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Nutrient Enrichment Promotes Eutrophication in the Form of Macroalgal Blooms Causing Cascading Effects in Two Anthropogenically Disturbed Coastal Ecosystems

Abstract

Humans are impacting almost every major ecological process that structures communities and ecosystems. Examples of how human activity can directly control key processes in ecosystems include destruction of habitat changing trophic structure, nutrient pollution altering competitive outcomes, overharvesting of consumers reducing top down control, and now climate change impacting virtually every global biogeochemical cycle. These human impacts may have an independent effect on the ecosystem, but they also have the potential to cause cascading effects and promote subsequent stressors. Also, these impacts are not limited to a particular system or geographic location making research on their overall effects vital for management practices. For example, tropical reefs have been transitioning from coral to mixed communities dominated by macroalgae, motivating research on how macroalgae respond to anthropogenic stressors and interact with each other during these stressful events. Further, while eutrophication of coastal estuaries due to increased anthropogenic supplies of nutrients has been of critical global concern for decades, the potential for eutrophication to drive new stressors is a growing concern. To address these knowledge gaps, I investigated how human stressors impact two different and major coastal ecosystems known to be vulnerable to anthropogenic disturbances.

In chapter 1, I demonstrate that anthropogenic stressors in the form of increased nutrients in the water and sediments have strong impacts on interspecific interactions of coral reef macroalgae. Abiotic stressors such as nutrients have been linked to phase-shifts from coral to algal domination on tropical reefs. However, few studies have considered how these stressors impact changes in the biotic and abiotic constituents of dominant species of calcifying macroalgae, and how this may be mediated by species-species interactions. I conducted 4 mesocosm experiments to examine whether different nutrient sources (water column vs. terrestrial sediment) as well as species interactions (alone vs. mixed species) affected total mass (biomass + calcium carbonate (CaCO3)) of two common calcifying macroalgae (Padina boryana and Galaxaura fasciculata). P. boryana gained total mass with increased water column nutrients but declined with increased nutrients supplied by the sediment. Conversely, G. fasciculata gained total mass with increased nutrients in the sediment but declined with increased water column nutrients. In both interactions, the “winner” (i.e., G. fasciculata in the sediment experiment) also had a greater % of thallus mass comprised of CaCO3, potentially due to the subsequent decomposition of the “loser” as this result was not found in the alone treatments. These findings ultimately suggest that nutrient stressors can cause cascading effects, such as promoting calcification and biomass growth or loss in these macroalgal communities, and the potential for domination or decline is based on the nutrient source and community composition.

In chapter 2, I demonstrate that decomposition of macroalgal blooms cause a sequence of biogeochemical processes that can drive acidification in shallow coastal estuaries, and that these processes are mediated by a dynamic microbial community. Eutrophication and ocean acidification are both widely acknowledged as major human-induced stressors in marine environments. While the link between eutrophication and acidification has been established for phytoplankton, it is unclear whether eutrophication in the form of macroalgal blooms can cause cascading effects like acidification in shallow eutrophic estuaries. I conducted seasonal field surveys and assessed microbial communities and functional genes to evaluate changes in biotic and abiotic characteristics between seasons that may be associated with acidification in Upper Newport Bay, CA, USA. Acidification, measured as a drop in pH of 0.7, occurred in summer at the site with the most macroalgal cover. Microbial community composition and functional gene expression provide evidence that decomposition processes contributed to acidification, and also suggest that other biogeochemical processes like nitrification and degradation of polyphosphate also contributed to acidification. To my knowledge, my findings represent the first field evidence that eutrophication of shallow coastal estuaries dominated by green macroalgal blooms can cascade to acidification.

In chapter 3, I demonstrate that macroalgal blooms in shallow estuaries are strong drivers of key microbially-mediated biogeochemical processes that can cause cascading effects, such as acidification and nutrient fluxing, regardless of simulated tidal flushing. Estuaries are productive and diverse ecosystems and are vulnerable to eutrophication from increased anthropogenic nutrients. While it is known that enhanced tidal flushing can reduce adverse effects of anthropogenic disturbances in larger, deeper estuarine ecosystems, this is unexplored for eutrophication in shallow coastal estuaries where macroalgae usually dominate. I simulated eutrophication as a macroalgal bloom in a mesocosm experiment, varied tidal flushing (flushed daily vs unflushed), and assessed the effects on water column and sediment biogeochemical processes and the sediment microbial community. While flushing did not ameliorate the negative effects of the macroalgal bloom, it caused transient differences in the rate of change in biogeochemical processes and promoted increased fluxes of nutrients from the sediment. In the beginning, the macroalgal bloom induced basification and increased total alkalinity, but during decomposition, acidification and the accumulation of nutrients in the sediment and water column occurred. The findings from this chapter ultimately suggest that macroalgal blooms have the potential to be the cause of, yet may also offer a partial solution to, global ecological changes to biogeochemical processes.

Overall, my results indicate that anthropogenic disturbances, particularly in the form of increased nutrients, can cause cascading effects like macroalgal blooms that in turn cause acidification, basification, increased interspecific interactions, nutrient depletion, and nutrient fluxing in multiple ecosystems. These data advance our current understanding of the ecological consequences of eutrophication in the form of macroalgal blooms in different ecosystems. It also provides mechanistic links to microbial communities and biogeochemical processes not previously identified for shallow coastal estuaries. As human population and subsequent nutrient pollution increases in watersheds globally, ecological phenomenon such as eutrophication will only be intensified, and macroalgal communities will continue to dominate. Consequently, this dominance, especially during decomposition as shown here, can drive a multitude of subsequent stressors that can impact the entire ecosystem.

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