Christopher Harley

Professor

Research Classification

Ecology and Quality of the Environment

Research Interests

community ecology
climate change
marine invertebrates
marine algae

Relevant Degree Programs

 

Research Methodology

field experiments
Laboratory experiments
Long-term surveys

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Graduate Student Supervision

Doctoral Student Supervision (Jan 2008 - May 2019)
Ecological responses to ocean acidification by developing marine fouling communities (2018)

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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Algal-herbivore interactions in a high carbon world : direct and indirect effects through individuals, populations, and communities (2017)

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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Climate change impacts on the kelp life history cycle (2015)

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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Community ecology in a warmer world : direct and indirect effects of temperature on community dynamics (2014)

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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Multiple abiotic changes and species interactions mediate responses to climate change on rocky shores (2014)

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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Evolutionary ecology of seaweed strength and flexibility (2013)

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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The influence of spatial and temporal climate variation on species' distributions, phenologies and interactions (2013)

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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Master's Student Supervision (2010 - 2018)
Effects of ocean acidification on predator-prey interactions in echinoderms (2015)

No abstract available.

Effects of ocean acidification on early developmental stages of the Pacific oyster (Crassostrea gigas) in an aquaculture setting (2014)

Ocean acidification is a great concern worldwide. It has important impacts on the shellfish industry. However, more information is needed to assess the impacts of ocean acidification (OA) on economically important shellfish in a realistic industry setting. The goal of this thesis was to determine the effects of OA on the early developmental stages of the Pacific oyster, Crassostrea gigas. To better represent industrial-scale oyster production than is possible in small-volume, short-term laboratory studies, experiments were conducted at the Island Scallops hatchery facility using large volume containers and appropriate time scales. In Chapter 2, I investigated the effects of acidification on fertilization and larval development to explore the potential links between vulnerability at these life stages and documented mass mortality events in hatcheries in the past. Elevated pCO₂ contributed to increased egg fertilization. However, not all fertilized eggs were viable, and elevated pCO₂ reduced the likelihood of further development to later embryonic stages, resulting in decreased overall fertilization success in C. gigas. Increased pCO₂ levels also negatively affected oyster larvae by reducing growth and reducing the production sufficiently large to be suitable for aquaculture rearing practices. Larval deformity and mortality also showed a trend towards increases in acidified conditions whereas feeding was reduced. In Chapter 3, I assessed early development in benthic juveniles to test for potential for carry-over and/or acclimation effects of prior larval exposure to elevated pCO₂. Settlement did not depend on pCO₂ conditions during the larval phase. However, metamorphosis was reduced when larvae had been exposed to elevated pCO₂ levels. Juvenile growth and condition were both reduced after juvenile’s exposure at higher pCO₂ levels, but shell strength was unaffected.iiOverall, these findings suggest that OA had negative impacts on multiple life history stages in C. gigas. However, the lack of larval exposure effects on juvenile growth or condition suggests an absence of carry-over effects or acclimation for juveniles. These results have important implications for the aquaculture industry and for the development of best practices for combating the effects of ocean acidification.

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Species invasion in the marine fouling communities of British Columbia : factors that influence invasion dynamics and how they may affect Botrylloides violaceus (2014)

Species invasion has been recognized as a major threat to biodiversity. Knowledge of the factors that limit the establishment and spread of non-indigenous species (NIS), such as biotic resistance and unfavourable environmental conditions, are important to their effective management. To test the biotic resistance and environmental favourability hypotheses in the fouling communities of British Columbia (BC), 22 locations were compared using settlement tiles in a large-scale survey. Biotic resistance is believed to be stronger in more diverse communities, therefore NIS richness and abundance were compared to native species richness and environmental conditions to investigate their importance using generalized and linear mixed models. Invader taxonomic group may influence biotic resistance, and environmental tolerances vary by species, therefore factors that affected Botrylloides violaceus presence and abundance were investigated as a case study. The biotic resistance hypothesis was not supported for NIS richness or NIS abundance, but could not be fully discounted due to a trend toward a negative slope between native species richness and B. violaceus presence and abundance, and the absence of predator data. Environmental variables affected NIS: salinity had a positive influence on NIS richness, NIS abundance, and B. violaceus presence, and temperature had a positive effect on B. violaceus presence and abundance. Salinity had a positive impact on native species richness as well, supporting the environmental favourability hypothesis. This suggests that knowledge of relevant environmental conditions is more important for the management of invasive species than the species richness of vulnerable communities.Environmental conditions are not static, so species invasion must be considered in the context of climate change. To understand how climate change may influence species invasion, B. violaceus presence and abundance in BC were compared to a range of abiotic conditions. This comparison informed a GAMLSS model that used linear trends from historical shore station data to project potential abundance in BC forward 50 years. Overall, the abundance of B. violaceus in BC was projected to increase. A larger increase in B. violaceus abundance was forecast for locations where conditions increased into the range favourable for growth. If temperature and salinity become more favourable for B. violaceus, as projected, climate change could intensify the invasion.

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Effects of ocean acidification on different life history stages of northern abalone (Haliotis kamtschatkana) (2010)

Anthropogenic atmospheric CO₂ levels are rapidly increasing; however, much of this CO₂ (ca. 30%) dissolves into the surface ocean (upper 200 m) where it reacts with seawater and disrupts both ocean pH and carbonate chemistry, a process termed ocean acidification. Average pH of the surface ocean has already decreased by 0.1 units since the beginning of the Industrial Revolution and is expected to drop another 0.2 to 0.4 units by the end of this century. Of primary concern is the potential for ocean acidification to dramatically disrupt biological processes, especially biogenic calcification. Different life history stages may also be affected in different ways. Furthermore, interactions between ocean acidification and other environmental perturbations are often non-additive and thus result in non-predictive outcomes. Here, I investigate the effects of ocean acidification on different life history stages of an endangered abalone, Haliotis kamtschatkana. I reared larvae and adults under elevated CO₂ conditions (800 and 1800 ppm), representing levels expected by the end of this century and beyond. Adults were also reared under two temperatures (9 and 12°C) to investigate interactions between CO₂ and temperature. Larval survival, shell size and shell morphology were negatively affected by elevated CO₂. At 1800 ppm, almost all larvae completely lacked a shell. Adults seem more tolerant of elevated CO₂. Survival, growth and feeding rates were unaffected by elevated CO₂, at either temperature. Early life history stages may be more sensitive due to differences in calcification processes. Near future levels of ocean acidification may dramatically impair early development of H. kamtschatkana but later life history stages may be more tolerant. Since H. kamtschatkana population growth is thought to be currently limited by successful fertilization, decreases in larval survival may have severe consequences for the recovery of this endangered species. Efforts to mitigate the dramatic population decline of H. kamtschatkana will need to consider the potential repercussions of ocean acidification.

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