Predicting ecological responses to changing ocean conditions is particularly challenging in highly dynamic marine ecosystems subject to multiple anthropogenic stressors. My dissertation centers upon understanding fine- and broad-scale patterns that affect energy flow through the California Current Ecosystem (CCE), a dynamic coastal upwelling zone in the eastern Pacific Ocean. I focus on trophic relationships between top predators and their prey by using an iconic indicator species – the California sea lion (Zalophus californianus; sea lions) – and a complex of key forage species to elucidate food web dynamics in the ecosystem.

In Chapter 1, I explore fine-scale temporal, spatial, and physiological patterns that drive the quality of prey species to top predators in the CCE and use bomb calorimetry to generate a novel dataset of energetics information on these forage species. I then integrate my findings with published data on the bioenergetics of sea lions to quantify how predator consumption rates can vary, given the differences in quality I observed within and among prey species. In Chapter 2, I argue that sea lions are an important ecosystem indicator of major food web shifts, which I determined by generating a ~55-year time series of sea lion trophic position using stable isotope analysis of archived tissues coupled with several environmental datasets. My findings demonstrate that regime shifts of two of the most important forage fishes to predators in the CCE can be observed through the trophic lens of sea lions. Sampling of archived tissues to create environmental chronologies is a process laden with error. Therefore, in Chapter 3, I constructed a Bayesian model to quantify the uncertainty in building ecological datasets from growth increment sampling of archived tissues (e.g., teeth, bones). This method can be applied to studies using these structures to create time series of importance for conservation and management questions.

My research fills critical knowledge gaps in our understanding of marine food web dynamics on multiple timescales that will contribute to the literature on community structure and function, while also providing important baseline data that will be useful in assessing future ecosystem states in a time of unprecedented change.

A grand challenge of the 21st century is to understand the response of ecosystems and populations of species to environmental variability and intensifying climate change. My dissertation focuses on the potential for changing environmental conditions to influence marine food webs, foraging ecology, and ultimately population success of consumers. I combined biogeochemical tools (stable isotope analyses) of zooplankton and endangered leatherback turtles with measures of oceanography and environmental conditions to evaluate changes in foraging ecology and food web dynamics over time. My research specifically focuses on long-term trends in the foraging ecology and habitat use of Atlantic and Pacific leatherback turtles and how environmental variability in the Pacific may alter food web dynamics in a critical foraging area for a declining leatherback population. My first two chapters were focused on leatherback turtles, a cosmopolitan species with populations inhabiting tropical and temperate regions throughout the global ocean. In Chapter 1, I examined the trophic ecology of North Atlantic leatherbacks over an eighteen-year period to test the hypothesis that shifts in foraging ecology or environmental conditions in the North Atlantic have contributed to leatherback population recovery. In Chapter 2, I focused on a subgroup of the critically endangered Western Pacific leatherback population that forages in the California Current. Here, I addressed questions about their diet, habitat use, and the trophic structure of leatherback prey in the California Current Large Marine Ecosystem (CCLME). These two chapters allowed me to better understand whether the continuing decline of Pacific leatherbacks was related to dietary differences potentially driven by variability in environmental conditions between ocean basins as the North Atlantic population of turtles are steadily increasing. In Chapter 3, I investigated ecosystem responses to a multi-year, warm water anomaly (a marine heatwave and strong El Niño event) in the CCLME, which is a productive upwelling system that supports the biomass of many commercially and ecologically important species, including the leatherback population that Chapter 2 focused on. My findings illustrate mechanisms through which the amount of energy transferred to higher trophic level consumers is altered by environmental variability in the CCLME. In my first three chapters, I used stable isotope analyses, which can be a valuable tool for reconstructing patterns of trophic or foraging ecology over time. However, archived tissues that are used for analyses are often stored in chemical preservatives, which may affect their potential for use in isotope ecology. In Chapter 4, I conducted laboratory experiments to test the effects of common chemical preservatives on stable isotope values to better understand how we can best use preserved and archived tissues in future studies. My research provides insight into the trophic ecology and habitat use of an endangered marine consumer. Although I found no differences in trophic position between leatherback conspecifics, environmental conditions in the North Atlantic may have contributed to the recent increases in this population. My research elucidates the effects of a strong environmental perturbation on the California Current food web, which is a productive upwelling region used by many commercially important and protected species. This work provides trophic position estimates for two leatherback populations, several gelatinous zooplankton species, and calanoid copepods in the California Current, which can be incorporated into future ecosystem or habitat models and used for ecosystem-based management of marine resources. Furthermore, my results contribute to our understanding of temporal trends in foraging ecology and food web responses to environmental variability and anomalous warming, which is useful for predicting ecosystem responses to future climate change scenarios.

Of the five species of sea turtles that inhabit the east Pacific Ocean, two, the North Pacific loggerhead (Caretta caretta) and East Pacific green turtle (Chelonia mydas), experience some of the highest rates of globally documented mortality in a productive foraging hotspot near the Baja California Peninsula (BCP), Mexico. This area, the Gulf of Ulloa, overlaps with high levels of fishing, resulting in thousands of dead turtles, many that wash up on the beach of Playa San Lázaro on the BCP. It is unknown how long loggerheads inhabit distinct regions of the North Pacific, and to what degree juvenile individuals in the population demonstrate variation in their life history patterns. Similarly, it is unknown how long green turtles occupy oceanic regions of the eastern Pacific before settling into more nearshore habitats, or how they use the Gulf of Ulloa. My research determined the residency duration at different foraging grounds within the eastern Pacific, as well as basic demographic information such as age-at-settlement, age-at-maturation, and timing of ontogenetic shifts, for these two endangered sea turtle populations.

By determining life history parameters and the length of time individuals in these populations spend in distinct high-risk habitats, managers can better understand exposure to spatially explicit threats and prioritize conservation approaches. I focused particularly on duration of time spent in the high-bycatch waters of the Gulf of Ulloa. To this end, I developed a novel technique that combined skeletochronology (the study of growth and age increments in bones) with sequential stable carbon (δ13C) and nitrogen (δ15N) isotope analysis of humerus bone growth layers. Naturally occurring stable isotope gradients exist in ocean systems such that habitats and foraging behaviors can be distinguished (i.e. nearshore vs. offshore habitats or high vs. low trophic levels). Given these isotope gradients, the combination of skeletochronology with stable isotope analysis of sequentially sampled growth layers provides a multi-year record of location, diet, size, age, and annual growth of individual turtles, allowing the reconstruction of life history and long-term habitat use patterns. The combination of these techniques allowed me to address questions that could not be answered using either technique alone.

Marine mammals spend much of their lives migrating across the ocean and are notoriously difficult to track over long periods of time. Stable isotope analysis (SIA) of animal tissues is an important tool used to determine foraging ecology and the timing of important developmental changes that occur throughout a marine mammal’s lifetime. Stable isotope values from whisker segments provide long-term information of an animal’s foraging, as whisker growth incorporates isotopic signals from their diet, such as dietary shifts that occur during birth and weaning events. We estimated the birth dates of 7–8-week-old Weddell seal (Leptonychotes weddellii) pups using the δ15N and δ13C values measured from sequentially sampled segments of their vibrissae to gain further insight into the utility of this technique to accurately predict important early ontogenetic events. Results showed that all pups shared similar stable carbon and nitrogen isotope trends. We designated a drop in nitrogen isotope values to pinpoint each individuals’ birth event and, using prenatal and postnatal whisker growth rates, found that estimated birth dates aligned with the individuals’ observed birth dates. Reconstructed timelines showed no evidence of a weaning signal. Post-birth, the δ15N values steadily increased, likely reflecting their dependency on their mothers’ milk, and the δ13C values remained mostly constant, suggesting that mothers did not forage far from their breeding colonies.

Due to the requirements for living in an extreme habitat, animals in desert ecosystems are experiencing significant deleterious effects from climate change, including those that impact their food availability. Conventional wisdom within ecology indicates that dietary generalists are more adaptable to the threats inherent to environmental changes than specialists. To better understand the potential for certain desert species to adapt to continual habitat alteration in the face of ongoing climate change, we used stable isotope analysis to investigate the degree to which members of a desert food web are potentially dietary generalists vs. specialists. We measured stable carbon and nitrogen isotope values from a top predator, sidewinder rattlesnakes (Crotalus cerastes), and several of their potential prey, including carnivorous lizards and granivorous rodents that have long been considered dietary specialists. Our stable isotope data indicate that a number of lizards were likely carnivorous as expected from previous research, whereas Yuman Desert fringe-toed (YDFT) lizards (Uma rufopunctata) and desert kangaroo rats (Dipodomys deserti), previously thought to be strict insectivores and seed-eaters, respectively, demonstrate stable isotope values more in alignment with those of generalist omnivores. In addition, we did not detect a shift in diet from lizards to rats with age as has been hypothesized for sidewinder rattlesnakes, but the isotope values from the YDFT lizards and rats overlapped significantly, hampering our ability to detect significant changes in snake diets over time. Our study provides valuable insights into the dietary niches and trophic relationships of several important desert species, which can be valuable for navigating animal and habitat conservation and management needs as we continue understanding the long-term impacts of climate change on extreme desert habitats.

Bonobos (Pan paniscus) are capable of diverse tool-use; however, research on the role of social learning on vertical tool-use transfer and the developmental stages of juveniles has been limited. Captive bonobo populations provide novel opportunities to study juvenile skill development in naturalistic social settings.This study was conducted using film taken at the San Diego Zoo over four consecutive years. The bonobo enclosure included an artificial termite mound which was provisioned to provide enrichment. All bonobos demonstrated the proper application of probe tools required to extract bait during the study, and “fishing” was a common activity. This bonobo group included two infants, a mother-raised female, and an effectively orphaned male. Both infants observed and interacted with older members as they fished. As they aged, their contacts with the artificial termite mound increased, and eventually both successfully used probe tools like their conspecific models. The skill development process involved five distinctive stages, the identification of which allowed for detailed evaluation of the social learning process of the young bonobos. The order and rate at which the juvenile bonobos acquired critical fishing skills paralleled the processes described for probe-fishing juvenile chimpanzees. Despite this inter-species concordance, the social learning environment the juvenile bonobos experienced involved a higher level of expert tolerance than that reported among probe-fishing chimpanzees. Two observed behaviors of primary models, active tool transfer to juveniles and repetitive dip exaggeration, are indicative of scaffolding, or parental modeling, in bonobos. Identified individual fishing technique preferences did not appear to be vertically transmitted.

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