Rocky shores have long served as model systems for examining the drivers of community assembly and structure, and particularly the importance of top-down versus bottom-up control. Despite growing recognition of the importance of microbial communities in these habitats, including primary production, nutrient cycling, and contributions to trophic webs, microbes have rarely been incorporated into the traditional frameworks of intertidal community ecology. Epilithic biofilms on rocky shores consist of diverse assemblages of autotrophic and heterotrophic bacteria, algae, predatory protists, and more, but are often conceptualized and investigated as phototrophs in the context of the macroscopic community. As such, these communities are hypothesized to respond, e.g., to molluscan consumers or nutrient availability, in ways that are similar to larger macroalgae. However, as I show here, biofilm communities are actually composed of multiple, co-occurring trophic levels, and consumers and nutrients likely trigger changes in trophic dynamics within the biofilm. Bottom-up processes like nutrient concentrations determine the diversity and abundance of marine organisms, limiting their growth and survival. For example, kelp populations have been declining globally as temperatures rise and nutrient availability declines. By understanding how these kelps, which act as both foundation species and conduits for nutrient inputs into marine systems, respond to variation in nutrient availability and identity, we can better understand how kelp populations may respond in the face of climate change. To examine the role of top-down and bottom-up processes in structuring epibenthic intertidal communities, I used field manipulation experiments combined with molecular tools to characterize the prokaryotic and eukaryotic biofilm communities and assess how molluscan grazers, nutrient concentrations, and temperature structured these communities. I found that biofilm community composition was largely determined by temperature and nutrient concentrations, with increased nutrient concentrations increasing the impact that grazers had on these communities, suggesting that grazers may influence these communities more through nutrient facilitation or altering dispersal processes (Ch. 1). I took a comparative experimental approach to assessing how the strength of top-down and bottom-up processes in structuring biofilm communities changes across regions in California that experience difference ambient temperatures and nutrient concentrations. I found that microbial biofilm communities were largely structured by physical distance (differences between sites and regions), with local-scale top-down and bottom-up processes having relatively weak effects on these communities in comparison. While the effects were weaker, there was regional variation in the strength of grazers and nutrients structuring these communities: grazers and nutrients had stronger effects in northern California, whereas more localized processes like establishment stage and direct grazer access had larger effects in southern California (Ch. 2). Lastly, I investigated how natural variation in nitrogen availability impacted the uptake rate of different forms of nitrogen by two species of kelp in southern California during periods of low nitrogen availability. Initial experiments included removal of biofilms from kelp blades to determine whether associated microbes might mediate nutrient uptake. The results of those experiments were inconclusive, but I subsequently found that both study species, Macrocystis pyrifera and Eisenia arborea, readily took up ammonium and nitrate, while urea uptake efficiency increased as ambient nitrogen availability decreased. Moreover, by calculating the expected rates of uptake of these nitrogen forms at various sites based on laboratory uptake experiments, I found that regenerated forms of nitrogen (ammonium and urea) contribute substantially to the nitrogen taken up by these kelps during periods of low nitrogen in the summer (Ch. 3).

A major goal of community ecology is to understand how communities are formed and which abiotic and biotic conditions constrain biodiversity and community assembly. To accurately predict and understand how communities are likely to change in response to changes in environmental conditions, it is important to understand the associations between species, the geographic patterns of species associations, how changes in associations and interactions affect community structure, and the demographic characteristics of populations throughout a species’ geographic range. To determine if the geographic distribution of species affects site diversity and potential interactions at each site, I executed an observational study of eight sites along the California coast where I categorized species as either narrow-range endemics or widespread species. I found that species were more likely to co-occur with one another south of Point Conception than north of Point Conception indicating potentially positive interactions in a more thermally stressful environment. I also found that narrow-range endemic species were the major drivers of the latitudinal patterns (Chapter 1). To determine if the effect of rockweeds on mobile invertebrate diversity and abundance differed across latitudes and at sites with differing levels of seaweed diversity, I used field observations and experimental removals of two rockweed species at three sites along the California coast. I found that rockweeds tended to increase mobile invertebrate species richness and abundance, especially at sites where functional redundancy was low (Chapter 2). Lastly, I followed populations of rockweeds at four different sites and characterized growth, survival, and reproduction of individuals over a 12-month period to determine how population demographic patterns differed between leading and trailing edge populations. Using these data, I constructed an integral projection model of each population of rockweeds. I found that populations living in the leading edge and central part of their species’ range had similar demographic characteristics, while trailing edge populations had lower population growth estimates and fecundity estimates compared to central populations (Chapter 3). My results identify and highlight some of the important drivers of biodiversity along California rocky shores, especially with respect to changes across spatial gradients and species’ ranges.

Steep environmental gradients offer the opportunity to study organismal adaptation to local conditions. Yet these local-scale gradients are often nested within latitudinal gradients, which could mediate neutral and selective processes on the local scale. I used a classic study system, a gradient in tidal elevation on temperate rocky shores, to test for geographic variation in intraspecific differentiation across tide heights in a marine primary producer. The seaweed Fucus vesiculosus is a foundation species on rocky shores throughout the temperate North Atlantic Ocean. In the Gulf of Maine in particular, F. vesiculosus occurs from the lower to upper intertidal zones along the entire coastline, spanning local and latitudinal gradients in abiotic and biotic stressors. I conducted a series of observations and experiments across the species’ intertidal distribution at sites along the Gulf of Maine coastline to: 1) identify patterns of genetic diversity and structure from tide height to regional scales, 2) test for inter-population differences in adaptation to tide height, and 3) determine if traits important to ecosystem-level processes were associated with local adaptation.

Molecular studies using microsatellite markers showed genetic variation was significant across multiple sampling scales. Patterns of inbreeding (i.e., F_IS) revealed spatial variation in isolation. Genetic differentiation (i.e., F_ST) was attributable to distance in between-site comparisons, but by environment in between-tide height comparisons. Reciprocal transplant experiments, between the upper and lower edges of the intertidal distribution of F. vesiculosus, were conducted at sites throughout the Gulf of Maine. Relative growth rates of F. vesiculosus showed adaptive phenotypic differentiation in the northeastern Gulf of Maine, countergradient variation in the central gulf, and environmentally-driven responses in the south. Importantly, observations of nutrient physiology demonstrated that nutrient uptake and allocation of tissue nitrogen towards growth were influenced by adaptation in the northeast and driven primarily by environment in the south. By combining molecular and physiological approaches, I have identified geographic variation in genetic and environmental constraints of organismal physiology and population-level processes. Given the important bottom-up role of seaweeds as providers of food and habitat, this variation could have important consequences for the associated rocky intertidal community.

Biodiversity is currently threatened at local, regional, and global scales, and identifying the species that are vulnerable to these changes is essential for conservation efforts. For example, the breadth of species’ ranges may offer important clues to their susceptibility to loss, as widespread species may be more resistant to loss than species with a narrower range breadth. To determine the potential for shifts in community interactions along the latitudinal geographic ranges of species, we examined pair-wise associations between narrow-range endemic and widespread rocky intertidal species. We surveyed rocky intertidal species composition at eight sites along the California coast from San Diego to Cape Mendocino. Four sites were south of Point Conception, and four sites were north of Point Conception. Point Conception is a major biogeographic feature for coastal marine species, where sea surface temperatures transition from cool temperate waters in the north to warm temperate waters in the south. To determine whether pair-wise species associations were significant, we compared the observed communities’ standardized effect size to a null model to determine which species occurred together more or less often than by chance. Across all sites, widespread species were considerably more abundant than narrow-range endemic species, and the majority of species were widespread. However, total species richness was unrelated to the number of widespread species, and was, instead, determined by the number of narrow-range endemic species present at a site. Our analyses suggest that species are more aggregated than segregated south of Point Conception, but the opposite is true north of Point Conception. Additionally, we found that species associations between narrow-range endemics drove the overall patterns in species associations. One possible explanation for these patterns is that positive interactions, especially those involving narrow-range endemic species, are more important in southern California’s more thermally stressful intertidal habitats.