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Graduate Student Supervision
Doctoral Student Supervision (Jan 2008 - Nov 2019)
Kelps are highly successful ecosystem engineers that substantially increase the productivity of nearshore ecosystems, forming nursery habitat for other species. Despite the importance of kelps to the modern ecology of temperate ecosystems, we have a limited understanding of their evolutionary relationships, the diversification dynamics that led to their modern distributions, and the factors that determine where they are found in nature. In this dissertation, I quantitatively explore how distributions and modern ecological strategies have arisen through kelp evolution. I utilize phylogenomic approaches to determine the evolutionary relationships between kelp species and the timing of their diversification, elucidating many previously unknown phylogenetic relationships between kelps (Ch. 2). I then investigate the strategies that kelps use to survive on wave-swept shores and test for trade-offs that may have constrained their broad range of morphological variation. I use flow tank experiments and field mechanical testing to investigate how external forces from the environment interact with morphology. I show that kelps with high mechanical support also experience greater environmental forces than weaker, more streamlined species, consistent with well known trade-offs of stress resistance in other organisms (Ch. 3). I also investigate the interspecific scaling of biomass allocation in organs of kelp that are analogous to those of land plants and showed that there are shared features of how size influences morphology in both groups (Ch. 4). Lastly, I combine trait and phylogenetic information to explore patterns of trait evolution and determine how species that specialize in different environments are distributed across the phylogeny. I assess whether phylogenetic relatedness or trait differences explain the assembly of kelp communities and demonstrate that kelp communities are composed of distantly related species that have converged on similar traits (Ch. 5). Taken together, these studies offer a multifaceted perspective on the morphological and ecological diversification of kelps and demonstrate that ecological strategies are convergent among phylogenetically divergent lineages.
Macroalgae living in wave-swept environments experience a high degree of mechanical stress. Flexible algae can mitigate this stress by bending with the waves, taking on smaller, more streamlined shapes that reduce drag. Coralline algae are limited in their flexibility due to having cell walls enriched in calcium carbonate, which cause thalli to be mostly rigid. While crustose species may avoid drag by growing prostrate along the substrate, most upright coralline species have uncalcified articulations (genicula) that allow them to retain flexibility despite their calcified constraint. Articulated corallines have evolved from crustose ancestors at least three separate times, leading to articulated species within the Corallinoideae, Lithophylloideae, and Metagoniolithoideae. The repeated evolution of genicula, and the rarity of upright coralline species without them, suggests that they play a key role in the ecological success of erect corallines. While previous studies have noted structural and developmental differences among genicula in the three evolutionary lineages, I address multiple levels of genicular organization to investigate the depth of convergent evolution of these structures. I found that genicular tissues are stronger and more extensible than other fleshy seaweed tissues, reflecting the fact that genicula must undergo a high degree of stress and strain to compensate for rigidity elsewhere in the algal thallus (Ch. 2). Differences exist between articulated clades; corallinoids are particularly strong, while lithophylloids are often highly extensible (Ch. 2). Articulated clades also differ in the way genicular morphology and tissue properties are adjusted to increase thallus flexibility; corallinoids possess a high number of genicula, metagoniolithoids possess long genicula, and lithophylloids possess particularly pliant genicular tissues (Ch. 3). Both the content and structure of polysaccharides in the genicular cell wall varies depending on subfamily, reflecting differences in genicular development and potentially causing differences in material properties (Ch. 4). Results from polarized microscopy suggest that the arrangement of polysaccharides within the cell wall also plays a role in how genicular tissue responds to mechanical stress (Ch. 5). In summary, while genicula may serve similar functions in corallinoids, lithophylloids, and metagoniolithoids, I show that there is more than one way to build an articulated coralline.
Climate change is progressing rapidly and is causing shifts in ecosystem function, species distributions, biodiversity, and abundances worldwide. In this thesis, I explore the physiological and biomechanical responses of red algae in multiple life history stages to climate change. In Chapter 1, I introduce the looming threat of climate change, and some of the forces driving ocean acidification. I introduce my study system and my study species: rocky intertidal ecosystems and articulated coralline algae. I also describe potential differences in responses to ocean acidification based on life history stage. Finally, I give an overview of my dissertation and objectives. In Chapter 2, I investigate the effect that ocean acidification may have on spore stages of red algae. Under reduced pH, I document a reduction in spore settlement of both Pterosiphonia bipinnata and Corallina vancouveriensis, and weakened spore attachment in C. vancouveriensis. Results demonstrate that ocean acidification can negatively impact macroalgal spore adhesion in both calcified and non-calcified algae, but in different phases of their spore adhesion process. In Chapter 3, I explore the effect of elevated pCO₂ and temperature on the growth, calcification, and material properties of two species of articulated coralline algae. I found that increased temperatures and reduced pH were found to negatively affect growth rates of these two species of coralline algae. On the other hand, increased temperature and reduced pH had little influence on the amount of calcium carbonate in the intergenicula, and also had minimal effects on the biomechanical properties. In Chapter 4, I explore the amount of natural variability of chemistry in tidepools and attempted to relate chemical differences to differences in Corallina vancouveriensis growth, calcification, and biomechanics. In general, I found that organisms within tidepools greatly alter the chemistry of the surrounding water, and these changes are larger in magnitude than what is predicted for global climate change. I also found that, despite extreme changes in chemistry during low tides, C. vancouveriensis was still able to grow all year long.
Master's Student Supervision (2010 - 2018)
Kelp forests are one of the most productive ecosystems in the world, supporting a diverse assemblage of species. Throughout their history of study, kelp forests have undergone shifts between kelp forests and urchin barrens. Urchin barrens – rocky reefs which have no remaining kelp habitat due sea urchin grazing – have important consequences for species that rely on this habitat for survival. In Howe Sound, British Columbia Neoagarum fimbriatum is the dominant habitat-forming kelp and is the essential settlement habitat for commercially important juvenile spot prawns, Pandalus platyceros. Since 2013, the abundance of Neoagarum has declined following an increase in green urchins, Strongylocentrotus droebachiensis, due to loss of top-predator sea stars. This shift in the rocky reef community has led to concerns of continued decline in Neoagarum. This study looks at two aspects of Neoagarum persistence in the face of intense grazer pressure. First, seasonal growth patterns with respect to light and temperature variation are examined. Second, the impact of high densities of green urchins on Neoagarum loss are quantified. Seasonal growth patterns showed that Neoagarum grows throughout the year with maximal growth rates during summer, reaching up to 7% d-¹. Light was determined to be the main driver of these patterns. This was apparent particularly during spring plankton blooms when periods of minimal light at the depth of the kelp beds correlated with the lowest growth rates, while highest growth correlated with the longest days and highest light intensity. These growth rates suggest that in the absence of grazer pressure, Neoagarum has the capacity to develop dense kelp beds in a matter of months. Urchin grazing experiments showed that the relationship between urchin density and the rate of kelp biomass loss scaled linearly, but only at density below 36 urchins m-². Density-dependent restriction of green urchins was apparent at densities greater than 36 urchins m-². Despite lower per capita grazing rates at high densities it appears that so long as densities of green urchins densities remain high, their ability to consume greater than just 7% kelp biomass per day will lead to further declines in Neoagarum kelp beds.
Maintaining buoyancy with pneumatocysts is essential for subtidal seaweeds with long flexible thalli, such as Nereocystis luetkeana (Nereocystis), to achieve an upright stature and compete for light. However, as Nereocystis grows, pneumatocysts are exposed to significant changes in hydrostatic pressure. Exposure to changing hydrostatic pressure could cause complications since the pneumatocyst is filled with gases that may expand or contract, potentially causing pneumatocysts to break, flood, and no longer be buoyant. This study explored how Nereocystis pneumatocysts resist biomechanical stress and keep the developing sporophyte upright in the water. Throughout development, pneumatocysts had an internal pressure consistently less than atmospheric pressure (3 – 100 kPa), indicating pneumatocysts always experience compressional loads. The structural integrity and design of the pneumatocyst to resist buckling was assessed by measuring compressional modulus (material stiffness), calculating material stress, analyzing critical geometry, and estimating critical buckling pressure. Small pneumatocysts found at depth (inner radius = 0.8 - 0.9 cm; wall thickness = 0.2 cm) were demonstrated to have reached a critical size in development and are at greatest risk of buckling. Pneumatocysts do not adjust material properties or geometry to reduce wall stress, but they are naturally resistant to hydrostatic loads. Critically small pneumatocysts are estimated to buckle at 35 m depth, which was observed to be sporophytes’ lower limit in the field. Data suggest that hydrostatic pressure, not just light limitation, might explain the maximum depth to which Nereocystis is capable of growing. Pneumatocyst gas composition did not change throughout development, and contrary to previous studies, internal gas concentrations were different from the atmosphere with O₂, N₂, CO, and CO₂ concentrations of 59%, 40%, 1.6%, and 0.6% respectively. Furthermore, pneumatocyst surface area to volume ratio did not correlate with the exchange of gases produced from photosynthesis and respiration. As sporophytes grow, total buoyant force is steadily outpaced by the weight of growing thalli, and the risk of the pneumatocyst sinking increases. Adult sporophytes are estimated to sink when pneumatocysts volume reaches 1.3 L, close to the maximum observed size in the field.
Organisms in the intertidal zone are regularly exposed to wave action, emersion, and competition. Competition for space may have been a factor leading to the evolution of epiphytes which have circumvented this problem by growing on other algae. Epiphytism is generally considered deleterious to hosts but, is this always true? This study explored costs and benefits of interactions between the epiphyte, Soranthera ulvoidea, and its host, Odonthalia floccosa, involving biomechanics, light acquisition, desiccation, and herbivory. Drag on epiphytized and unepiphytized hosts was measured in a recirculating water flume. Epiphytes increased drag on hosts by approximately 50% at each test velocity. Increased drag caused epiphytized hosts to be more likely to break from the substratum than hosts without epiphytes. Epiphytes experienced reduced drag when attached to hosts but sometimes broke before hosts. In fact, epiphytized hosts and epiphytes were equally likely to dislodge; this suggests that drag added by epiphytes may not be entirely harmful to hosts if epiphytes dislodge half the time, reducing overall drag on epiphytized hosts. The effects of epiphytism on light acquisition, desiccation, and herbivory were also investigated. Photosynthesis versus irradiance curves were constructed for hosts and epiphytes; saturation irradiances for both were approximately 50μmol m⁻²s⁻¹, and were not significantly different from irradiances under submerged algal canopies in the field. Thus, it was inferred that these epiphytes do not likely affect host light acquisition. Also, these epiphytes may not have arisen in response to light limitation as they reached photosynthetic saturation when exposed to light levels under other algae. When hosts with and without epiphytes were exposed to air, epiphytes doubled the time required for hosts to lose 50% of the water originally associated with their thalli. By delaying desiccation, epiphytes likely reduce physiological damage of emergent hosts. Lastly, invertebrate herbivores common to this study’s field site preferred grazing epiphytes over hosts. This feeding preference could benefit hosts by diverting herbivores away from host tissue and toward epiphytes. In sum, this study demonstrates that hosts and epiphytes often benefit by closely associating; these complex interactions could help explain the evolution and persistence of intertidal algal epiphytism.
Intertidal macroalgae endure stresses associated with submerged and emerged conditions on a daily basis. Differences in physiology at high tide, low tide, and during recovery underlie spatial separation of species along the shore. Tidepools provide refugia from physical stresses associated with the low tide, and species with low stress tolerance may be restricted to these habitats. Species that survive emergence employ physiological and morphological strategies to survive exposure to pseudo-terrestrial conditions. I explored how tidepool and non-tidepool macroalgae respond to and recover from intertidal stressors, such as light, temperature, and desiccation. I investigated whether differences in physiology could explain differences in habitat distributions. To answer these questions, I explored the physiological responses of the coralline algae, Calliarthron tuberculosum (Postels and Ruprecht) E.Y. Dawson and Corallina vancouveriensis Yendo, to simulated tidal conditions. Calliarthron is restricted to tidepools, while Corallina can survive emersion during low tide. First, I documented physiological differences between the two species at high tide. Corallina performed similar to a high light adapted plant, while Calliarthron’s performance resembled that of a low light adapted plant. Surprisingly, their pigment composition did not differ, suggesting that both species are able to harvest light similarly but that other metabolic processes are at play. Second, I compared morphological and physiological strategies employed by Calliarthron and Corallina to resist stress during low tide. I found differences in the physiological responses of the two species to increased light and temperature, two chief stressors present in the tidepool microhabitat. Unlike Calliarthron, Corallina exhibited high tolerance to increasing water temperatures and was more effective at resisting desiccation via morphology. However, neither species photosynthesized in the air, regardless of hydration level. Finally, I quantified recovery upon the return of the tide. Both species recovered from warm tidepool temperatures. However, only Corallina recovered from the combination of temperature and desiccation stress associated with emergence.This study describes the variation in physiological performance of two intertidal macroalgal species during the tidal cycle, and documents several morphological and physiological strategies employed by species to survive stresses associated with low tide. Results help to explain the habitat differences between the two species.