Time and energy are finite resources in any environment, and how and when organisms use their available resources to survive and reproduce is the crux of life history theory (Gadgil and Bossert 1970; Balon 1975; Stearns 1976). The different survival strategies used by animals are often shaped by their environment in addition to their biology (Winemiller and Rose 1992), which allows for exploration into biological variability when environmental factors are known. For this reason, the Line Islands in the Central Pacific provide an ideal location to perform observational studies due to their unique productivity gradient and fish assemblage structures across the island chain (Sandin et al. 2008; DeMartini et al. 2008; Fox et al. 2018; Zgliczynski et al. 2019). Many of the world’s coral reefs are in remote regions that lack monitoring programs or even local populations, so conducting ecological surveys on fish communities in these regions can require extensive amounts of time, energy, resources and people. The inherent variability an environment exerts on the many factors that contribute to growth over a lifetime make it difficult to generate a directly proportional formula that calculates age. A novel age estimation method was developed that utilizes in-situ visual census data to estimate the age of fishes, and as a case study, several fish were chosen as representative species to explore its capabilities. Through this process, new ecological information and insight can be gained about the age structures of fish populations both between and throughout the Line Islands.
Understanding fish diversity patterns is critical for fisheries management amidst overfishing and climate change. Fish egg surveys have been used to characterize pelagic spawning fish communities, estimate biomass, and track population trends in response to perturbations. Environmental DNA (eDNA) metabarcoding has been implemented to rapidly and non-invasively survey marine ecosystems. To understand the efficacy of eDNA metabarcoding for assessing pelagic spawning fish community composition, concurrent eDNA metabarcoding and fish egg DNA barcoding off Scripps Institution of Oceanography’s Pier (La Jolla, CA) were conducted. Both methods revealed seasonal patterns in agreement with previous fish and fish egg surveys. Species richness was highest in late spring and summer. The presence and spawning of commercially important species and species of conservation concern were detected. Both methods showed overlap for pelagic spawning fishes for broadcast spawners, schooling fish, and locally abundant species. Some actively spawning species were not co-detected with eDNA, likely due to different sampling strategies, taxonomic biases, and abiotic/biotic factors influencing eDNA transport, shedding, and degradation. We identified key advantages and disadvantages of each method. Fish egg barcoding provided information on spawning trends but did not detect taxa with alternate reproduction strategies. Metabarcoding eDNA detected species not found in fish egg sampling, including demersal and viviparous bony fishes, non-spawning adults, Chondrichthyan, and Mammalian species, but missed abundant pelagic fish eggs. This study demonstrates that DNA barcoding of fish eggs and eDNA metabarcoding work best in tandem as each method identified unique fish taxa and provided complementary ecological and biological insight.
The western North Atlantic is a dynamic region characterized by the Gulf Stream western boundary current and inhabited by a diverse host of odontocete, or toothed whale, top predators. Their habitats are highly exploited by commercial fisheries, shipping, marine energy extraction, and naval exercises, subjecting them to a variety of potentially harmful interactions. Many of these species remain poorly understood due to the difficulties of observing them in the pelagic environment. Their habitat utilization and the impacts of anthropogenic activities are not well known. Over the past decade, passive acoustic data has become increasingly utilized for the study of a wide variety of marine animals, and offers several advantages over traditional line-transect visual survey methods. Passive acoustic devices can be deployed at offshore monitoring sites for long periods of time, enabling detection of even rare and cryptic species across seasons and sea states, and without altering animal behaviors. Here we utilized a large passive acoustic data set collected across a latitudinal habitat gradient in the western North Atlantic to address fundamental knowledge gaps in odontocete ecology. I approached the problem of discriminating between species based on spectral and temporal features of echolocation clicks by using machine learning to identify novel click types, and then matching these click types to species using spatiotemporal correlates. I was able to identify novel click types associated with short-beaked common dolphins, Risso’s dolphins, and short-finned pilot whales in this way. Next I characterized temporal patterns in presence and activity for ten different species across our monitoring sites at three different temporal scales: seasonal, lunar, and diel. I observed spatiotemporal separation of apparent competitors, and complex behavioral patterns modulated by interactions between the seasonal, lunar, and diel cycles. Finally I investigated the relationships between species presence and oceanographic covariates to predict habitat suitability across the region, and explored niche partitioning between potentially competitive species. The insights gained here significantly advance our understanding of toothed whale ecology in this region, and can be used for more effective population assessments and management in the face of anthropogenic threats and climate change.
Parasites and pathogens exert strong selection on their hosts and alter the structure, diversity, and productivity of communities of ecosystems. This paper presents results of a survey of parasite composition and prevalence observed on and within the freshwater hybrids Owens (Siphateles bicolor snyderi) and Lahontan (Siphateles bicolor obesa) Tui Chubs, a native minnow species, in the Eastern Sierra Nevada mountains of California. The Owen and Lahontan Tui Chub is present in many lakes and rivers in Northern California and its parasite community has yet to be characterized. My thesis asks what kinds of parasites are found in the freshwater Tui Chub, which lakes or streams held the highest parasitic loads, and which features of individual fish and the habitat influence parasite density and/or types of parasites. Fish samples were collected in Summer 2019 by PhD student Henry Baker at 10 different sampling sites including freshwater lakes and streams that vary in size, temperature, water chemistry and species present across Owens Valley, California. I dissected 134 individual fish to characterize the ecto- and endo-parasite communities. My results show that two of the locations had significantly higher parasite infection rates than the others, where few macroscopic parasites were observed. These two locations were both geothermal with warmer waters and distinct water chemistry with high salinity and alkalinity. This pattern suggests that some aspects of geothermal habitat favor the parasite life cycle and makes fish in these sites more easily accessible as a host, though the mechanism behind the pattern is unknown. Four main types of visually distinct parasites were found: one adult life-stage tapeworm, one adult life- stage nematode and two metacercaria trematodes, though none were identified taxonomically. The greater parasite infection rates in geothermal habitats may be related to the greater abundance of snails in these sites, which may serve as intermediate hosts to fish parasites. No differences in parasite infection rates or composition were observed between lake and stream habitats. My thesis suggests that the atypical thermal and chemical environment of geothermal springs promotes parasitism in Tui Chub, but that lakes and streams are similar in containing low rates of infection by any parasites among fish.
Gut microbes provide vital functions for animal hosts. While it is known that host ecology and evolutionary history play a role in shaping gut microbiomes, a majority of studies have focused on mammal hosts. Other vertebrates, including fish, have received little attention. Coral reef fish, in particular, exhibit a wide range of distinct feeding behaviors, evolutionary histories, and geographic distributions that likely correlate with gut microbiome composition and diversity. They also inhabit a fragile ecosystem that is highly sensitive to anthropogenic disturbance—disturbances that are known to impact coral microbiomes but may or may not affect fish gut microbiomes. My thesis leverages a large unprecedented coral reef fish gut microbiome dataset (N=550), where I sampled the gut microbiomes of 20 host species of fish with robust replication spanning three islands across the South Pacific, to better understand how host phylogeny, host diet, and host environment shape vertebrate gut microbiomes. Comparing the gut microbiomes of distantly related hosts can reveal evolutionary and ecological dynamics that govern gut microbiomes across the animal kingdom. Chapter 1 investigates the possible similarities between coral reef fish and mammal gut microbiomes to elucidate any microbial features that may have converged between the two distantly related hosts. Through multivariate and Bayesian analyses, I show that fish and mammal gut microbiomes exhibit striking similarities in composition, particularly within carnivores and herbivores. Specifically, carnivores and herbivore gut microbiomes show more similarities within their diet groups than within their host phylogenies, and share a significant number of ASVs. Herbivore fish and mammal gut microbiomes, in particular, share a significant number of amplicon sequence variants (ASVs) associated with the functional requirements of herbivory, such as Ruminococcus and Treponema. My results indicate that despite 365 million years of evolution and two drastically distinct habitats (terrestrial vs. marine), fish and mammal gut microbiomes have converged on the basis of diet. Expanding on Chapter 1, Chapter 2 moves beyond host phylogeny and diet and aims to isolate and analyze the effects of host habitat on gut microbiome composition and diversity. Previous work on environmental effects acting on animal gut microbiomes largely focused on captive hosts or wild hosts of a single species, potentially ignoring any interactions between host environment and host phylogeny in the wild. Here, I leverage my dataset of coral reef fish gut microbiomes from a diverse range of hosts from three geographically distinct habitats to better understand how host habitat shapes vertebrate gut microbiomes. I find that host habitat significantly shapes fish gut microbiome composition and diversity and these effects are highly dependent on host phylogeny. For example, within the same analyses, a fish such as R. aculeatus, had significantly different gut microbiomes between the three islands, whereas E. merra gut microbiomes were largely unaffected by island location. For the fish gut microbiomes that were significantly impacted by host habitat, many of the associated ASVs were ASVs found in Chapter 1, suggesting that host habitat may also shape gut microbiome function. While comparative approaches on wild hosts are crucial in elucidating generalizable rules that govern animal gut microbiomes, experimental approaches are also imperative to unpack the finer-scale qualities and mechanisms of these rules. Chapter 3 builds on Chapter 2 by leveraging a simulated nutrient enrichment experimental design to further investigate the effects of host environment on gut microbiome composition and diversity. Nutrient enrichment is one of the most threatening consequences of anthropogenic stress on coral reef ecosystems, and the effects of nutrient enrichment on reef fauna gut microbiomes are largely unknown. Here, I artificially enrich the territories (N=40) of a highly abundant, territorial gardening fish, Stegastes nigricans, and use multivariate and differential abundance analyses to elucidate how nutrient enrichment impacts animal gut microbiome composition and diversity. I find that nutrient enrichment effectively “enriches” the gut microbiome, with S. nigricans gut microbiomes in enriched territories exhibiting significantly higher alpha diversities than those in control territories. I also find that these changes are specific to the hindgut and do not occur in the microbiomes of the food source that S. nigricans gardens.
In late 2019, at multiple hatcheries in California’s Central Valley (CCV), offspring of recently spawned fall-run Chinook salmon (Oncorhynchus tshawytscha) exhibited abnormalities in swimming, lethargy, and high early life-stage mortality; the combination of these symptoms is commonly referred to as thiamine deficiency complex (TDC). The cause of thiamine deficiency in Pacific salmonids is hypothesized to be due to a lack of diet heterogeneity and reliance on northern anchovies (Engraulis mordax), containing high levels of thiaminase, a thiamine-cleaving enzyme. Of CCV’s four runs, the endangered Sacramento River winter-run Chinook salmon (WRCS) is perhaps the most vulnerable to thiamine deficiency as any additional stressor will exacerbate current threats to survival. The goal of this study was to evaluate the effect of thiamine supplementation in pre-spawn WRCS females on their offspring egg thiamine concentrations, survival, prevalence of TDC-related symptoms, and physiological performance and behavioral traits. Sixty female WRCS at Livingston Stone National Fish Hatchery were randomly administered either a thiamine injection (n=33; 500 mg/ml thiamine hydrochloride) at a dose of 50 mg/kg body weight or a sham injection (n=27; sterile saline solution) at a volume of 0.127 ml/kg body weight. After spawn, a subset of fertilized eggs from each female were analyzed for thiamine concentration. Eyed embryos were transferred to the University of California, Davis and kept for observations of TDC, survival, and to assess the effects of maternal thiamine treatments on offspring physiology and behavior. Upper thermal tolerance, routine metabolic rate, spontaneous swimming activity, boldness, and anti-predator responses were evaluated in swim-up fry. On average, total egg thiamine concentrations were 5.02 and 34.91 nmol/g for untreated (n=27) and thiamine treated (n=33) females, respectively. Mortality rate of offspring from untreated females averaged 32.97 ± 0.33 %, with rates ranging from 0 to 100%, while offspring from thiamine treated females had a mean mortality rate of less than 1%. Using a binomial logistic regression model, we predicted that a mean total egg thiamine concentration of ~5 nmol/g supports 95% survival within a family (EC95). There were no statistically significant effects of maternal treatment on any of the physiological or behavioral metrics assessed in this study. Overall, we recommend the administration of supplemental thiamine to increase thiamine concentrations past the threshold at which TDC symptoms are commonly observed; however, additional research should be conducted to further examine potential latent effects of thiamine deficiency in Pacific salmonids.
Amines were measured by aerosol mass spectrometry (AMS) and Fourier Transform Infrared (FTIR) spectroscopy during the North Atlantic Aerosols and Marine Ecosystems Study (NAAMES) cruises. Both AMS non-refractory (NR) amine ion fragments comprising the AMS CxHyNz family and FTIR non-volatile (NV) amine measured as primary (C-NH2) amine groups typically had greater concentrations in continental air masses than marine air masses. Secondary continental sources of AMS NR amine fragments were identified by consistent correlations to AMS NR nitrate, AMS NR m/z 44, IC non-sea salt potassium, and radon for most air masses. FTIR NV amine group mass concentrations for particles with diameters <1 μm showed large contributions from a primary marine source that was identified by significant correlations with measurements of wind speed, chlorophyll a, seawater dimethylsulfide (DMS), AMS NR chloride, and ion chromatography (IC) sea salt as well as FTIR NV alcohol groups in both marine and continental air masses. FTIR NV amine group mass concentrations in <0.18 μm and <0.5 μm particle samples in marine air masses likely have a biogenic secondary source associated with strong correlations to FTIR NV acid groups, which are not present for <1 μm particle samples. The average seasonal contribution of AMS NR amine fragments and FTIR NV amine groups ranged from 27% primary marine amine and 73% secondary continental amine during Early Spring to 53% primary amine and 47% secondary continental amine during Winter. These results demonstrate that AMS NR and FTIR NV amine measurements are complementary and can be used together to investigate the variety and sources of amines in the marine environment.
This project is directed towards implementing aspects of the tidewater goby recovery plan in coordination with, and funded by, the US Fish & Wildlife Service (USFWS) through a Section 6 Cooperative Agreement awarded to the University of California, Los Angeles on May 15, 2015. The primary focus of this dissertation was to developed a quantitative framework to complete a metapopulation viability analysis (MVA) for the endangered tidewater gobies in the genus Eucyclogobius. Modeling tidewater goby metapopulation dynamics is an essential component in constructing long-term management plans rangewide throughout the California Coast. This dissertation examines more closely how these dynamics affect viability, connectivity, and long-term persistence of tidewater goby metapopulations throughout the California coast. In the first chapter of this dissertation, I conducted annual population surveys (2014, 2015, and 2017-2018) in 117 estuaries and lagoons to assess the current health and status of the tidewater gobies in five of the six Recovery Units, spanning from Bodega Bay to San Diego, CA. This massive effort has provided continuous coastal surveys over four years, and over 300 observations, which helped create the framework for a robust and comprehensive presence/absence dataset to help inform metapopulation management and recovery actions. In the second chapter of this dissertation collated all existing rangewide occupancy data, metapopulation descriptors, wetland site characteristics, and repository specimen collections into an open access database. This database will provide critical information relative to the federally endangered tidewater gobies and help inform the metapopulation viability analysis model developed in this study, as well as support continued research on the conservation and management of these incredible fish species and the coastal wetland ecosystems they inhabit. In the third chapter of this dissertation I review the general biology, conservation status, habitat impacts, and metapopulation dynamics of the northern tidewater goby (Eucyclogobius newberryi) and southern tidewater goby (Eucyclogobius kristinae). In addition, I demonstrate the effectiveness of a Bayesian approach to provide a flexible method to generate metapopulation viability analyses and provide a detailed summary of the MVA model framework, including limitations, required corrections, and future amendments that need to be addressed in order to meet the recovery criterion envisioned in the recovery plan.
Aerosol-cloud interactions are one of the largest sources of uncertainty in our understanding of the Earth’s climate system. In order to develop better predictive models and understand how the climate will respond to future changes in atmospheric composition, we must determine the sources and nature of aerosols which serve as cloud condensation nuclei (CCN), thus influencing the properties of clouds. Oceans cover 70% of the Earth’s surface and represent a major source of atmospheric aerosols. Sea spray aerosol (SSA) is formed by the action of breaking waves, whereas secondary marine aerosols (SMA) are formed from the oxidation products of gases emitted from the oceans. Biological activity in seawater (i.e. the life, death, and interactions of marine phytoplankton, bacteria, and viruses) can significantly affect the chemical composition of SSA through processing of dissolved organic matter and SMA through the emission of volatile gases. This dissertation investigates the cloud-relevant properties of SSA and SMA generated using ocean-atmosphere simulators in the laboratory, with a specific emphasis on the influence of biological activity in seawater on the properties of these aerosols. For the first time, SMA was produced from the oxidation of the headspace gases of a phytoplankton bloom grown in natural seawater, enabling measurements of its chemical composition and CCN activity. Overall, these studies show that the formation and properties of SMA are much more sensitive to biological activity in seawater than SSA. In addition, the chemical composition of SMA is highly dependent on the extent of photochemical oxidation, with a distinct shift from organic-rich to sulfate-rich composition in response to increased atmospheric aging. This change in SMA composition leads to a significant change in its hygroscopicity. These results suggest that the properties of SMA evolve temporally in the atmosphere, which has implications for CCN concentrations and cloud properties over the oceans.
The Delta Smelt (Hypomesus transpacificus) is a small Osmerid native to the San Francisco Bay Delta (Bay-Delta) in California. Delta Smelt population has declined dramatically since the species was declared as endangered in 1993, and now has been listed as critically endangered by the International Union for Conservation of Nature (IUCN). The Bay Delta is a highly modified ecosystem, and the Delta Smelt has been used as an indicator species to assess the overall health of this ecosystem. Recently, a wealth of evidence exists showing that anthropogenic intervention and change in ecosystems leads to alteration in the sensory perception of the environment by aquatic animals compromising survival in highly modified environments. One of the main modalities used by aquatic organisms to assess and survive in the wild is the olfactory system. The olfactory system is involved in pivotal functions such as recognition of predators, kin recognition, mating, foraging and migration. The olfactory system is highly susceptible to contaminants including copper, which is a common contaminant and a well-studied and measurable olfactory toxicant of fish. A link between the olfactory biology and the effects of common contaminants (i.e., copper) found in the Bay Delta on Delta Smelt is lacking. I studied the basic morphological characteristics of the olfactory organ (olfactory rosette) of Delta Smelt using histological, immunohistochemical and ultrastructural techniques; the olfactory mediated behavioral responses to predation related odorants using a behavioral standardized assay and tracking software; and finally, I evaluated morphological changes of the olfactory epithelium and behavioral responses to alarm cues after copper exposures using concentrations of 2, 8 and 32 µg/L and two exposure times (24 and 96 hours). The Delta Smelt can be classified as a macrosmatic fish, based on the morphological features of the olfactory rosette. This fish has multilamellar, paired olfactory rosettes containing a highly specialized olfactory epithelium. The olfactory epithelium was composed by several populations of cells including sensory neurons with distinct morphology and immunocytochemical features. Delta Smelt have a highly sophisticated and sensitive response to predation related odorants. They detect alarm cues in a concentration dependent fashion using olfaction and display specific behaviors (escape responses and freezing) upon detection that all together are considered as olfactory mediated antipredator behaviors. Finally, I demonstrated using histopathological and immunohistochemical techniques that Delta Smelt olfactory epithelium is highly susceptible to copper exposure at concentrations commonly found in the Bay Delta and considered as sublethal. Moreover, there were differential effects on antipredator behaviors after exposure to copper for 24 and 96 hours. Fish exposed to 8 µg/L of copper for 24 hours showed severe damage to the olfactory epithelium and hyperexcitability when presented to alarm cues. At higher concentrations, the epithelium was severely damaged, the antipredator response was absent and there were signs of histological and behavioral toxicity. The results of these experiments demonstrate that Delta Smelt is a highly olfactory species and establishes that copper contamination can impair olfactory responses at environmentally relevant concentrations in this endangered fish.