Impacts of Macrobenthos on the Rates and Pathways of Organic Matter Mineralization in Two Coastal Marine Ecosystems of the Southeastern United States

Coastal ecosystems are among the most productive in the world, and they serve as an invaluable resource to society. Despite many decades of biogeochemical research in the coastal zone, carbon and nutrient budgets remain uncertain largely due to the inherent complexity and spatiotemporal variability observed in coastal ecosystems. This dissertation addresses the rates, pathways, and microorganisms responsible for organic-matter mineralization and nutrient release in the sediments of coastal marine ecosystems. In particular, the research herein focuses on the role of macrobenthos and spatial/ temporal variability in impacting organic matter and nutrient cycles in such ecosystems. The common theme throughout the dissertation research was to combine ecology with biogeochemistry to explore the impacts of benthic organisms in the macroscale on microbial processes that mediate organic matter mineralization and nutrient release over the microscale. Sulfate-reducing prokaryotes (SRP) play a key role in carbon and nutrient cycles of coastal marine, vegetated ecosystems, but interactions of SRP communities with aquatic plants remain little studied. In the subtidal zone of Santa Rosa Sound, Florida, SRP abundance, activity, and community composition were studied in relation to sediment geochemical gradients and plant growth state in a Thalassia testudinum seagrass bed and in adjacent unvegetated areas (Chapter 1). The community composition of SRP was determined using restriction fragment length polymorphism (RFLP) screening and amino acid sequence comparisons inferred from partial dissimilatory bisulfite reductase (dsrA and B) genes that were PCR-amplified and cloned from DNA extracted from sediment samples. Our results indicate that seagrass growth state affects the abundance and activity of SRP, while SRP community composition remains relatively stable across the environmental parameters tested. Sequence data from this study may be used to direct future cultivation efforts and to design new genetic probes for sulfate-reducers in seagrass sediments. The remaining dissertation research focused on a second coastal marine ecosystem, the saltmarsh, on Skidaway Island near Savannah, Georgia. The Georgia saltmarsh contrasts with seagrass beds from the west coast of Florida in that it exists in the intertidal zone, contains a large tidal range of 2-3 m, and the sediments are exposed to extensive burrowing and feeding activities by macrofauna. In addition, larger seasonal change may be observed in the Georgia marsh because it is intertidal and exposed to slightly larger annual temperature extremes. In chapter two, extensive biogeochemical field characterization was combined with state-of-the-art diagenetic modeling to elucidate feedbacks between macrobenthic organisms (macrophyte plants, bioturbating macrofauna) and the controls of organic matter mineralization in saltmarsh sediments. A multicomponent, inverse model was used to support the field work by quantifying properties and processes that in some cases could not be experimentally determined. Modeled rates of organic matter diagenesis were determined by attempting to find the best agreement with measured profiles of major redox species. Results indicated that sulfate reduction is the dominant degradation pathway for sites with less bioturbation, while iron reduction outcompeted sulfate reduction where intense bioturbation activity caused the rapid recycling of Fe(III)-oxyhydroxides. These results were fairly consistent across seasons, however, the magnitude of degradation rates decreased dramatically in the winter, and microbial sulfate reduction was more greatly affected by changes in temperature than microbial iron reduction. The objective of the third and final study was to scale up biogeochemical measurements over an entire ecosystem (saltmarsh basin) in order to address spatial variability that has confounded estimates of organic matter and nutrient mineralization at the whole ecosystem level. A 100,000 m2 area of Georgia marsh was mapped using a combination of aerial photography, Geographic Information Systems (GIS), and localized identification of plant types. Major habitats were delineated according to the predominant vegetation, including the short form of Spartina alterniflora (SS), the tall form of S. alterniflora (TS) and unvegetated creekbank (CB). Spatial variability was addressed across all major habitats with a statistically-sound experimental design to carry out determinations of porewater and solid-phase geochemistry, sulfate reduction rates (SRR), bacterial abundances, macrofaunal burrow size/density, plant stem height/density, and above/belowground plant biomass. Habitat type had a large influence on the rates and pathways of carbon oxidation. Consideration of spatial variability revealed that overall carbon oxidation rates in saltmarsh ecosystems may be higher than previously thought. Surprisingly, microbial Fe(III) reduction (and not sulfate reduction) was observed to be the predominant terminal-electron-accepting process coupled to carbon oxidation for the majority of the marsh basin studied. Together with the observation that most of the Georgia marsh studied was not sulfidic, results indicate that our perceptions of the redox poise, and the impacts of redox poise on biogeochemical cycles, need to be revised for marsh ecosystems taking into account spatial variability driven by macrobenthic activities. Typically, coastal sediments rapidly become anaerobic just below the sediment surface, and the flux of oxidants into sediments is limited. Under these conditions, anaerobic bacteria are responsible for the majority of organic matter remineralization. Increased solute and particle transport via macroorganismal activities (bioturbation, bioirrigation, and phytoirrigation) aids in mixing reactants throughout sediments, thereby encouraging microbial activities, and increasing organic matter remineralization rates. The following research employed an array of new and diverse multidisciplinary approaches from molecular biological techniques and GIS mapping to state-of-the-art diagenetic modeling in order to elucidate the impacts of macrobenthos on carbon and nutrient cycles mediated by anaerobic microorganisms in coastal marine ecosystems. In all three studies, geochemical parameters indicated that bacterial activities were stimulated in vegetated sediments, while saltmarsh studies revealed that macrofaunal burrows strongly influenced the pathways of terminal electron acceptor (TEA) usage. The uncertainty of current estimates of carbon and nitrogen cycling in saltmarsh habitats indicates the need for a more comprehensive approach to address the spatial variability that exists in these habitats. From the research reported in this dissertation, it is clear that macrobenthos have a profound impact on the rates and pathways of organic matter mineralization and that the resulting spatial variability in sediment biogeochemical cycles must be incorporated into future studies that attempt to determine elemental budgets in coastal marine ecosystems.