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In this dissertation, I use a combination of laboratory mesocosm experiments, observational field surveys across spatial and temporal scales, and a manipulative field experiment to understand the role of animal-excreted ammonium in driving microbial and algal function in a rocky intertidal ecosystem. By studying the influence of naturally relevant ammonium concentrations on species interactions, I have assembled baseline data against which predicted environmental change can be compared. Many coastal ecosystems are nitrogen limited. Nitrate is the quantitatively dominant form of dissolved inorganic nitrogen (DIN) delivered to intertidal biota from the oceanic water column but locally regenerated animal-excreted ammonium is another important DIN source. Both primary producers and chemolithotrophic microbes (bacteria and archaea) utilize ammonium. Through a series of outdoor mesocosm experiments (Chapter II: Context-dependent algal-microbial competition for a shared nitrogen) I isolated the interaction between marine phototrophs (algae) and benthic microbes in terms of ammonium. Experiments tested the hypothesis that the interaction between benthic microbes and primary producers is bidirectional and context-dependent. Results indicate that phototrophs and microbes compete for the shared resource of ammonium: periphyton blooms limited microbial nitrogen use, and microbial biofilms affected macroalgal growth. Data presented in this chapter provide a baseline for potential range of a simplified natural interaction between algae and microbial biofilms that could be expected in natural systems. Microbial-algal interactions likely play an important role in net community interactions, a link will improve community structuring models. Determinants of microbial community structure in aquatic environments remain poorly understood. In rocky shore environments, microbes might be influenced by both local abiotic and biotic factors, as well as larger-scale physical drivers. In Chapter III: Drivers of variability among NE Pacific rocky intertidal microbial communities, I used spatially and temporally broad field surveys and characterized microbial community composition and structure from a rocky intertidal benthic biofilm across four sites and two years to address three questions: 1) Within a site (<100m), do benthic surfaces of tidepools and emergent rock host distinct microbial communities? 2) Do intertidal microbial communities vary on a regional scale (>25km), between sites? 3) Are microbial communities temporally stable? I sequenced microbial communities cultured in situ on replicated artificial surfaces deployed May-August in 2013 and 2014 at four southwest-facing sites in the San Juan Islands, WA, USA on both emergent rock and in permanent tidepools. Simultaneous with microbial community analysis, I quantified neighboring macrobiota and local environmental variables. Results from this chapter indicate strong local control of microbial community composition. Microbial communities were highly differentiated between habitat types (tidepools, emergent rock). Several phototrophic cyanobacteria were tightly associated with emergent substrate, suggesting that temperature, desiccation, and light are strong drivers of community variability. Despite variation in macroscopic community composition, sites hosted only weakly differentially structured microbial communities. Taken together, these results indicate intersite (>25km) homogeneity of intertidal microbial communities present in biofilm, with overwhelming intrasite (between-habitat; <100m) heterogeneity. I observed community turnover on a coarse annual scale (August 2013 to August 2014), with maintenance of source habitat identity. Although distribution of microbial taxa was broadly regional, microbial community structure in this NE Pacific rocky intertidal system was strongly environmentally selected. Growth of primary producers is often limited by the single factor necessary for growth that is available in shortest supply; a single limiting factor can limit the distribution and productivity of an entire guild of organisms. In the nearshore and intertidal environment, nitrogen limitation can be ameliorated by animal regenerated ammonium, but algae and ammonia oxidizing benthic microbes compete for this shared resource. In Chapter IV: Algal-microbial response to rocky intertidal ammonium availability, I used field dispensers to elevate ammonium several times above ambient levels at sites with measured differences in animal composition, testing the hypothesis that ammonium availability drives algal and microbial function in a temperate rocky intertidal system. I queried whether elevated ammonium gets immediately incorporated into local microbes and phototrophs, and whether a site with elevated animal abundance (and animal-excreted ammonium) leads to a microbial community that utilizes this ammonium, looking at microbial identities and associated genes. Our simulated animal regenerated ammonium drove microbial community structure to resemble that in naturally high ammonium tidepools, but only at our low-animal site. Macroalgae did not utilize our experimentally elevated ammonium, but the photosynthetic biofilm did show an ammonium treatment response that was strongest at the low-animal site. This study contributes to better prediction of the consequences of human-induced changes in nutrient cycles in the productive temperate rocky intertidal habitat. Understanding the interaction between microbes and algae in systems with varied natural and enhanced levels of N will help guide coastal management. Microbial composition and function has been largely ignored in studies of rocky shore community assembly. Through observational and empirical investigations, this dissertation quantifies how microbes contribute to rocky shore productivity via interactions with ammonium-excreting animals, the microbial potential to retain N in coastal waters, and human impacts (e.g., harvest of marine fauna, terrestrial agriculture). In Chapter V: Microbial associations with macrobiota in coastal ecosystems: patterns and implications for nitrogen cycling (written collaboratively), I (along with my coauthors) present a broadened view of interactions between macrobiota and associated microbial communities. Although macrobiota can have significant effects on nitrogen cycling via excretion by macrofauna and assimilation by macroflora, many macrobiota also host or facilitate microbial taxa responsible for nitrogen transformations. This is an area of expanding interest in coastal marine systems, where nitrogen is a limiting nutrient. Our understanding of the diversity of microbes associated with coastal marine animals and macrophytes is increasing, and recent studies indicate that the microbiomes of macrobiota may directly contribute to nitrogen cycling. In this chapter, we review the roles that macrobiota play in coastal nitrogen cycling, appraise current understanding of macrobial-microbial associations in terms of nitrogen processing, and suggest implications for coastal ecosystem function as animals are harvested and foundational habitat is lost or degraded. Given the biodiversity of microbial associates of macrobiota, we advocate increased research into the functional consequences of these associations for the coastal nitrogen cycle.


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