Christopher Harley

Extractive human systems are driving unprecedented biodiversity loss and exacerbating social inequity. The magnitude of the intertwined climate, biodiversity, and social inequity crises has prompted the development of interdisciplinary research approaches to address these complex problems. One such approach, social-ecological systems (SES), aims to understand the relationships between coupled human and ecological systems. This thesis applies an SES lens to understand the science of human impacts on and relationships with marine ecosystems and inform characterizations of system vulnerability. First, I examined the sensitivity of marine ectothermic animals to climate change by conducting a meta-analysis of the effects of ocean acidification and warming. My synthesis of nearly five hundred factorial studies demonstrates the negative effects of these two drivers, identifies specific taxonomic groups (molluscs), life- history traits (adults, sessile), and latitudes (tropical and temperate) that are more sensitive, and refutes two common assumptions about the drivers’ interactive effects. Next, I tested whether populations of a marine snail vary in their vulnerability to ocean warming based on thermal sensitivity and local rates of ocean warming. Using coupled lab and field experiments with snails from two regions in the middle of their range that differ in thermal characteristics, I found that snails from the warmer Salish Sea, an urban sea, showed greater vulnerability to ocean warming than those from the cooler central coast of British Columbia, Canada. Finally, to inform how humans can mitigate our impacts while sustaining complex relationships with the ocean, I partnered with the Sḵwx̲wú7mesh Úxwumixw (Squamish Nation) and regional stewardship organizations on a marine spatial planning project in the Salish Sea. I employed a mixed- methods community-based participatory mapping approach to characterize place-based values and outline opportunities to decolonize research and mapping processes. The results contribute important social data about place-based values, reveal value interactions, reflect knowledge system plurality, and identify avenues to advance reconciliation. Overall, this thesis highlights the vulnerability of marine life, particularly life within urban seas, to climate change and provides a roadmap for researchers and decision-makers to meaningfully steward the health and well-being of coastal social-ecological systems.

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To better predict the responses of ecological systems to climate change we must better understand how interactions between multiple stressors alter organismal function, how these changes may propagate to the community level, and how these interactions may vary across environmental gradients through time. Here, I address this gap in knowledge, primarily using a macroalgal foundation species, Fucus distichus, and its associated community, with a combination of laboratory and field experiments. First, I conducted a reciprocal transplant experiment with F. distichus from areas of differing thermal regimes and simulated a thermal stress event prior to the occurrence of an extreme heatwave. Results show that thermal history matters, as individuals originating from the cooler site that experienced the initial thermal stress had decreased photosynthetic efficiency and increased bleached thallus tissue as a result of the extreme heatwave. Second, I asked how hyposalinity modulates thermal response of early life stages in F. distichus, and whether this is mediated by historical exposure to hyposaline conditions in the parent generation. I found that hyposalinity had larger impacts on the thermal response in individuals that originated from a high saline vs. a hyposaline environment. Next, I asked how the temporal dynamics of stressors impact the interactive effects of hyposalinity and high air temperature in F. distichus from low vs high salinity regions. I found that hyposalinity reduced growth and caused more bleaching in individuals from both regions regardless of whether stressors were imposed simultaneously or sequentially. Lastly, I investigated the indirect effects of salinity on intertidal community composition through diversity surveys in high and low salinity regions, identifying the salinity tolerance of a subset of key resident species, and manipulating the abundance of grazers in a field study replicated across regions. I show that rocky intertidal shores from regions of disparate salinity regimes host distinct ecological communities, which is likely mediated by salinity-driven differences in herbivore population size and thus grazing pressure. By working across temporal and spatial scales, this research advances our understanding of how multiple stressors interact in a marine foundation species with cascading impacts on associated communities.

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As environmental stress increases due to climate change, species and the ecological communities that they comprise will be impacted, in many cases according to species’ abiotic tolerances. Ecological theory predicts that foundation species may become increasingly important for mitigating this environmental stress for the species that associate with them. However, it is often unclear how foundation species will be affected by climate change and if, and how, their ability to facilitate associated species may be altered. Here, I addressed questions stemming from this knowledge gap using field studies of intertidal, sessile invertebrate foundation species using natural and manipulated environmental stressors, primarily within coastal British Columbia, Canada. First, how are foundation species affected by realistic combinations of environmental stressors in situ? I found that an introduced oyster grew more quickly with increasing temperature and — though its survival was reduced by acutely high temperatures — it was not vulnerable to other environmental stressors, possibly because there was no temporal overlap between these and high temperatures. Second, how do foundation species and their associated community respond to extreme events? I found that a heatwave caused substantial mortality of a mid-intertidal barnacle where solar irradiance, and thus substratum temperature, was high and resulted in composition and diversity shifts in barnacle- associated communities. Third, do the impacts of environmental stress on foundation species persist through time? Within a high intertidal barnacle bed, I found that elevated temperatures in one summer had legacy effects on communities during the subsequent summer, likely mediated by differences in barnacle density. Finally, can introduced foundation species have positive effects in their introduced range on species with which they did not co-evolve? I found that high intertidal acorn barnacles, likely due to the generalist nature of their facilitation, can have positive effects in both their native and introduced ranges. Foundation species, while they are able to benefit associated species by buffering environmental stress, are often themselves vulnerable to that stress. By exploring these nuances, my work helps elucidate the importance of considering foundation species when predicting the ecological impacts of global change.

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Increasing levels of CO₂ in the atmosphere are rapidly affecting ocean chemistry, leading to increased acidification (i.e., decreased pH) and reductions in calcium carbonate saturation state. This phenomenon, known as ocean acidification, poses a serious imminent threat to marine species, especially those that use calcium carbonate. In this dissertation, I use a variety of methods (field-based experiments, surveys, meta-analysis) to understand how marine communities respond to both natural and experimental CO₂ enrichment and how responses could be shaped by species interactions or food availability. I found that ocean acidification influenced community assembly, recruitment, and succession to create homogenized, low diversity communities. I found broadly that soft-bodied, weedy taxa (e.g., algae and ascidians) had an advantage in acidified conditions and outcompeted heavily calcified taxa (e.g., mussels, serpulids) that were more vulnerable to the effects of acidification, although calcified bryozoans and barnacles exhibited mixed responses. Next, I examined an important hypothesis of context dependency in ocean acidification research: that negative responses by calcifiers to high CO₂ could be reduced by higher energy input. I found little support for this hypothesis for species growth and abundance, and in fact found that, for some species, additional food supply exacerbated or brought out the negative effects of CO₂. Further, I found that acidification stress can tip the balance of community composition towards invasion, under resource conditions that enabled the native community to resist invasions. Overall, it is clear that acidification is a strong driving force in marine communities but understanding the underlying energetic and competitive context is essential to predicting climate change responses.

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Consumer-resource interactions play an important role in determining the structure and function of ecological communities. Thus, herbivores may buffer or magnify the impacts of environmental change. In this thesis, I examine the ways in which herbivory mediates the effects of one of the most important facets of environmental change in marine ecosystems: ocean acidification (OA). Responses to OA by invertebrate herbivores are wide ranging, typically negative, and depend on species traits (e.g. reliance on calcification), population dynamics, and shifts in interspecific interactions. My goal was to conduct research across levels of biological organization to better understand the main pathways by which OA and associated increases in carbon dioxide (CO₂) will drive ecological change in herbivore-dominated systems.In Chapter 2, I examine the effect of CO₂ on herbivore growth and size-specific changes in feeding rate. I found that CO₂ had no impact on the size-specific feeding rates of the four-herbivore species I examined. However, changes in growth and body size in response to increased CO₂ may drive an overall reduction in the feeding rates of highly-calcified herbivores (e.g. urchins and gastropods), but not less calcified, crustacean herbivores. In Chapter 3, I used amphipod herbivores with short generation times to test the effects of CO₂ on per capita and abundance driven changes in herbivory. Again, I found no evidence for per capita changes in herbivory rate of this less calcified species, however increases in amphipod abundance lead to an increase in total herbivory. Finally, In Chapter 4, I manipulated both the abundance of gastropod herbivores and CO₂ in experimental tidepool communities in situ. I found that the indirect effects of CO₂ via the reduction of calcified herbivore pressure had a larger impact on tidepool community than CO₂ had directly.These results show that changes in herbivore pressure in response to OA will be driven primarily through changes in individual body size and herbivore abundance. Further, these changes in herbivory pressure can be more important in determining community structure under conditions of high CO₂ than other species-specific responses.

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Anthropogenic climate change will cause changes to the abundance, distribution, and survival of species in ecosystems worldwide. Kelps are foundation species that form the structure of temperate, marine ecosystems on coastlines worldwide. Kelps support highly productive communities that are ecologically and economically valuable, but are susceptible to the increases in environmental stressors associated with climate change. This susceptibility varies with life history stage, with macroscopic stages less sensitive to environmental stress than microscopic stages. I addressed the effects of climate change on the different life history stages of intertidal kelp from rocky shores on the Pacific coast of North America. I began with two studies on the interactive effects of multiple climate stressors on microscopic stages of kelp. Increasing temperature, CO₂, and UV caused mechanical and functional damage to zoospores during their motile phase, and caused further reductions in settlement, germination, and adhesion of the initial sessile phase of the life history cycle. Settlement style was also affected, with decreased time spent looking for suitable attachment locations and microenvironments, and overdispersion of spore settlement distribution, which has been shown to decrease fertilization rates and sporophyte abundance. In my final research chapter, I describe the effects of increases in frequency of extreme warming events on macroscopic juvenile and adult kelp sporophytes. I also manipulated adult density in situ to determine the stress ameliorating affect of neighbor proximity on both juvenile recruitment and seasonal adult growth along a vertical tidal gradient. Extreme warming treatments reduced recruitment and seasonal growth of adults in the upper shore when adult density was low and environmental stressors were not mitigated by neighboring individuals. All other treatment combinations showed slightly positive effects of warming on recruitment and adult size. I predict that the aforementioned population effects resulting from increases in frequency of extreme warming events will cause an overall reduction in this species’ habitable vertical space in the intertidal zone. The combined impacts of overall reductions in microscopic life history stages with decreasing recruitment and habitable space for the macroscopic life history stage indicate overall reductions in abundance of future populations of intertidal kelp species.

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As the Earth’s climate changes so too do its ecosystems, due to shifts in abundance, biodiversity and interaction strengths among their constituent species. Although warming will simultaneously affect many aspects of ecological communities, disentangling the abiotic and biotic contributions will improve our understanding of how assemblages of interacting species will respond to climate change. My goal was to determine how warming affects community assemblages via direct (mediated by organismal physiology) vs. indirect effects (mediated by species interactions). I addressed this with 12-16 month-long manipulative experiments in the rocky intertidal zone of Salt Spring Island, Canada. I created a novel in situ method for increasing substratum temperature for settling benthic organisms, using black- and white-bordered settlement plates. In the first experiment (Chapter 3), I monitored the response of functional groups and diversity to warmed treatments. Results from this experiment suggest that communities in thermally stressful habitats respond to warming via the interplay between species-specific physiological responses and secondary adaptive strategies such as behavioral microhabitat selection. In Chapter 4, I concentrated on the direct effects of warming. As a case study, I monitored the direct effects of in situ warming on the vital rates of two competing barnacle species. Warming negatively affected both species of barnacles, however the population of the competitive dominant was more severely affected than the subordinate species, leading to a temperature-induced change in space occupancy. In Chapter 5, I focused on the indirect effects of warming on community dynamics by manipulating temperature and herbivore access to communities. Community structure and successional trajectory differed markedly between treatments, due to disturbance from herbivores and high species turnover due to warming. Despite the stochastic nature of development, warmed communities with herbivores ultimately lost the variability created by herbivore-associated disturbances, resulting in highly similar assemblages between warm and cool treatments. These results illustrate how environmental change can alter species-specific thermal responses, complex population dynamics, and interaction strengths, with cascading impacts on community dynamics. They further demonstrate how assemblages of multiple, interacting species will respond to climate change, which is imperative if we hope to effectively prepare for and adapt to its effects.

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Anthropogenic climate change poses a serious threat to biodiversity. Accurate predictions of the ecological consequences of future abiotic change will require a broad perspective that takes into account multiple climate variables, species-specific responses, and intra- and interspecific dynamics. I addressed these issues in the context of a marine rocky intertidal community to determine how abiotic and biotic factors can mediate the effects of climate change. I began with two studies on the organismal-level effects of multiple abiotic variables. In the first study, I found that acute exposure to low salinity reduced the survival of littorine snails facing thermal stress, but that ocean acidification (OA) had no such effect. In a second study, I showed that sustained exposure to increased temperature and OA had positive and additive effects on the growth and feeding of the purple ochre sea star. These findings demonstrate that studies of multiple climate variables will be important not only to identify additive and non-additive effects, but also to determine which climate variables will be detrimental for a given species. Next, I measured how species-specific responses to climate change can alter species interactions. By quantifying the effects of body size on the feeding behaviours of sea stars preying on mussels, I demonstrated that climate-driven changes in body size can have profound impacts on the strength of this interaction. Finally, I investigated how population-level responses to multiple abiotic variables can be affected by the presence of an interacting species. I built a predator-prey model that simulates the ecologically important interaction between the purple ochre sea star and its preferred prey, mussels. Using empirical estimates of sea star and mussel responses to increased temperature and OA, I simulated their interaction under various climate scenarios. I found that predation exacerbated the effects of climate change on mussel populations, and that climate change increased the strength of the sea star-mussel interaction. My work demonstrates that the effects of climate change will likely be mediated by a combination of biotic and abiotic factors, and that these factors should be considered when making predictions about the ecological consequences of climate change.

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An organism’s success is largely dependent upon its ability to function and survive within the physical constraints of its environment. The wave-swept shoreline is one of the most mechanically challenging environments on Earth, with passing waves imposing hydrodynamic forces comparable to those in a hurricane every 5-10 seconds. Nonetheless, the wave-swept intertidal hosts an exquisite diversity of plants and animals. I used field and laboratory techniques to examine morphological and material adaptations of seaweeds to life in high-energy environments. In Chapter 2, I experimentally manipulated size and shape of 16 species of foliose red algae and showed that variation in tissue material and structural properties explain differences in hydrodynamic performance among species- thinner, more flexible tissues allow blades to reconfigure in flow and reduce drag. Because material and structural properties may shift through an organism’s lifespan, I then investigated how reproduction and aging impact seaweed mechanical traits. In Chapter 3, I documented the mechanical costs associated with reproduction in the winged kelp, Alaria marginata, and found that shifts in other structural and material traits compensated for the increased drag associated with reproductive blades. In Chapter 4, a survey of 27 species of foliose algae showed that aging affected material properties of all species similarly. However, the implications of aging tissues on mechanical design varied with the growth form of the species: apically growing red algae have their oldest (stiffest) tissue attaching their blades to the substrate, while kelps, whose blades grow basally, are supported by their newest (most flexible) tissue. Finally, in Chapter 5, I tested for intraspecific variation in mechanical traits and found that variation among individuals (Egregia menziesii) at an exposed site accurately predicted survivorship during winter storms. Individuals with weaker fronds were more likely to survive because their increased propensity to self-prune in smaller waves reduces their risk of dislodgement in larger waves. Taken together these results support the notion that the material and structural properties of organisms have important functional consequences and highlight how mechanical traits can impact ecological and evolutionary processes.

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With climate change, species are shifting their distributions polewards and upwards, and advancing their phenologies. However, there is substantial interspecific variation in these responses and ecologists are having difficulty explaining why. Understanding this variation is critical as it is likely to lead to widespread consequences for trophic interactions and ecological communities. In this thesis, I test several hypotheses concerning the causes and ecological consequences of interspecific and intertaxonomic variation in climate-distribution and phenology-temperature relationships. First, I tested and found support for the hypothesis that species from different taxonomic groups vary in the strength of climate-distribution relationships, likely because of differences in their life history strategies. However, my results suggest that dispersal ability is unlikely to be the key trait affecting species' geographic distributions at broad scales.Across broad-scales, I found that butterfly and plant phenologies were strongly affected by temperature, suggesting that phenological shifts in response to future climate change are likely to be widespread. Flight season timing of early-season butterfly species and those with lower dispersal ability was more sensitive to temperature than later-season species and those with greater dispersal ability, suggesting that ecological traits can account for some of the interspecific variation in phenological sensitivity to temperature. Differences in phenological sensitivities of butterflies and plants to temperature imply that shifts in phenological synchrony are likely and could be substantial for interacting species, potentially resulting in important fitness consequences. Finally, experimentally warming the egg masses and larvae of the western tent caterpillar (Malacosoma californicum pluviale) placed on the branches of its host plant, red alder (Alnus rubra), in the field led to opposing direct and indirect effects on larval development. Warming significantly advanced larval but not leaf emergence, which initially prolonged larval development. However, once leaves were present, warming accelerated larval development, resulting in no overall effects on larval development.Taken together, this thesis demonstrates that to understand the full implications of climate change for species and communities, accounting for species' life history strategies and interactions will be essential. However, without more quantitative estimates of the fitness consequences of shifts in phenological synchrony, this understanding will be limited.

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