One challenge of global change biology is understanding the fate of organisms under future pH change in variable coastal environments (Shaw et al., 2013). Coastal pH dynamics can vary at the global scale (Hofmann et al., 2011), as well as at finer regional scales (Frieder et al., 2012), and this mosaic of pH exposure will likely play a large role in mediating the fate of coastal organisms to near-future change.

Through this dissertation, I deploy oceanographic sensors to categorize these changes at a variety of scales, and pair these results with biological experiments designed to investigate the response of juvenile life stages to current and future extremes. I deployed and retrieved moorings, conducted time series data analysis, deployed caged outplant experiments, spawned and cultured sea urchin embryos, and conducted respirometry on macrozooplankton.

This dissertation consists of 4 chapters: 1) deploying sensors to investigate fine-scale spatiotemporal variation in a Southern California kelp forest, 2) conducting a transgenerational experiment to the biological performance of offspring when adults are conditioned inside of a kelp forest environment, 3) gathering a long-term time series of ocean pH in Antarctica by deploying oceanographic sensors under the fast ice, and 4) investigating the metabolic response of juvenile Antarctic pteropods to current and near-future extremes of temperature and pH.

Anthropogenic carbon emissions are predicted to alter marine ecosystems. One such change is the decline in ocean pH, known as ocean acidification. Model predictions of ocean acidification have guided biological experiments for more than a decade. Many studies predict negative consequences of future ocean pH on marine species. To understand how species will respond to future conditions, however, knowledge of present-day pH exposures is necessary and often limited. In this dissertation, I described present-day pH variability in three coastal regions and used the data to design laboratory experiments assessing the physiological response of two organisms, sea urchins and mussels, to changing ocean conditions. As recorded by autonomous pH sensors, I found three unique patterns of coastal pH variability. Near-shore Antarctica was characterized by a steep seasonal increase in pH and pH variability during summer phytoplankton blooms. The northern Channel Islands, California, exhibited event-scale and diurnal pH variability due to primary production of phytoplankton and fixed vegetation. Only mild effects from upwelling were detected at the islands, suggesting that this region may become a spatial refuge from extreme low pH in the future. Finally, Oregon was characterized by event-scale decreases in pH due to periodic upwelling events. The results from this research show that many coastal species experience short-term changes in pH that are within the same magnitude of change predicted for ocean acidification by the end of the century. While such present-day exposures to pH variability may promote tolerance of future pH change, these near-shore regions are also characterized by unique patterns of thermal stress. I conducted two studies to investigate the interactive effects of pH and temperature on organismal physiology. First, Antarctic sea urchin, Sterechinus neumayeri, early developmental stages (EDSs) currently experience < 2 °C seasonal warming and may only experience a few degrees of ocean warming over the next 100 years. Despite development under pH and temperatures outside of current exposures, S. neumayeri EDSs exhibited high tolerance of a one-hour heat stress test, suggesting this species may be more resilient to ocean change than previously thought. Second, unlike Antarctic species, intertidal species at mid-latitudes experience daily temperature fluctuations that can exceed four times end-century predictions of ocean warming, due to tidal cycles. In Oregon, upwelling events enhance this temperature range by periodically delivering cold, low pH water to the intertidal zone. Depending on sea water conditions simulating an upwelling event (cold, low pH) or wind relaxation (warm, high pH), the intertidal mussel Mytilus californianus generated different transcriptomic signatures of the cellular heat shock response, following exposure to aerial heat stress. This suggests that future changes in seawater conditions may alter the heat stress tolerance of M. californianus during low tides. The results from this dissertation highlight the importance of designing experiments that reflect species’ present-day and future multi-stressor environment, in order to generate ecologically relevant conclusions. As anthropogenic stressors continue to take hold of coastal seas, understanding the biological consequences is critical for management and conservation efforts.

Ocean acidification (OA) and rising sea surface temperatures will likely shape the structure and function of coral reefs in the future (Fig. 1). Understanding the sensitivity of corals to ongoing shifts in pCO₂ and temperature is imperative as coral are the engineers of the coral reef ecosystem. Specifically, coral larvae may be a life history stage of corals that is particularly vulnerable to environmental stress. Shifts in physiological processes in response to environmental conditions may affect the success of larval dispersal and recruitment.

The aim of this dissertation was to examine the physiological plasticity of coral larvae in response to two potentially interacting anthropogenic stressors - OA and warming. Pocillopora damicornis (Linnaeus, 1758) was an excellent study organism for this research given its ubiquitous Indo-Pacific distribution, reef-building role, and long dispersal potential. To accomplish the objectives of this dissertation, I conducted laboratory experiments in which P. damicornis larvae were exposed to seawater of different pCO₂ and temperature conditions. P. damicornis larvae were collected from populations in Moorea, French Polynesia and southern Taiwan.

To understand the consequences of OA and warming on the physiology of P. damicornis larvae, I employed a holistic approach, examining the response of a suite of physiological processes from the levels of gene expression up to the level of the whole organism. I used metabolic rate and lipid utilization as whole-organism techniques for assessing the effects of OA and warming on larval energy consumption. Planulae released after the peak of spawning experienced metabolic suppression under high-temperature, high-pCO₂ conditions. There was evidence of biochemical limits of increasing oxidative capacity to satisfy elevated energy demands under future ocean conditions. Measurements of lipid utilization suggested that the metabolic costs of tolerating OA and warming will be greatest when both environmental stressors occur simultaneously. Larvae released at the peak of spawning will experience greatest changes in lipid content in response to OA and warming, with associated changes in buoyancy that affect their dispersal potential.

The organism-level studies revealed physiological plasticity within coral larval energy consumption. Biochemical and transcriptomic techniques were used to better understand the underlying mechanisms. P. damicornis larvae increased their total antioxidant potential in response to oxidative stress under exposures to high pCO₂ but not elevated temperature. Furthermore, OA-induced hypercapnia caused increased acid-base regulation, observed through elevated pNPPase activity of Na⁺/K⁺-ATPase. As was observed at the whole-organism level, physiological traits varied between cohorts of larvae. Finally, comparisons of gene expression profiles revealed down-regulation of genes under single-stressor treatments but up-regulation of genes when high-pCO₂ and high-temperature co-occurred.

An important facet of my dissertation research was to provide environmental context for the results of my biological experiments. I deployed autonomous pH and temperature sensors on the fringing reefs where the experimental corals were collected. The time series of pH and temperature approximated the conditions of the water mass bathing the reef to which the study organisms were acclimatized and into which the larvae would have been released. These environmental data confirmed that control treatments in the laboratory experiments were within the range of conditions experienced on the reef. The elevated pCO₂ treatment levels were not observed in the present-day time series. Additionally, pH and temperature regimes differed between reefs in Moorea and Taiwan. pH and temperature were on average lower in Taiwan and more variable in Moorea. Temperature was on average lower and more variable in Taiwan. These results highlight the importance of generating such an environmental context for study species. Environmental data informed metrics of biological performance of individuals at these sites as well as the potential heterogeneity of phenotypes across the biogeographic species range, products of local adaptation to regimes of pH and temperature.

The rapid pace of global climate change is challenging marine species worldwide. Increases in average seawater temperatures, combined with extreme climatic events such as marine heatwaves (MHWs), are pushing organisms near or past their physiological tolerance limits. To predict how these stressors will impact species and ecosystems, knowledge of thermal limits and the capacity to adjust these limits via acclimation is critical. This is especially true for species living near their thermal limits or species that vary in sensitivity to thermal stress across their life history.In my dissertation I examined how changes in ocean temperature are impacting two ecologically important species in coastal waters of the Northeast Pacific, the California mussel (Mytilus californianus) and the purple sea urchin (Strongylocentrotus purpuratus). For both study organisms, I began by examining how the thermal experience of adult animals was altered during MHW events using data collected by long-term monitoring programs. Here, I found that across the biogeographic range of M. californianus, mussels differed in thermal exposure during MHW events where exposure of the Oregon and California populations differed in the onset of elevated temperatures and the proximity to optimal performance thresholds. Regarding S. purpuratus, I found that MHWs coincide with reproductive life history stages that may have implications for gametogenesis, spawning, and larval development. For early life history events in my study organisms, I examined transgenerational and intragenerational plasticity as an acclimatory response mechanism to warming oceans. In a field-to-laboratory experiment using intertidal mussels, I investigated transgenerational plasticity in nature by examining how parental exposure to differing thermal regimes that exist across tidal height and season impact offspring phenotype. To further examine the influence of developmental temperature on larval performance, offspring were reared at two developmental temperatures. At the veliger stage, physiological performance of offspring was assessed via measurements of larval body size, respiration rate, and thermal tolerance. Results from this study show that seasonal acclimatization of adult M. californianus and larval developmental temperature had prevailing effects on offspring performance. Lastly, to study whether MHWs might induce a transgenerational response in S. purpuratus, adult urchins were acclimated to MHW and non-MHW conditions in the laboratory during their period of gametogenesis. Following the adult acclimation, offspring from each parental treatment were reared in reciprocal conditions. To assess for transgenerational and intragenerational effects throughout ontogeny, thermal tolerance and body size of each offspring treatment was measured at critical developmental stages. Embryos from MHW-acclimated females were more thermally tolerant with higher LT50 values compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of development - early gastrula and prism. To examine maternal provisioning as a means to also alter embryo performance, I examined egg size and biochemical composition. Here I found that eggs from MHW-acclimated female had higher total protein concentrations. Overall results from my dissertation research highlighted natural temperature variation experienced by M. californianus and S. purpuratus, and how this thermal exposure was influenced during heatwave events. Further, using a combination of field and laboratory experiments I provided evidence for transgenerational and intragenerational acclimation to alter performance of early developmental stages.

Marine heatwaves (MHWs) are becoming an increasingly pervasive threat to marine ecosystems. Projected increases in the frequency and intensity of future MHW events highlight the need to assess the adaptive capacity of marine organisms to such extreme events. While the massive mortality caused by MHWs is frequently observed, the sublethal consequences for reproduction and development serve as understudied areas of research. Phenotypic plasticity, the ability of an organism to change its physiology and/or morphology without alteration to the genome, presents an avenue in which the effects of MHWs can be transduced across life history stages. In this dissertation, I explored the impact of elevated temperatures associated with MHW events on the fertilization process and early development of two species of sea urchin found in the Santa Barbara Channel (SBC).First, I used the purple urchin species, Strongylocentrotus purpuratus, to measure the effects of male thermal history on fertilization and early development. In the lab, male urchins were acclimated for one month to either non-MHW or MHW-like temperature conditions, as determined by temperature data collected in the SBC during past MHW events. Fertilization trials and offspring rearing were then conducted at both temperatures to assess sperm and developmental performance. While sperm appeared robust to elevated temperatures during fertilization, sperm produced by MHW-acclimated males had overall diminished fertilization capacity as compared to those acclimated to non-MHW temperatures. For early developmental stages, the effects of paternal temperature were masked by the influence of developmental thermal conditions, where elevated temperatures resulted in larger offspring. Alternatively, the thermal physiology of offspring was significantly influenced by the interaction of paternal and developmental temperatures. Here, offspring had a higher thermal tolerance when their developmental temperature matched that experienced by their sire, possibly hinting at an adaptive paternal effect. The influence of fertilization temperature on later developmental success was also explored in the summer-spawning sea urchin species, Lytechinus pictus. For this experiment, fertilization trials were performed under one of three temperatures representing: ambient, current MHW, and future MHW temperature. The resulting embryos from each fertilization treatment were then split and raised under the three temperatures. Here, elevated temperatures during fertilization had largely negative effects on fertilization success and the performance of later developmental stages. The number of successfully hatched and gastrulated embryos, representing key stages of development in echinoderms, was significantly lower in embryos produced from fertilizations at both MHW conditions than those from fertilizations under ambient conditions. Overall, the results of this dissertation highlight the importance of the reproductive response to extreme events like MHWs. The carry-over effects within and across generations seen here, show that the stress response of individual life history stages should not be studied in isolation, and that the negative effects of MHW events may persist long after these events have passed.

Marine heatwave (MHW) events defined as prolonged periods of anomalously high seawater temperatures have emerged as influential and disruptive climate-change driven disturbances in coastal oceans, threatening marine biodiversity worldwide. As a physical phenomenon, MHW events are extreme disturbance events in coastal marine ecosystems and have impacted marine invertebrate communities. In coastal California, impacts of a major MHW in 2014 to 2016 included major declines in the kelp canopy biodiversity, high mortality of abalone, and altered biogeographic ranges of marine invertebrates. Recent modeling efforts suggest that MHW events will intensify in frequency and intensity in the future, with estimates that MHW events will become annual events under “business as-usual” emission scenarios. In this light, my dissertation at the University of California, Santa Barbara (UCSB) in the Hofmann Lab examined adult and early stages of an emerging shellfish fisheries species, a benthic gastropod, the Kellet’s whelk (Kelletia kelletii) in the ecological context of MHWs.

Global climate change will likely impose selective pressures on biodiversity to not only increase limits for environmental stress, but the phenotypic plasticity of those limits. While we know a great deal about natural selection on performance traits such as upper thermal tolerance, our knowledge of the evolution of plastic responses to the environment is limited. Whether and when the plasticity of performance traits like thermal tolerance and body size incur fitness costs and benefits is unclear. Opposing theories and a lack of empirical research have resulted in a poor understanding of genetic variation underpinning adaptive phenotypic plasticity. Here I report the results of my dissertation research, which aimed to study ecological and evolutionary processes shaping (i) fitness effects of plasticity in thermal tolerance, (ii) intraspecific variation in plastic and evolved responses to warming, and (iii) the heritability of plastic responses to the environment. Studying populations and families of two coastal marine invertebrates, the intertidal copepod Tigriopus californicus and the purple sea urchin Strongylocentrotus purpuratus, I demonstrated potential for plastic responses to global change to evolve via natural selection evidenced by fitness effects and heritability of phenotypic plasticity. However, this evolution may be constrained by factors including fitness tradeoffs between performance and its plasticity, low genetic variation for maladaptive plasticity, and countergradient variation in performance reducing genetic variation for plasticity.

Within climate change biology, the red sea urchin Mesocentrotus franciscanus has remained relatively overlooked despite its sizeable ecological and economic importance, particularly within the context of multi-stressor effects. I assembled and described a developmental transcriptome for M. franciscanus, providing a useful molecular resource with which to study this organism. I then examined both the physiological and molecular mechanisms that underlie the response of early developmental stage (EDS) M. franciscanus to different combinations of pH levels and temperatures that represented ecologically relevant present and future ocean conditions. Elevated pCO2 levels decreased embryo body size, but at the prism embryo stage, warmer temperatures helped to offset this via an increase in body size. Warmer temperatures also slightly increased the thermal tolerance of prism stage embryos. Neither pCO2 nor temperature stressors affected prism metabolic rate as measured by rate of oxygen consumption. Gene expression patterns differed by developmental stage and by temperature exposure. Elevated temperatures led to an up-regulation of cellular stress response genes. Under colder temperatures, the embryos exhibited an up-regulation of epigenetic genes related to histone modifications. There was a comparatively minimal transcriptomic response to different pCO2 levels. Examining the physiological and molecular responses of EDS M. franciscanus to multiple stressors provided much needed information regarding a species of significant ecological and economic value by examining its capacity to respond to stressors related to climate change and ocean acidification under an ecologically relevant context.

I also investigated the role of transgenerational plasticity (TGP), in which the environmental conditions experienced by parents affect progeny phenotypes. TGP may provide a valuable mechanism by which organisms can keep pace with relatively rapid environmental change. Adult S. purpuratus were conditioned to two divergent, but ecologically relevant pH levels and temperatures throughout gametogenesis. The adults were spawned and crossed, and their progeny were raised under different pH levels to determine if maternal conditioning impacted the response of the progeny to low pH stress. I investigated maternal provisioning, a mechanism of TGP, by measuring the size, total protein content, and total lipid content of the eggs that they produced. Acclimatization of the adult urchins to simulated upwelling conditions (combined low pH, low temperature) appeared to increase maternal provisioning of lipids to the eggs but did not affect egg size or protein content. I also investigated the physiology and gene expression of progeny responding to low pH stress, which were affected more by maternal conditioning than by offspring pH treatment. Maternal conditioning to simulated upwelling resulted in larger offspring body sizes. Additionally, I found the progeny expressed differential regulatory patterns of genes related to epigenetic modifications, ion transport, metabolic processes and ATP production. This work showed that adult exposure to upwelling conditions can improve the resilience of EDS progeny to low pH levels.