Constraining natural and anthropogenic disturbances in the delivery of coastal ecosystem services

Coastal ecosystems provide key services that benefit human wellbeing yet are undergoing rapid degradation due to natural and anthropogenic pressures. This thesis seeks to understand how disturbances impact salt marsh and estuarine ecosystem functioning in order to refine their role in coastal ecosystem service delivery and predict future resilience. Salt marsh survival relative to sealevel rise increasingly relies on the accumulation and preservation of soil organic carbon (SOC). Firstly, I characterized SOC development and turnover in a New England salt marsh and found that salt marsh soils typically store marsh grass-derived compounds that are reworked over centuries-to-millennia. Next, I assessed how two common marsh disturbances – natural ponding and anthropogenic mosquito ditching – affect salt marsh carbon cycling and storage. Salt marsh ponds deepen through soil erosion and decomposition of long-buried marsh peat. Further, the SOC lost during pond development is not fully recouped once drained ponds are revegetated and virtually indistinguishable from the surrounding marsh. Mosquito ditches, which were installed in ~ 90% of New England salt marshes during the Great Depression, did not significantly alter marsh carbon storage. In Buzzards Bay, Massachusetts, a US National Estuary, we tested relationships among measures of estuarine water quality, recreational activity, and local socioeconomic conditions to understand how the benefits of cultural ecosystem services are affected by shifts in water quality associated with global change and anthropogenic activity. Over a 24-year period, water quality degradation coinciding with increases in Chlorophyll a is associated with declines in fishery abundance and cultural ecosystem service values ($0.08 – 0.67 million USD). In combination, incorporation of both anthropogenic and natural disturbances to coastal ecosystem functioning and service delivery can produce improved estimates of ecosystem service valuation for effective resource decision-making under future climate scenarios.

Biotransformation and oxidative stress responses in fish (Astyanax aeneus) inhabiting a Caribbean estuary contaminated with pesticide residues from agricultural runoff

The estuarine ecosystem of Laguna Madre de Dios (LMD), in the Caribbean coast of Costa Rica, is exposed to contamination with pesticide residues coming from the upstream agricultural areas. Biomarkers can provide a better indication of the fitness of biota in real mixture exposure scenarios than traditional lethal dose toxicity measurements. Here, we measured biomarkers of biotransformation, oxidative stress and neurotoxicity on Astyanax aeneus, an abundant fish species in LMD. Glutathione S-transferase activity (GST), catalase activity (CAT), lipid peroxidation (LPO), and cholinesterase activity (ChE) were measured in fish collected during seven sampling campaigns, carried out between 2016 and 2018. Pesticide residues were analysed in surface water samples collected every time fish were sampled. Residues of 25 pesticides, including fungicides, insecticides and herbicides, were detected. The biomarkers measured in A. aeneus varied along the sampling moments, however, biotransformation and oxidative stress signals showed coupled responses throughout the assessment. Furthermore, significant correlations were established between three biomarkers (GST, LPO and CAT) and individual pesticides, as well as between GST and LPO with groups of pesticides with shared biocide action. Among pesticides, insecticide residues had a major influence on the responses observed in fish. This work shows that the frequent exposure to environmentally relevant concentrations of pesticides can be related to physiological responses in fish that affect their health. This early warning information should be considered to improve the protection of estuarine ecosystems in the tropics.

Prior exposure to weathered oil influences foraging of an ecologically important saltmarsh resident fish

Estuarine ecosystem balance typically relies on strong food web interconnectedness dependent on a relatively low number of resident taxa, presenting a potential ecological vulnerability to extreme ecosystem disturbances. Following the Deepwater Horizon (DwH) oil spill disaster of the northern Gulf of Mexico (USA), numerous ecotoxicological studies showed severe species-level impacts of oil exposure on estuarine fish and invertebrates, yet post-spill surveys found little evidence for severe impacts to coastal populations, communities, or food webs. The acknowledgement that several confounding factors may have limited researchers’ abilities to detect negative ecosystem-level impacts following the DwH spill drives the need for direct testing of weathered oil exposure effects on estuarine residents with high trophic connectivity. Here, we describe an experiment that examined the influence of previous exposure to four weathered oil concentrations (control: 0.0 L oil m−2; low: 0.1 L oil m−2; moderate: 0.5–1 L oil m−2; high: 3.0 L oil m−2) on foraging rates of the ecologically important Gulf killifish (Fundulus grandis). Following exposure in oiled saltmarsh mesocosms, killifish were allowed to forage on grass shrimp (Palaeomonetes pugio) for up to 21 h. We found that previous exposure to the high oil treatment reduced killifish foraging rate by ~37% on average, compared with no oil control treatment. Previous exposure to the moderate oil treatment showed highly variable foraging rate responses, while low exposure treatment was similar to unexposed responses. Declining foraging rate responses to previous high weathered oil exposure suggests potential oil spill influence on energy transfer between saltmarsh and off-marsh systems. Additionally, foraging rate variability at the moderate level highlights the large degree of intraspecific variability for this sublethal response and indicates this concentration represents a potential threshold of oil exposure influence on killifish foraging. We also found that consumption of gravid vs non-gravid shrimp was not independent of prior oil exposure concentration, as high oil exposure treatment killifish consumed ~3× more gravid shrimp than expected. Our study findings highlight the sublethal effects of prior oil exposure on foraging abilities of ecologically valuable Gulf killifish at realistic oil exposure levels, suggesting that important trophic transfers of energy to off-marsh systems may have been impacted, at least in the short-term, by shoreline oiling at highly localized scales. This study provides support for further experimental testing of oil exposure effects on sublethal behavioral impacts of ecologically important estuarine species, due to the likelihood that some ecological ramifications of DwH on saltmarshes likely went undetected.

Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay

Background Annually reoccurring microbial populations with strong spatial and temporal variations have been identified in estuarine environments, especially in those with long residence time such as the Chesapeake Bay (CB). However, it is unclear how microbial taxa cooccurr and how the inter-taxa networks respond to the strong environmental gradients in the estuaries. Results Here, we constructed co-occurrence networks on prokaryotic microbial communities in the CB, which included seasonal samples from seven spatial stations along the salinity gradients for three consecutive years. Our results showed that spatiotemporal variations of planktonic microbiomes promoted differentiations of the characteristics and stability of prokaryotic microbial networks in the CB estuary. Prokaryotic microbial networks exhibited a clear seasonal pattern where microbes were more closely connected during warm season compared to the associations during cold season. In addition, microbial networks were more stable in the lower Bay (ocean side) than those in the upper Bay (freshwater side). Multivariate regression tree (MRT) analysis and piecewise structural equation modeling (SEM) indicated that temperature, salinity and total suspended substances along with nutrient availability, particulate carbon and Chl a, affected the distribution and co-occurrence of microbial groups, such as Actinobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, Proteobacteria, and Verrucomicrobia. Interestingly, compared to the abundant groups (such as SAR11, Saprospiraceae and Actinomarinaceae), the rare taxa including OM60 (NOR5) clade (Gammaproteobacteria), Micrococcales (Actinobacteria), and NS11-12 marine group (Bacteroidetes) contributed greatly to the stability of microbial co-occurrence in the Bay. Modularity and cluster structures of microbial networks varied spatiotemporally, which provided valuable insights into the ‘small world’ (a group of more interconnected species), network stability, and habitat partitioning/preferences. Conclusion Our results shed light on how estuarine gradients alter the spatiotemporal variations of prokaryotic microbial networks in the estuarine ecosystem, as well as their adaptability to environmental disturbances and co-occurrence network complexity and stability.

High-Resolution Spatiotemporal Dynamics of Harmful Algae in the Indian River Lagoon (Florida)—A Case Study of Aureoumbra lagunensis, Pyrodinium bahamense, and Pseudo-nitzschia

The Indian River Lagoon (IRL), located on the east coast of Florida, is a complex estuarine ecosystem that is negatively affected by recurring harmful algal blooms (HABs) from distinct taxonomic/functional groups. Enhanced monitoring was established to facilitate rapid quantification of three recurrent bloom taxa, Aureoumbra lagunensis, Pyrodinium bahamense, and Pseudo-nitzschia spp., and included corroborating techniques to improve the identification of small-celled nanoplankton (<10 μm in diameter). Identification and enumeration of these target taxa were conducted during 2015–2020 using a combination of light microscopy and species-specific approaches, specifically immunofluorescence flow cytometry as well as a newly developed qPCR assay for A. lagunensis presented here for the first time. An annual bloom index (ABI) was established for each taxon based on occurrence and abundance data. Blooms of A. lagunensis (>2 × 108 cells L–1) were observed in all 6 years sampled and across multiple seasons. In contrast, abundance of P. bahamense, largely driven by the annual temperature cycle that moderates life cycle transitions and growth, displayed a strong seasonal pattern with blooms (105–107 cells L–1) generally developing in early summer and subsiding in autumn. However, P. bahamense bloom development was delayed and abundance was significantly lower in years and locations with sustained A. lagunensis blooms. Pseudo-nitzschia spp. were broadly distributed with sporadic bloom concentrations (reaching 107 cells L–1), but with minimal concentrations of the toxin domoic acid detected (<0.02 μg L–1). In summer 2020, multiple monitoring tools characterized a novel nano-cyanobacterium bloom (reaching 109 cells L–1) that coincided with a decline in A. lagunensis and persisted into autumn. Statistical and time-series analyses of this spatiotemporally intensive dataset highlight prominent patterns in variability for some taxa, but also identify challenges of characterizing mechanisms underlying more episodic yet persistent events. Nevertheless, the intersect of temperature and salinity as environmental proxies proved to be informative in delineating niche partitioning, not only in the case of taxa with long-standing data sets but also for seemingly unprecedented blooms of novel nanoplanktonic taxa.

Estuarine Gradients Dictate Spatiotemporal Variations of Microbiome Networks in the Chesapeake Bay

Background: Annually reoccurring microbial populations with strong spatial and temporal variations have been identified in estuarine environments, especially in those with long residence time such as the Chesapeake Bay (CB). However, it is unclear how microbial taxa cooccurrence with each other and how the inter-taxa networks respond to the strong environmental gradients in the estuaries. Results: Here, we constructed co-occurrence networks on prokaryotic microbial communities in the CB, which included seasonal samples from seven spatial stations along the salinity gradients for three consecutive years. Our results showed that spatiotemporal variations of planktonic microbiomes promoted differentiations of the characteristics and stability of prokaryotic microbial networks in the CB estuary. Prokaryotic microbial networks exhibited a clear seasonal pattern where microbes were more closely connected during warm season compared to the associations during cold season. In addition, microbial networks were more stable in the lower Bay (ocean side) than those in the upper Bay (freshwater side). Multivariate regression tree (MRT) analysis and piecewise structural equation modeling (SEM) indicated that temperature, salinity and total suspended substances along with nutrient availability, particulate carbon and Chl a, affected the distribution and co-occurrence of microbial groups, such as Actinobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, Proteobacteria, and Verrucomicrobia. Interestingly, compared to the abundant groups (such as SAR11, Saprospiraceae and Actinomarinaceae), the rare taxa including OM60(NOR5) clade (Gammaproteobacteria), Micrococcales (Actinobacteria), and NS11-12 marine group (Bacteroidetes) contributed greatly to the stability of microbial co-occurrence in the Bay. Modularity and cluster structures of microbial networks varied spatiotemporally, which provided valuable insights into the ‘small world’ (a group of more interconnected species), network stability, and habitat partitioning/preferences.Conclusion: Our results shed light on how estuarine gradients alter the spatiotemporal variations of prokaryotic microbial networks in the estuarine ecosystem, as well as their adaptability to environmental disturbances and co-occurrence network complexity and stability.

Unraveling the impacts of meteorological and anthropogenic changes on sediment fluxes along an estuary-sea continuum

Sediment fluxes at the estuary-sea interface strongly impact particle matter exchanges between marine and continental sources along the land-sea continuum. However, human activities drive pressures on estuary physical functioning, hence threatening estuarine habitats and their ecosystem services. This study explores a 22-year numerical hindcast of the macrotidal Seine Estuary (France), experiencing contrasted meteorological conditions and anthropogenic changes (i.e., estuary deepening and narrowing). The hindcast was thoroughly validated for both water column and sediment bed dynamics and showed good capacities to simulate annual sediment budgets observed from 1990 to 2015. We aim at disentangling the relative contributions of meteorological and human-induced morphological changes on net sediment fluxes between the estuary and its adjacent coastal sea. Our results highlight that intense wave events induce fine sediment (≤ 100 µm) export to the sea but coarser sediment (≥ 210 µm) import within the estuary. Although intense river discharges induce mud export to the sea, moderate to large river discharges prove to support mud import within the estuary. Wave and river discharge events were less intense in 2005–2015 than in 1990–2000, reducing fine sediment export to the sea. The estuary deepening and narrowing due to human activities increased fine sediment import within the estuary, shifting the estuary from an exporting to importing system. We propose a conceptualization of mud flux response to river discharge and wave forcing, as well as anthropogenic pressures. It provides valuable insights into particle transfers along the land-sea continuum, contributing to a better understanding of estuarine ecosystem trajectories under global changes.