Groundwater-driven nutrient inputs to coastal lagoons: the relevance of lagoon water recirculation as a conveyor of dissolved nutrients

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Threats to coastal lagoons

Human impacts

Whilst coastal lagoons are ecologically and economically important for coastal communities, their strong terrestrial influence makes these ecosystems vulnerable to anthropogenic impact, and terrestrial and freshwater inputs, and considered as among the most heavily impacted aquatic ecosystems (Fig. 1.3) (Kennish and Paerl 2010). Most of the anthropogenic pressures are related to rapid population growth and intensification of urbanization. For instance in the Mediterranean region, the coastal population is about one third of the total population of the bordering countries and could reach 220 million by the year 2025 (Brochier and Ramieri 2001). Coastal watershed development often result in water quality problems, contamination, and habitat alteration (Pérez-Ruzafa et al. 2011). Harbor and marine development, recreational and commercial fishing, aquaculture, and agriculture are among the anthropogenic activities threatening coastal lagoons. Nutrient loading from agricultural activities and sewage effluents are major issues in coastal lagoons and often cause eutrophication (Fig. 1.3) (Caumette et al. 1996; De Wit 2011). Eutrophication of coastal surface waters may lead to phytoplankton bloom, hypoxia, loss of seagrass beds and change of community structure, loss of biodiversity, and therefore severe economic impacts (Valiela et al. 1992; Castel et al. 1996; Anthony et al. 2009). While the importance of surface water discharge as source of human-induced pollution to coastal ecosystems has been well documented for decades, the role of groundwater discharge is often overlooked.
Because of their importance for coastal communities and their vulnerability, there is an increasing need to protect and manage coastal lagoons. Best management strategies are often implemented as part of integrated coastal zone management strategies to reduce anthropogenic impacts threatening the conservation and sustainability of coastal lagoon habitat (Kennish and Paerl 2010).

Climate change impacts

Well-known consequences of climate change include sea level rise, increase in water temperature, and changes in precipitation intensity and volume.
Sea level rise is one of the most important effects of climate change in the coastal zone, particularly in semi-enclosed basin such as the Mediterranean Sea (Brochier and Ramieri 2001). Satellite observations since 1993 showed that sea level increases at a rate of approximately 3 mm year-1, which is significantly higher than the rate reported during the previous half-century (1.7 ± 0.3 mm year-1; Church and White 2006). Low-lying and shallow-gradient coastal lagoons are more vulnerable to sea level rise as it narrows the barrier islands and may result in complete disappearance of lagoon, as the lagoon may be converted to an open bay. Sea level rise increases also exchange between lagoon and the open sea and thus increase lagoon water salinity, which may alter species composition in the lagoon (Anthony et al. 2009).
Water temperature increase is also a well-recognized consequence of climate change. The temperature of the world’s ocean has increased by 0.3°C and will likely continue to increase for the next century (Anthony et al. 2009). Changes in air temperature significantly influence the water temperature of slow-moving, shallow water bodies such as coastal lagoons (Anthony et al. 2009; Dailidienė et al. 2011). Water temperature has great influence on dissolved oxygen concentrations and the physiology of living organisms in coastal lagoons. Increasing water temperature tend to reduce the dissolved oxygen concentrations (Bopp et al. 2002), which may affect considerably aerobic species and may even cause hypoxia. Chronic hypoxia in coastal waters is often associated with long-term change in benthic community structure dominated by hypoxia-tolerant species and thus decreases the lagoonal biodiversity (Conley et al. 2007). Furthermore, small change in water temperature may have large impacts on the distribution pattern and migration of lagoonal species (Tomanek and Somero 1999) as increase in water temperature may increase the colonization of allochthonus species that are adapted to the new climatic conditions (Stachowicz et al. 2002).
It is widely recognized that climate change has significant impact on precipitation intensity, timing and volume (Dore 2005; Tabari and Willems 2018). Enhanced precipitation events increase freshwater input to coastal lagoons and thus decrease the salinity. Decreased salinity may have significant negative impacts on marine species living in coastal lagoons and increase the colonization of euryhaline or freshwater species (Kennish and Paerl 2010). Another effect of increased precipitation includes increased surface runoff, which increases the delivery of sediment and nutrients to coastal lagoons (Orpin et al. 1999). Conversely, lower precipitation reduces freshwater inputs and potentially cause hypersaline environment (Anthony et al. 2009). In coastal lagoons with low precipitation, terrestrial groundwater discharges can play an important role in maintaining the brackish conditions and thus preventing hypersalinity of a lagoon during the dry season in a seasonal environment (Stieglitz et al. 2013).

Groundwater processes

While the ecosystem functioning and the impacts of human activities and climate on coastal lagoons have been well studied, the role of groundwater process has only been recently recognized. Indeed, recent investigations demonstrated that groundwater discharge and porewater fluxes (recirculation), are important sources of nutrients to coastal lagoons (Tait et al. 2014; Malta et al. 2017; Rodellas et al. 2018).

Terrestrial groundwater and porewater fluxes (recirculation)

Terrestrial groundwater is defined as low salinity groundwater originated from inland recharge driven by terrestrial hydraulic gradient and includes point source discharge from springs, and diffuse seepage from coastal aquifers (Taniguchi et al. 2002; Burnett et al. 2003) (Fig. 1.3). Distinctly different from groundwater inflow, porewater fluxes or recirculation refer to both short- and long-scale recirculation of saline lagoon water through sediments, which are driven by pressure gradients forced by tides, waves, bottom currents, benthic organisms and porewater density changes (Burnett et al. 2003; Santos et al. 2012a; Huettel et al. 2014) (Fig. 1.3). A part of the marine community uses the term SGD (submarine groundwater discharge) to include both processes and describes SGD as “flow of water through continental margins from seabed to the coastal ocean, with scale lengths of meters to kilometres, regardless of fluid composition or driving forces” (Moore 2010).

Quantification techniques

Quantifying groundwater discharge and porewater fluxes is a challenging task due to the inherent complexity of the discharge process (Burnett et al. 2006). Groundwater inputs are temporally and spatially variable and occur below the sea surface, where direct measurement and observation are complicated. Quantification of groundwater and porewater fluxes depends on the hydrogeological conditions, climate variability and human management of coastal ecosystem (McCoy and Corbett 2009). Groundwater discharge and porewater fluxes (recirculation) can be detected and quantified by a numbers of method including chiefly (1) direct measurements, (2) piezometers, (3) tracer techniques, (4) water balances, (5) thermal imaging, (6) electromagnetic techniques and (7) eddy correlation approach. Whatever the quantification method, groundwater-derived solute flux to coastal systems is most often determined by multiplying the concentration of that solute in the coastal aquifer by the calculated groundwater flux.
– Seepage meters are the most common method of direct measurement as they are relatively simple and inexpensive. They are recognized for providing accurate estimations on small spatial scales (ca. 1 m2) (Corbett and Cable 2003; Burnett et al. 2006). The main disadvantage of the seepage meter method is that it is labour intensive and time consuming (Corbett and Cable 2003). Therefore, automated seepage meters were developed based on heat pulse (Taniguchi and Fukuo 1993), acoustic Doppler technologies (Paulsen et al. 2001) and dye dilution technologies (Sholkovitz et al. 2003).
– The use of piezometers (often multi-level piezometer nests) is another method for quantifying groundwater discharge and porewater fluxes in coastal systems. With this technique, groundwater potential in the sediments can be measured at multiple depths (Povinec et al. 2008). The method is based on the measurements of the hydraulic conductivity and gradient of porewater combined with the Darcy Law. The drawback of the method is the natural variability in the seepage fluxes because of the heterogeneity in the local geology (Burnett et al. 2006). Hydraulic conductivity varies within the aquifer and it is thus difficult to obtain representative value.
– Natural tracer approaches are widely applied to estimate groundwater inputs in costal systems. The main advantage of the method is that natural tracers present an integrated signal when entering the system via different pathways in the aquifer, allowing smoothing out small-scale spatial and temporal variability. However, natural tracers require that all other sources (e.g. river discharge, sediment inputs, precipitation, in situ production) and sinks (e.g. export offshore, in situ consumption, radioactive decay, atmospheric evasion) are evaluated, which is often a difficult task. Among different tracers, naturally occurring radionuclides (radium isotopes and radon) have been extensively used in groundwater studies (Charette et al. 2001; Beck et al. 2007; Burnett et al. 2008; Rodellas et al. 2012; Stieglitz et al. 2013). Radium isotopes (223Ra, 224Ra, 226Ra and 228Ra) and radon (222Rn) are highly enriched in groundwater relative to surface waters (typically 1-2 orders of magnitude), (quasi) conservative, and easy to measure, making them suitable tracers for estimating groundwater discharge and porewater fluxes in coastal systems.
– The water balance approach has been useful in some situations as an estimate of groundwater discharge (Sekulic 1996; Stieglitz et al. 2013; Prakash et al. 2018). The method is based on the quantification of the inputs (e.g. precipitation) and the outputs (e.g. evapotranspiration, surface runoff, and groundwater discharge) of freshwater into a system (Burnett et al. 2006). By constraining all other terms, groundwater discharge can be estimated. The method is relatively simple but it has some limitations. The input and output terms need to be precisely determined for an accurate estimation of the groundwater discharge. Fresh groundwater estimation is often imprecise due to large uncertainties associated with the values used in the calculation.
– Thermal imaging has been used to detect the location and spatial variability of groundwater discharge (Johnson et al. 2008; Bejannin et al. 2017). The method allows detecting cold or warm groundwater inputs in coastal areas due to the thermal contrast between groundwater and the surrounding waters. Whilst discrete temperature measurements are feasible, airborne thermal infrared (TIR) remote sensing is frequently used because it allows covering larger areas. TIR technique is often effective because of its combined used with in-situ measurements, including salinity and geochemical tracers (Wilson and Rocha 2012; Kelly et al. 2013; Tamborski et al. 2015).
– The electromagnetic technique is based on the measurement of the electrical resistivity of the sediments, which is a function of porosity and fluid conductivity (Moore 2010). The technique is based on stationary or streaming electrodes attached to an electric generator to allow rapid data acquisition across relatively long distances from beach or coastal waters (Stieglitz et al. 2008).
– The eddy correlation approach is based on measuring continuously and simultaneously the fluctuation vertical velocity above the sediment-water interface using acoustic Doppler velocimeters (ADCP) and the variations on salinity or temperature. If the groundwater salinity or temperature differs from that of the water column, the groundwater flow can thus be estimated from heat or salt balance (Crusius et al. 2008).

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Groundwater- and recirculation-driven nutrient in coastal ecosystems

Nutrient such as nitrogen, phosphorus, silica and carbon are elements essential for primary production in coastal ecosystems. During the past decade, terrestrial groundwater and porewater fluxes (recirculation) are recognized as an important conveyor of these elements to coastal ecosystems (Santos et al. 2012b; Maher et al. 2013; Rodellas et al. 2014b; Tovar-Sánchez et al. 2014; Tamborski et al. 2018).

Nitrogen sources and biogeochemistry

Nitrogen is the most important element in coastal systems such as lagoons as it is often a limiting factor for primary producers’ growth and thus evaluating its input and biogeochemical cycling is particularly important (Castel et al. 1996; Caumette et al. 1996). Groundwater typically has higher dissolved nitrogen concentrations than surface water, making it an important contributor to the biogeochemical budgets in coastal ecosystems (Table 1.1) (Johannes 1980; Null et al. 2012). For instance, groundwater discharge delivers over 85% of the nitrogen into Buttermilk Bay, Massachusetts USA (Valiela and Costa 1988). In the Mediterranean Sea, which is an oligotrophic basin characterized by limited surface water inputs, numerous studies have demonstrated that the flux of dissolved inorganic nitrogen via groundwater inputs is equal or greater than that from other sources (Garcia-Solsona et al. 2010a; Weinstein et al. 2011; Tovar-Sánchez et al. 2014; Rodellas et al. 2015).
Such large nitrogen input driven by groundwater processes may have biogeochemical impacts on coastal ecosystems. Nitrogen originated from terrestrial groundwater and porewater fluxes are generally subject to active biogeochemical processes in coastal sediments (Slomp and Van Cappellen 2004). Once delivered into a coastal lagoon, the cycle of nitrogen cycle in coastal lagoons includes many processes that are mostly mediated by bacteria, which are summaries in Fig. 1.4 and briefly here.
– Uptake of dissolved inorganic nitrogen (NO3- and NH4+) by the primary producers (phytoplankton and macrophytes) from the water column or porewaters is an important process of the nitrogen cycle in coastal lagoons (Capone 2008). In aquatic ecosystems, the main pathway of nitrogen uptake is through the leaves (Madsen and Cedergreen 2002; De Brabandere et al. 2007), accounting for about the 80% of the total nitrogen acquisition (Lee and Dunton 1999). Uptake through roots is often negligible (De Brabandere et al. 2007).
NH4+ is preferentially taken up by primary producers over NO3- due to reduced energetic costs for its uptake (Middelburg and Nieuwenhuize 2000; Cohen and Fong 2005). Assimilation of NO3- is more energetically demanding, because it requires the synthesis of NO3- and NO2- reductases and associative active transport systems (Syrett 1981).
– Nitrogen fixation is the biological reduction of N2 to reactive nitrogen by diverse arrays of Eubacteria and Archaea called diazotrophs that have the enzyme nitrogenase (Purvaja et al. 2008). It is a crucial process in oligotrophic ecosystems because it can provide potential N in usable form to primary producers. N2 fixation can contribute to more than 50% of the nitrogen required for seagrass growth in tropical zones (Capone 1988) and between 5 and 30% in temperate areas (McGlathery et al. 1998; Welsh 2000). Lower N2 fixation rates were reported in coastal lagoons with high denitrification rates because of the competition between diazotrophs and denitrifiers (Hernández-López et al. 2017).
– The mineralization of organic nitrogen (also called ammonification) converts organic nitrogen to ammonium (Herbert 1999). The process is the result of the breakdown of organic matter such as dead macrophytes and animals or waste materials like excrement, and is carried out by bacteria. The rate of mineralization varies with soil temperature, moisture and the oxygen concentration in the sediments.

Table of contents :

Chapter 1: Introduction
1.1 Coastal lagoons
1.1.1 General characteristics
1.1.2 Classification
1.1.3 Ecological characteristics
1.1.4 Threats to coastal lagoons
1.2 Groundwater processes
1.2.1 Terrestrial groundwater and porewater fluxes (recirculation)
1.2.2 Quantification techniques
1.2.3 Groundwater- and recirculation-driven nutrient in coastal ecosystems
1.3 Study site description
1.3.1 French Mediterranean coastal lagoons
1.3.2 La Palme lagoon
1.3.3 Salses-Leucate lagoon
Chapter 2: Groundwater-driven nutrient inputs to coastal lagoons: the relevance of lagoon water recirculation as a conveyor of dissolved nutrients
2.1 Introduction
2.2 Theory
2.2.1 Concurrent water and radon mass balances for surface waters
2.3 Methods
2.3.1 Porewater collection and analysis
2.3.2 Surface water collection and analysis
2.3.3 Ancillary measurements and analysis
2.3.4 Radon equilibration experiment
2.4 Results
2.4.1 Porewater profiles
2.4.2 Radon and salinity distributions in lagoon surface waters
2.4.3 Nutrients in lagoon surface waters
2.4.4 Estimation of karstic groundwater and recirculation inputs from water and radon mass balances
2.4.5 Nutrient fluxes from karstic groundwater and recirculation
2.5 Discussion
2.5.1 Uncertainties on estimated radon, water and nutrient fluxes from recirculation
2.5.2 Nutrient fluxes to La Palme lagoon
2.5.3 The role of lagoon water recirculation as nutrient source
2.6 Conclusions
Chapter 3: Primary production in coastal lagoons supported by groundwater discharge and porewater fluxes inferred from nitrogen and carbon isotope signatures
3.1 Introduction
3.2 Materials and Methods
3.2.1 Nutrient sources
3.2.2 Sample collection and analysis
3.3 Results
3.3.1 NO3- and NH4+ concentrations
3.3.2 Source isotopic signatures
3.3.3 δ15N in macrophytes and POM
3.3.4 δ13C in macrophytes and POM
3.3.5 Interspecific variations in isotopic signature in macrophytes
3.4 Discussion
3.4.1 Processes affecting macrophyte and phytoplankton δ15N
3.4.2 Macrophyte and phytoplankton carbon uptake and isotope signature
3.5 Conclusion
Chapter 4: Enhanced growth rate of the Mediterranean mussel in a coastal lagoon driven by groundwater inflow
4.1 Introduction
4.2 Materials and Methods
4.2.1 Study sites
4.2.2 Installation of mussel cages and monitoring of environmental parameters
4.2.3 Sample preparation
4.2.4 Condition Index
4.2.5 Growth analyses
4.2.6 Growth curves
4.2.7 Statistical analyses
4.3 Results
4.3.1 Condition index
4.3.2 Shell growth rate
4.3.3 Growth curves
4.3.4 Growth increments
4.3.5 Environmental parameters
4.4 Discussion
4.4.1 Periodicity in shell growth and environmental influences
4.4.2 Growth of M. galloprovincialis in the Mediterranean region
4.4.3 Role of groundwater discharge
4.4.4 Economic implications
4.5 Conclusion
Chapter 5: Conclusion and perspectives
5.1 Conclusion
5.1.1 Quantification of nutrient fluxes from groundwater discharge and recirculation (Chapter 2)
5.1.2 Role of groundwater discharge and porewater fluxes in supporting primary production (Chapter 3)
5.1.3 Effects of groundwater discharge in the growth of the Mediterranean mussels (Chapter 4)
5.2 Research perspectives


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