Biogeochemical and Hydrological Drivers of Heterogeneous Nutrient Exports From Subterranean Estuaries

Submarine groundwater discharge (SGD) to coastal zones contributes terrestrial freshwater and nutrients that may support harmful algal blooms (HABs). The magnitude of nutrient exports via SGD depends on volumes of fresh groundwater discharge, its chemical composition, and modifications by biogeochemical processing within subterranean estuaries. Thus, the ability to upscale SGD exports requires knowing the range of chemical composition of inland groundwater and how those compositions may be transformed as fresh and saltwater mix within subterranean estuaries. These processes may create heterogeneous magnitudes of solute exports, even at small spatial scales, and such heterogeneities have rarely been assessed for regional or global SGD nutrient export estimates. To evaluate heterogeneity in subterranean estuary processes and nutrient export, we collected seasonal pore water samples in 2015–2016 at three proximal (<20 km) subterranean estuary sites in Indian River Lagoon, FL. Sites have homogenous hydrogeological settings, but differ in land use and coastal features, and include a mangrove site, an urban site, and a site offshore of a natural wetland. All sites exhibit little variation through time in nutrient concentrations and modeled SGD rates. In contrast, each site exhibits significantly different nutrient concentrations of potential fresh groundwater sources, fresh groundwater discharge volumes, and nutrient transformations within subterranean estuaries. Groundwater specific discharge correlates with nutrient concentrations, suggesting that higher residence times in the subterranean estuary increase biogeochemical transformations that reduce anthropogenic nutrient loads but increase in situ nutrient sources derived from organic matter remineralization. The differences in transformations lead to SGD nutrient contributions that differ by orders of magnitude between sites and have N:P ratios that are greater than the Redfield ratio (15) for the mangrove (29) and urban sites (28), but less than the Redfield ratio for the wetland site (8). These results indicate that heterogeneity of both absolute and relative nutrient export via SGD complicates integration of nutrient fluxes across regional coastal zones and evaluations of its impacts to coastal ecosystems. A better understanding of the drivers of heterogeneity, including subterranean estuary processes, land use, coastal topography, and vegetation dynamics could improve assessments of regional nutrient loading and upscaling for estimates of global solute cycles.

A State-Of-The-Art Perspective on the Characterization of Subterranean Estuaries at the Regional Scale

Subterranean estuaries the, subsurface mixing zones of terrestrial groundwater and seawater, substantially influence solute fluxes to the oceans. Solutes brought by groundwater from land and solutes brought from the sea can undergo biogeochemical reactions. These are often mediated by microbes and controlled by reactions with coastal sediments, and determine the composition of fluids discharging from STEs (i.e., submarine groundwater discharge), which may have consequences showing in coastal ecosystems. While at the local scale (meters), processes have been intensively studied, the impact of subterranean estuary processes on solute fluxes to the coastal ocean remains poorly constrained at the regional scale (kilometers). In the present communication, we review the processes that occur in STEs, focusing mainly on fluid flow and biogeochemical transformations of nitrogen, phosphorus, carbon, sulfur and trace metals. We highlight the spatio-temporal dynamics and measurable manifestations of those processes. The objective of this contribution is to provide a perspective on how tracer studies, geophysical methods, remote sensing and hydrogeological modeling could exploit such manifestations to estimate the regional-scale impact of processes in STEs on solute fluxes to the coastal ocean.

Changes in Organic Matter Deposition Can Impact Benthic Marine Meiofauna in Karst Subterranean Estuaries

Subsurface mixing of seawater and terrestrial-borne meteoric waters on carbonate landscapes creates karst subterranean estuaries, an area of the coastal aquifer with poorly understood carbon cycling, ecosystem functioning, and impact on submarine groundwater discharge. Caves in karst platforms facilitate water and material exchange between the marine and terrestrial environments, and their internal sedimentation patterns document long-term environmental change. Sediment records from a flooded coastal cave in Cozumel Island (Mexico) document decreasing terrestrial organic matter (OM) deposition within the karst subterranean estuary over the last ∼1,000 years, with older sediment likely exported out of the cave by intense storm events. While stable carbon isotopic values (δ13Corg ranging from −22.5 to −27.1‰) and C:N ratios (ranging from 9.9 to 18.9) indicate that mangrove and other terrestrial detritus surrounding an inland sinkhole are the primarily sedimentary OM supply, an upcore decrease in bulk OM and enrichment of δ13Corg values are observed. These patterns suggest that a reduction in the local mangrove habitat decreased the terrestrial particulate OM input to the cave over time. The benthic foraminiferal community in basal core sediment have higher proportions of infaunal taxa (i.e., Bolivina) and Ammonia, and assemblages shift to increased miliolids and less infaunal taxa at the core-top sediment. The combined results suggest that a decrease in terrestrial OM through time had a concomitant impact on benthic meiofaunal habitats, potentially by impacting dissolved oxygen availability at the microhabitat scale or resource partitioning by foraminifera. The evidence presented here indicates that landscape and watershed level changes can impact ecosystem functioning within adjacent subterranean estuaries.

Saltwater Intrusion and Submarine Groundwater Discharge: Acceleration of Biogeochemical Reactions in Changing Coastal Aquifers

Intrusion of saltwater into freshwater coastal aquifers poisons an essential resource. Such intrusions are occurring along coastlines worldwide due largely to the over-pumping of freshwater and sea level rise. Saltwater intrusion impacts drinking water, agriculture and industry, and causes profound changes in the biogeochemistry of the affected aquifers, the dynamic systems called subterranean estuaries. Subterranean estuaries receive freshwater from land and saltwater from the ocean and expose this fluid mixture to intense biogeochemical dynamics as it interacts with the aquifer and aquiclude solids. Increased saltwater intrusion alters the ionic strength and oxidative capacity of these systems, resulting in elevated concentrations of certain chemical species in the groundwater, which flows from subterranean estuaries into the ocean as submarine groundwater discharge (SGD). These highly altered fluids are enriched in nutrients, carbon, trace gases, sulfide, metals, and radionuclides. Seawater intrusion expands the subterranean estuary. Climate change amplifies sea level variations on short and seasonal time scales. These changes may result in higher SGD fluxes, further accelerating release of nutrients and thus promoting biological productivity in nutrient-depleted waters. But this process may also adversely affect the environment and alter the local ecology. Research on saltwater intrusion and SGD has largely been undertaken by different groups. We demonstrate that these two processes are linked in ways that neither group has articulated effectively to date.

Habitat Partitioning in the Marine Sector of Karst Subterranean Estuaries and Bermuda's Marine Caves: Benthic Foraminiferal Evidence

Karst subterranean estuaries (KSEs) are created from the two- and three-way mixing of saline groundwater, rain, and oceanic water in the subsurface on carbonate landscapes, and this hydrographic framework promotes unique physical processes, biogeochemical cycling, and biological communities. Here we provide evidence that the source and quantity of particulate organic matter (POM) that is delivered to the benthos strongly correlates to benthic habitat partitioning in the oxygenated marine sectors of KSEs. A dataset of benthic foraminifera at 128 different locations from several large flooded cave systems in Bermuda were compiled and evaluated against common environmental characteristics (e.g., tidal exposure, substrate particle size, bulk organic matter, C:N, total organic carbon, and δ13Corg). Benthic areas receiving more carbon isotopically depleted organic matter sources (mean δ13Corg values < −23.2‰, C:N ratios >11), most likely from the terrestrial surface and some marine plankton, were dominated by Trochammina inflata, Bolivina spp., and Helenina anderseni. In contrast, benthic areas receiving more carbon isotopically enriched organic matter sources (mean δ13Corg values > −21.6‰, C:N ratios <10), most likely from marine plankton transported through marine cave openings cave from adjacent coastal waters, were dominated by Spirophthalmidium emaciatum, Spirillina vivipara, Patellina corrugata, and Rotaliella arctica. The benthic foraminifera most distal from any cave entrances were dominated by taxa also known from the deep-sea (e.g., Rotaliella, Spirophthalmidium) in sediment with the lowest bulk organic matter content (mean: 6%), or taxa that prefer hard substrates and are potentially living attached to cave walls (Patellina, Spirillina). While physical groundwater characteristics (e.g., salinity, dissolved oxygen) are expected drivers of benthic ecosystems in KSEs, these results suggest that POM source, quantity, and delivery mechanisms (e.g., groundwater-seawater circulation mechanisms, terrestrial flux) play an important role in benthic habitat partitioning and the spatial variability of biogeochemical cycles in the oxygenated marine sector of KSEs.

Modern methane and dissolved organic matter radiocarbon signatures suggest rapid transfer of organic carbon from a tropical forest to the underlying subterranean estuary ecosystem

<p>Biogeochemical processing of dissolved organic matter, including methane, along sharp salinity gradients in subterranean estuaries greatly alters the composition of submarine groundwater discharge into the marine environment. Along the margins of coastal carbonate (karst) platforms, which account for ~25% of all coastlines, subterranean estuaries extend kilometers inland within porous bedrock, flooding extensive cave networks. This environment harbors a poorly understood, but globally dispersed, anchialine fauna (invertebrates with subterranean adaptations) and characteristic microbial communities. In Mexico’s Yucatan Peninsula, microbial processing of methane and dissolved organic carbon (DOC), originating from overlying tropical soils, is the critical link for shuttling organic matter to higher trophic levels of the food web within the coastal aquifer. To better understand carbon turnover during organic matter transformations in this habitat, we collected samples for stable and radiocarbon analyses targeting the biotic and abiotic components of the carbon cycle. In the freshwater, radiocarbon signatures of terrestrially originated DOC (pMC = 105.1; [DOC] = 517 µM; δ<sup>13</sup>C = ˗27.8 ‰) and methane (pMC = 101.6; [CH<sub>4</sub>] = 6460 nM; δ<sup>13</sup>C = ˗71.5 ‰) correspond with modern <sup>14</sup>C ages, suggesting these sources of energy within the habitat are comprised of modern carbon fixed recently by photosynthesizing primary producers at the land surface. By contrast, DOC in the deeper saline groundwater is significantly lower in concentration (21 µM), and substantially older (pMC = 47.3, equates to 6010 ± 95 <sup>14</sup>C yrs). Similarly, dissolved inorganic carbon (DIC) in the freshwater is significantly younger (pMC = 86.5, equates to 1170 ± 15 <sup>14</sup>C yrs) than in the deeper saline water (pMC = 58.4, equates to 4320 ± 25 <sup>14</sup>C yrs). These findings demonstrate that important sources of nutrition for the food web are intimately linked to the overlying subaerial habitat, which suggests these ecosystems are highly vulnerable to nearby land use alterations. Furthermore, this study provides new insights into carbon turnover during the process of methane production/consumption, carbon exchange, and organic matter transformation before the emission of the dissolved constituents into coastal oceans from karst subterranean estuaries. Radiocarbon and stable isotopic analyses of the resident fauna will allow us to evaluate the ecological effects of the rapid top-down transfer mechanism for methane and DOC. Beyond better understanding the sources and fate of these carbon sources, our findings have the potential to support management and conservation efforts aimed at coastal groundwater ecosystems.</p>