Marine species face several challenges as a result of human activities including direct effects on populations (e.g. overharvesting) and indirect impacts on individuals (e.g. physiological responses to ocean warming and acidification). Ameliorating these impacts requires successful regulation at both the population and physiological levels. One group of critically threatened organisms are the so called “giant clams” (genus Tridacna) of tropical coral reefs. Like corals, giant clams possess calcifying larvae and host symbiotic microalgae and are therefore susceptible to environmentally-driven failure of biomineralization and symbiotic disruption. In addition, giant clams are economically important fisheries species which have been severely overexploited throughout much of their range. While marine reserves have been established to replenish dwindling giant clam stocks, their efficacy in promoting population recovery remains unknown. Similarly, little is known regarding the magnitude of climate-change associated physiological effects on giant clams. This stems, in part, from a lack of knowledge regarding the response of early life-history stages to warming and acidification and because the molecular mechanisms regulating acid-base homeostasis and symbiont photosynthesis in giant clams remain poorly characterized. I addressed these knowledge gaps in populations of the small giant clam, Tridacna maxima, from across a network of marine protected areas (MPAs) on Mo’orea, French Polynesia. I employed a combined physiological and ecological approach to (1) investigate mechanistic processes underlying acid-base regulation within giant clams, specifically in relation to maintenance of host-symbiont homeostasis, (2) measure the effects of increased temperature and elevated pCO2 on giant clam fertilization success, and (3) assess the efficacy of a recently established Marine Protected Area Network in promoting conservation and recovery of this species in an exploitative environment.

I demonstrate that giant clams regulate symbiont photosynthesis through the activity of an ion-transport protein, vacuolar-type H+-ATPase (VHA), which is strongly localized in close proximity to symbiotic algae. I further show that clam VHA actively promotes algal photosynthesis, increasing rates of O2 production and holobiont metabolic rate, and likely represents a convergent exaptation for carbon concentration shared by reef-building corals. This process has implications for climate-related responses and may offset the negative impacts of future ocean acidification in these species. I also present the first data demonstrating giant clam early life-history responses to climate change drivers and show that syngamy in giant clams is extremely sensitive to environmental warming. Finally, I demonstrate the significant, positive, effect of MPA establishment in permitting recovery of overharvested giant clam populations. T. maxima populations have increased approximately 3-fold in Mo’orea’s protected sites relative to non-protected controls and this rate of recovery is significantly higher than the global average for marine reserves. Taken together, these results suggest that effective regulation at both the population and physiological level may permit the recovery and persistence of giant clams in the face of anthropogenic challenges.

Freshwater streams are incredibly variable habitats where abiotic conditions change daily and seasonally. The species that inhabit streams must have the physiological capacity to deal with that variation. Variation that extends outside of the limits of an organism’s tolerance thresholds can cause sub-lethal or lethal stress and dictate which habitats are suitable to the organism. In addition to variation in abiotic conditions, organisms must fit into the ecological interaction web of their habitat and handle variation in biotic conditions. In my dissertation, I focus on two pathways for organisms to encounter new sources of environmental variation: invasion of novel habitats and climate change. Understanding how organisms deal with environmental variation is critical to predicting where they can live now and in the future.

In Chapter 1, I aimed to identify the temperature and oxygen conditions that limit respiration and locomotion in the highly invasive New Zealand mud snail, Potamopyrgus antipodarum. To accomplish this, I generated thermal performance curves for resting respiration rate and voluntary locomotor behaviors under normoxia and hypoxia to find the conditions that limited each performance. I found that extremely high and low temperatures limited respiration and activity, but respiration rate was more sensitive to changes in oxygen at low temperatures. Hypoxia did not significantly decrease activity. Under hypoxic conditions, activity was less thermally sensitive, increased under high temperatures, and may be fueled by anaerobic metabolism. Relying on anaerobic energy is a time-limited survival strategy, so further warming and deoxygenation of freshwater systems may limit the spread of this invasive species.

In Chapter 2, I focused on finding the abiotic and biotic conditions that explain variation in Potamopyrgus antipodarum population density in San Francisco Bay Area streams. P. antipodarum is a prolific invader of freshwater streams in California and worldwide, with the ability to form extremely dense populations that dominate the invaded habitat. To strengthen our ability to predict where this species can thrive, it is critical to understand which abiotic and biotic conditions explain variation in population density. I approached this need by measuring 25 conditions over one year in three streams with varying densities of P. antipodarum populations. The different streams could be distinguished by their water chemistry profiles. Conductivity and filamentous green algae cover were the factors most correlated to population density, but there was only marginal linear statistical support for the response to algae. Overall, P. antipodarum is robust to considerable variation in many ecological factors, and each factor may have a small effect in controlling their population sizes.

In Chapter 3, I focused on the effect that past environmental variation, specifically thermal history, had on the response to different warming regimes in the larval caddisfly Dicosmoecus gilvipes. To accomplish this, I tested the molecular physiology responses of three populations of field-acclimatized D. gilvipes from different eco-regions (mountain, valley, coast) to current and future warming scenarios. I hypothesized that distinct thermal histories could differentiate populations at baseline levels of gene expression and gene expression changes in response to daily warming and heat shock. Population-specific responses were apparent under the control and daily warming conditions, while responses to heat shock were similar across populations. In addition, underlying gene expression patterns in the daily warming and heat shock treatments were different. These results highlight the importance and limitations of measuring the stress response of wild-caught organisms in their natural environment.

Understanding how climate change affects the physiology and population dynamics of grazers that can reduce epiphyte growth on seagrass is important for predicting the future dynamics of seagrass ecosystems. Seagrass habitats provide a number of important ecosystem services, including carbon sequestration, nutrient mitigation, sedimentation and erosion control, and providing nursery habitat for fishes and invertebrates. Climate change threatens seagrass communities as increased temperature promotes photosynthesis-inhibiting epiphytic growth. Grazers have the potential to mitigate this increased epiphytic growth if their physiological performance is maintained in future climatic regimes. Phyllaplysia taylori is a grazing sea hare with two generations per year in the Zostera marina seagrass habitat along the Pacific coast of North America. It exhibits direct embryonic development with crawl-away young, greatly limiting long-distance dispersal capacity and population connectivity. In Central CA, P. taylori is a bivoltine species with non-overlapping generations that span different seasonal regimes. As a grazer species inhabiting many thermally disparate environments throughout space and time, it provides an opportunity to look at how physiological plasticity plays a role in population persistence and how this can impact the seagrass ecosystem. In my dissertation, I examined the factors that influence P. taylori’s geographic distribution at different spatial scales and variation in the plasticity of thermal physiology across life stages and among populations.

In my first chapter, I documented where P. taylori populations are found along the coast and investigated the environmental and/or ecological factors that account for their distribution. Although temperature was expected to be a major driver of population persistence, this was not the case. Nutrient-rich runoff from anthropogenically-modified land was the strongest predictor of P. taylori presence, as it may contribute to epiphyte growth resulting in increased sea hare food availability. I also found that seasonal fluctuations in eelgrass density and length, epiphytic coverage, and average temperature played the biggest roles in determining relative seasonal abundance of P. taylori. The presence/absence models applied to existing restoration sites within San Francisco Bay indicated a 53% success rate for P. taylori within currently planned restoration areas. These correlation models demonstrate that it is important to consider grazer communities when planning restoration efforts.

In my second chapter, I investigated the physiological differences among the populations examined in Chapter 1, testing for a relationship between phenotypes and thermal characteristics of the source habitat. To address intraspecific differences in thermal tolerance plasticity across their geographic range, thermal sensitivity of metabolic rate and upper critical limits (CTmax), as well as the acclimation response of these metrics were assessed. Metabolic rate estimated by whole-organism respiration rate showed depression after acute heat stress in populations with warm thermal habitat histories. This trend was only observed in lab acclimation groups above 17ºC and indicates beneficial acclimation, whereby acclimation to warmer temperatures dampens the acute heat stress response, resulting in less energy expenditure with stress. Compared with other taxa, P. taylori had high intraspecific variation in CTmax. Short-term plasticity of CTmax with acclimation varied among collection sites, but contrary to my prediction, was not correlated with microhabitat temperature regimes. Instead, short-term plasticity elevated CTmax and its acclimation capacity well above habitat temperatures in no apparent pattern. Therefore, this study does not find sufficient evidence for positive selection acting upon the plasticity of CTmax. However, on the scale of seasons within a single population, I found significant seasonal acclimatization whereby individuals collected in the summer exhibited the highest CTmax and the greatest capacity for acclimation in this trait. These data provided relevant information on season-specific phenotypes, which were investigated in the next chapter.

In my third chapter, I used laboratory acclimation temperature treatments to induce seasonally-relevant phenotypes. Within these temperature treatments, I investigated how shifts in transgenerational and developmental plasticity impacted offspring success. I found that seasonally-driven differences in offspring success were correlated with egg size and total maternal investment per clutch (transgenerational plasticity), with winter temperatures corresponding to larger, fewer eggs. Future summer temperatures resulted in significantly decreased total maternal investment with more investment per egg. Developmental plasticity sufficiently mitigated differences in maternal investment in the current climatic regime to result in equal numbers of successful offspring in all seasonal scenarios, but acclimation capacity and offspring success decreased with acute and chronic heat stress in mothers and offspring. Transgenerational and developmental plasticity decrease with high temperatures, suggesting that these life stages may be more susceptible and subject to selection with increased habitat temperature.

These studies illustrate how the physiology of an important grazer in the eelgrass ecosystem will respond to climate change and outlines potential consequences at the population level. Although short-term plasticity sufficiently buffers adults from future climate shifts, maturation is made difficult by inadequate transgenerational and developmental plastic responses. While some populations may suffer due to increased mean and variation of habitat temperatures, responses across populations are highly variable. Therefore, in restoration efforts, selection of relevant source populations of P. taylori based on thermal physiology is highly advantageous. Understanding how the physiological plasticity of P. taylori is able to compensate for future climatic shifts is important for both eelgrass restoration and in determining how physiologically-plastic taxa cope with fluctuating environments.