023) Sparagon, Wesley James; Nelson, Craig E.; Marine Biology
Coral reefs are a paradox: these vibrant ecosystems maintain high levels of gross primary production and biomass, all while bathed in resource-poor waters. A longstanding hypothesis is that these properties are the result of efficient recycling of organic carbon and nutrients, partially underpinned by the interaction between microbes and organic matter (OM). Microbe-OM interactions occur in both organism-associated and free-living compartments on coral reefs, and the outcome of these interactions dictates the flow of carbon and nutrients through the food web. In this dissertation, I explore how microbe-OM interactions support the tight recycling of carbon on coral reefs in both organism-associated and free-living forms, and how these interactions may shift as coral reefs change. Specifically, I examined 1) the succession of microbes and metabolites as algal biomass is digested in the gut of nenue (Kyphosus spp.), an herbivorous Hawaiʻian reef fish, 2) the impacts of changing benthic primary producers on the carbon cycling capabilities of reef bacterioplankton and 3) how thermal stress induced bleaching alters coral OM release into the water column and the subsequent bacterioplankton response. In nenue, associations between microbes and metabolites continuously shifted through the gut as macroalgal biomass was digested: bile acid deconjugation associated with early gut microbiota, small peptide production associated with midgut microbiota, and phospholipid production associated with hindgut microbiota. In the coral reef water column, shifts in abundance of benthic primary producers from corals to algae had a dramatic effect on microbe-DOM (dissolved organic matter) interactions and carbon cycling. Coral-associated bacterioplankton grew significantly more efficiently and to significantly lower abundances than algal-associated bacterioplankton, with growth efficiencies ranging from 3% in algal-associated bacterioplankton to 50% in coral-associated bacterioplankton. This suggests that bacterioplankton switch from acting as trophic links for carbon transfer to trophic sinks as reefs undergo coral-algal phase shifts. Change in sea surface temperatures can also have dramatic impacts on the water column via altered DOM exudation from thermally stressed and bleaching corals. Controlled aquaria and bottle incubations revealed that thermal stress and bleaching altered coral DOM exudate quantity and composition, yielding upwards of 3x DOC release from corals and DOM with distinct metabolomic compositions. These DOM exudates in turn yielded a 2-fold increase in microbial loads and altered microbial community structure, driven by a significant enrichment of copiotrophic and putatively pathogenic bacterial taxa. Together the work comprising this dissertation collectively points to the critical role microbe-OM interactions have in mediating carbon flow in coral reefs, and how environmental changes may fundamentally shift these interactions and alter coral reef ecosystem function.
Following bonefishes in Hawai‘i: Connecting the dots from ocean to table
(University of Hawaii at Manoa, 2023) Kamikawa, Keith; Bowen, Brian R.; Marine Biology
Hawai‘i is home to the Indo-Pacific round jaw (Albula glossodonta) and the endemic sharp jaw (A. virgata). These species’ hold cultural, recreational, and commercial value in Hawai‘i and it is important to fill various data gaps in their life history. Our understanding of bonefish site fidelity, habitat use, population structure and effective conservation measures is based on limited information in Hawai‘i. First, leptocephalus larvae were captured by light trap in Kāne‘ohe and Maunalua Bays and aged through otolith analyses. Leptocephali ranged from 28-72 days old and 54-66 mm. The mean age of the larvae was 48.8 days, indicating high dispersal ability. Tissue samples from larvae and over 300 fin clips, collected by volunteer anglers from O‘ahu, Maui, Kiritimati and Anaa Atoll, were used to determine population structure within the Pacific Ocean. Results showed Anaa and Hawai‘i exhibiting distinct genetic stocks and Kiritimati with admixed individuals. Lastly, a survey was conducted of bonefish anglers to understand their motivations and preferences. Of the anglers that keep bonefish for food, they prefer fish over a four-pound threshold. Comments also revealed anglers’ attitudes towards current management and competing demands. Aligning biological and social information regarding bonefish life history is critical to update fisheries management tools and promote responsible fishing practices.
Dimensions in marine biodiversity: Traditional and molecular approaches to unraveling the mysteries of the deep
(University of Hawaii at Manoa, 2022) Hoban, Mykle L.; Bowen, Brian R.; Marine Biology
Biodiversity research is a critical field for addressing global change and species loss. Understanding patterns of species distribution and community composition is fundamental to many other aspects of biology and conservation, and molecular approaches are increasingly central to such work. Here I explored three separate but related dimensions in biodiversity research: infrastructure, taxonomy, and exploration. DNA barcoding is a critical component of the infrastructure underlying conservation and biodiversity research, yet public reference databases are incomplete. I used genome skimming to sequence complete mitogenomes and nuclear ribosomal repeats to build comprehensive barcode reference databases for marine fishes, with all sequences matched to voucher specimens housed in natural history collections. Results affirm that genome skimming is an efficient and cost-effective method to generate multiple commonly used barcoding loci simultaneously. This approach has great potential for future projects and to facilitate completing barcode reference databases for marine fishes. Robust molecular resources can also illuminate previously unknown biodiversity and its origins. I used DNA barcoding combined with integrated molecular-phylogeographic-taxonomic methods to reveal and describe a new species of combtooth blenny, named Cirripectes matatakaro. The distribution and phylogenetic position of the new species helped uncover the evolutionary origins of a closely related Hawaiian endemic, showing that it most likely arose via colonization from the Central/Southern Pacific through the Line Islands and possibly Johnston Atoll. In addition to revealing previously undescribed species, molecular biodiversity approaches can be used to explore new habitats. Mesophotic coral ecosystems (MCEs) are coral reef communities found from 30–150 m depth. I used environmental DNA (eDNA) metabarcoding to investigate patterns of community composition across the tree of life from the surface to ~100 m on Hawaiʻi Island. I found a transition zone at 45–60 m, where shallow reef communities give way to distinctly mesophotic assemblages, for a broad range of invertebrates and eukaryotes but not for fishes. I attribute this finding to the higher mobility of fishes, although methodological limitations may contribute as well. Since the invertebrate communities below 45 m are taxonomically distinct, they are seemingly unlikely to act as refugia to reseed depleted shallow reefs over ecological timescales. Together, this work examines three avenues in biodiversity research and provides insight into genetic infrastructure, the importance and relevance of traditional taxonomy, and the application of new technologies to marine exploration.
Visual pigment diversity and function in larval stomatopods and other malacostracan pancrustaceans
(University of Hawaii at Manoa, 2022) Palecanda, Sitara; Porter, Megan L.; Marine Biology
Stomatopods have among the most complex eyes of any pancrustacean, with up to 33 opsin proteins, the basis of visual pigments, found in a single retina. While the adult visual system has been the subject of many studies, visual capabilities of stomatopod larvae are comparatively less well understood. Learning how larval stomatopods perceive the world can help us further understand the signals that drive their behavior. Adult stomatopods generally live in shallow waters containing a wide range of wavelengths in the visible spectrum, while larvae are pelagic and live in environments dominated by blue and green light. Previous work has thus suggested that larval stomatopod visual systems contain a single photoreceptor type and correspondingly a single visual pigment that absorbs maximally in the blue/green portion of the spectrum. However, more recent studies have found anatomical and physiological complexity in larval stomatopod eyes which exceeded expectations. In this dissertation I have further investigated the visual ecology of larval stomatopods, focusing on the thus far uncharacterized visual pigments which form the basis of light perception. I first looked at the extent of larval diversity at one of my study locations, to understand how larval versus adult stomatopod sampling efficiency differ and affect estimates of species richness. I then investigated the expression of opsin proteins in different developmental stages of stomatopods, testing the hypothesis that larval stomatopods have only one unique visual pigment. The unexpected expression of multiple ultraviolet sensitive opsins in all stomatopod developmental stages prompted a detailed study of these proteins and the molecular mechanisms that affect their specific ultraviolet absorbance in malacostracans. Finally, I investigated the significance of ultraviolet light perception in larval stomatopods by quantifying the effect of different light spectra on behavior period and opsin expression. Taken together this work offers evidence that larval stomatopod visual systems are surprisingly complex at the molecular level and gives insight into the ecology of these early life stages.
Studying the Ecophysiological Responses of Native Hawaiian Macroalgae in a Changing World
(University of Hawaii at Manoa, 2022) Yamase, Nicole Hokulani; Smith, Celia; Marine Biology
In the Hawaiian flora, approximately 550 species of algae or limu are identified, yet little is known about their physiological ecology: growth rates, photosynthetic capacities, or other features of biology, even for common native species. Culturally, Native Hawaiians as with many Pacific Islanders gather marine plants for nourishment, use in medicine, hula, and other traditional ceremonies. Ecologically, the limu are the primary producers of coastal reefs, provide refuge, and food for a wide range of herbivores and omnivores, and thus are of critical importance to nearshore marine food web. In this study, I 1) analyzed the biodiversity, species composition, and photosynthetic rates of a 2-year-old benthic plant community under future climate change conditions, 2) explored how irradiance and temperature affect the growth and photosynthesis of the native macroalga Microdictyon setchellianum, and 3) cultivated Sargassum aquifolium germlings on limestone tiles to characterize their early life stages and explored the effects of shading. Results reveal that 1) the biodiversity, species composition, and total photosynthetic rates did not dramatically change under predicted climate change conditions suggesting that our limu community may be resilient to changes in coastal acidification and increasing temperatures of coastal waters, 2) M. setchellianum fulfilled expectations for a broadly distributed alga in terms of depth as well as biogeography, had lower growth rate under shaded conditions, but still photoacclimated under both low and high irradiance levels in a short period of time which is consistent with the physiological adjustments for an alga that can be found in the intertidal to deep water communities, 3) and young Sargassum germlings successfully grew on tiles, had high rates of photosynthesis, and an ability to recover after being shaded with physiological expectations for germlings that grow under deep shade of dense, moving canopies of adult Sargassum. This research provides valuable insight into the physiological capabilities of two abundant Native Hawaiian limu, as well as the community of 32 species that developed in experimental mesocosms. In sum, single species studies reveal remarkable abilities that sustain their abundance in current reefs and give insight into changes in our future reefs. Analysis of communities that develop under future scenarios reveals hope for the stability of primary producer communities, at least in the Hawaiian islands. Further research to provide other crucial data will help estimate the ecological success of our benthic community and build restoration tools to help rehabilitate native limu populations such as Sargassum, as interest is building to restore native species on our reefs. Overall, this dissertation fills in biological data gaps for important native Hawaiian algal species and describes a cultivation tool that serves as a step towards replenishing the population of Sargassum on the reefs.
Phylogenetic and functional characteristics that underlie the spatiotemporal distributions of marine bacteria and phytoplankton across a coastal to open-ocean model system
(University of Hawaii at Manoa, 2022) Tucker, Sarah J.; Rappe, Michael S.; Marine Biology
Understanding the roles that marine microbes play in ecosystem functioning has been historically difficult in large part because of the immense genetic and ecological diversity found within natural populations. This dissertation research characterized the steep physical and biogeochemical gradients found across Kāneʻohe Bay, Oʻahu, Hawaiʻi and surrounding offshore waters, and used this system as a model platform to examine the genetic diversity, population structure, and metabolism of marine microorganisms. Time-series analyses across this system revealed an increase of inorganic nutrient concentrations within the near-shore environment of coastal Kāneʻohe Bay co-varied with elevated phytoplankton biomass of up to ~1700% compared to open-ocean waters of the North Pacific Subtropical Gyre. Steep gradients in environmental parameters and phytoplankton biomass coincided with shifts in phytoplankton community composition and diversity, including the abundance and population structure of numerically dominant picocyanobacteria. The steep physical and biogeochemical gradient also impacted the distribution of subclades and genome clusters within the numerically abundant alphaproteobacterial lineage known as SAR11. Seven of eight SAR11 subclades detected in this system were distributed nonuniformly across the coastal to offshore environments within and adjacent to Kāneʻohe Bay. Pangenomic analyses with metagenomes and a collection of high-quality SAR11 Ia genomes from strains recently isolated from this system revealed the hallmarks of ecotypic differentiation: distinct distributions, the accumulation of differences in metabolic gene content, and the cohesion of both ecological and genetic diversity within SAR11 Ia genome clusters. The utilization of data collected through both the Kāneʻohe Bay Time-series (KByT) and the Hawaii Ocean Time-series (HOT) provided the unique opportunity to elucidate the genetic, genomic, and metabolic variability of surface ocean microbial populations across narrow (<6km) and broad (>100km) spatial scales in the tropical Pacific. In sum, this dissertation provides insight into the forces that contribute to the genetic and ecological diversity of dominant and biogeochemically relevant lineages of marine bacteria.
The effects of the pesticides atrazine and brodifacoum on two Hawaiian corals
(University of Hawaii at Manoa, 2022) Barkman, Alexandria Lynn; Richmond, Robert H.; Marine Biology
Coral reefs are threatened by the effects of multiple anthropogenic stressors, including land-based runoff of sediments and toxicants. My dissertation focuses on determining the sublethal effects of exposure to two pesticides on two common species of Hawaiian corals. Atrazine is a restricted use herbicide that is still frequently found in stream samples around the Hawaiian Islands. In Chapter 1, I present data demonstrating sublethal effects in the lobe coral Porites lobata after exposure to 1 ppb and 10 ppb atrazine, through increased expression of stress response proteins. In Chapter 2, I present results of a dose-response experiment confirming that exposure to increasing concentrations of atrazine depresses photosynthetic efficiency rapidly and reversibly in the algal symbionts of Porites lobata. Brodifacoum is commonly used to eradicate populations of invasive rodents. Data presented in the third chapter identifies decreased fertilization success and larval survival in Montipora capitata after exposure to high concentrations of cereal bait pellets, regardless of whether the pellets contained the active ingredient brodifacoum. In Chapter 4, I describe decreases in dissolved oxygen and pH in cereal bait pellet solutions. Upregulation of citrate metabolism was observed in Porites lobata corals exposed to the brodifacoum treated pellets. Increased expression of glutathione S-transferase, an enzyme associated with detoxification, was observed in coral exposed to both brodifacoum treated and inert pellet solutions. The herbicide atrazine and rodenticide brodifacoum had sublethal impacts on corals at multiple life stages. Efforts to prevent pesticide contamination of nearshore waters can reduce threats to coral health. Managers should increase the use of tools such as proteomics that assess sublethal indicators of stress in corals to inform management decisions and monitor the effectiveness of interventions while moving away from death as an indicator of stress on a reef.

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