Flow as a Mediator of Ecosystem Engineering: Hydrodynamics Shape Chemical Modification by Kelp and Mussel Beds

Abstract

Ecosystem engineers are organisms that modify their physical and chemical surroundings in ways that shape the structure and function of ecological communities. Physically, they build biogenic structures that modify flow, light, and habitat complexity. Chemically, they change oxygen and pH levels through metabolic processes such as photosynthesis and respiration. These modifications can either facilitate the presence of associated species by creating favorable microhabitats or inhibit them by amplifying environmental stress. Understanding the circumstances under which and how these shifts occur has become increasingly important as climate change intensifies environmental variability in coastal ecosystems. Advancing our understanding of how ecosystem engineers shape their communities requires considering how external factors, particularly flow, mediate their influence on the surrounding environment. Driven by tides, waves, and currents, flow regulates water residence time and thus the accumulation or dispersion of biologically modified water. Yet despite its central importance, the role of flow in controlling the strength and direction of ecosystem engineering remains poorly understood.This dissertation examines how local hydrodynamics influences the capacity of marine ecosystem engineers to modify their surrounding chemical environments. It focuses on two contrasting but complementary systems: an autotroph, bull kelp (Nereocystis luetkeana), and a heterotroph, mussels (Mytilus spp.). Looking across these systems provides a broader view of how different types of engineers—those that produce oxygen through photosynthesis and those that consume it through respiration—shape their local chemical environments. By studying both systems, this work links two aspects of ecosystem engineering: 1) oxygen production and depletion, and 2) explores how flow determines when these species have the potential to act as facilitators or inhibitors within their communities. I combined field observations with laboratory and field experiments to explore how flow dynamics interact with biological traits, such as canopy structure, density, and behavior, to determine when these engineers act as facilitators or inhibitors within their communities. Across chapters, the work progresses from identifying environmental controls on kelp-driven chemical modification (Chapter 1) to isolating mechanistic feedbacks between flow, mussel behavior, and chemistry (Chapter 2), and then investigating density effects on chemistry and behavior by out-planting manipulated mussel aggregations in natural conditions (Chapter 3). Chapter 1 addresses a fundamental gap in understanding how hydrodynamic variability constrains the ability of kelp forests to alter seawater chemistry. Using high-frequency, long-term measurements of flow, light, dissolved oxygen (DO), and pH, this chapter quantifies how diel and tidal cycles interact to control the timing, magnitude, and spatial pattern of kelp-driven chemical change within a tidally dominated bull kelp forest in the Salish Sea. The results show that kelp effects on local seawater chemistry are not static “hotspots” but dynamic, flow-dependent features that shift predictably across space and time. Kelp-driven increases in DO occur primarily during daytime slack tides, when reduced flow allows oxygen-enriched water to remain within the canopy before being rapidly replaced by the next tidal exchange. These findings demonstrate that even in a highly productive kelp forest, strong and variable tidal currents limit the persistence of chemical modification to only a few hours per tidal cycle. As a result, the capacity for kelp forests to function as chemical refugia depends less on their metabolic potential and more on the hydrodynamic context that influences water retention and exchange. By explicitly linking diel and tidal processes, this chapter reframes kelp-driven buffering from a static to a dynamic process and provides a framework for predicting when and where macrophyte canopies can locally ameliorate chemical stress. Chapter 2 builds on this framework by examining how flow and organismal behavior mediate chemical modification in a heterotrophic engineer, the mussel. Valve gaping in mussels regulates the flow generated by their pumping activity, which drives water exchange between the ambient environment and the interstitial spaces within aggregations. This chapter presents an experimental approach that couples behavioral measurements from high-frequency gape sensors with real-time oxygen data to evaluate how valve activity and flow together shape interstitial water chemistry across three Mytilus species. Two consistent patterns emerged: oxygen depletion within mussel beds decreased exponentially with increasing flow speed, and gaping behavior remained largely static across flow and low-oxygen conditions. The absence of compensatory gaping under low-flow conditions indicates limited behavioral feedbacks between gaping, chemistry, and flow, underscoring the dominant role of physical flow in driving oxygen dynamics within mussel aggregations. Variation in oxygen depletion among species was best explained by differences in biomass density, suggesting that morphometric traits, rather than behavior, primarily govern their capacity for chemical modification. These findings refine our understanding of ecosystem engineering by identifying the conditions under which structural and hydrodynamic factors outweigh behavioral influences. Chapter 3 builds on insights from Chapter 2 by extending the work into the field, where mussel aggregations experience natural tidal flow and greater variation in density. The first goal was to determine whether higher mussel densities lead to stronger oxygen depletion under natural flow conditions. A second goal was to test whether the relationship between flow speed and dissolved oxygen follows the same exponential pattern observed in the steady-flow flume (Chapter 2), and whether mussel gaping remains insensitive to flow and oxygen variation across different aggregation positions in a more dynamic environment. The field experiment showed that oxygen concentrations declined sharply with increasing aggregation density, with the highest-density aggregations exhibiting the lowest mean DO levels, the largest diel fluctuations, and frequent short-lived hypoxic events. Gaping behavior varied with density and position within an aggregation, as interior mussels gaped wider and spent more time open than edge mussels, but showed little response to short-term changes in flow or oxygen availability. These results demonstrate that structural traits of an aggregation, such as density, amplify chemical modification, while flow regulates its magnitude and persistence. Moreover, there was no evidence that behavior provides any buffering capacity once physical exchange is constrained. Across systems, this dissertation highlights a unifying principle: the capacity of marine engineers to alter their environment depends primarily on how their biological traits, such as metabolism, structure, and abundance, interact with hydrodynamic forces. By quantifying how flow controls oxygen variability across autotrophic and heterotrophic systems, this work advances a better understanding of when and where ecosystem engineers function as facilitators or inhibitors, emphasizing the central role of local physical dynamics in shaping their ecological influence.