Submarine groundwater discharge impacts on coastal nutrient biogeochemistry

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                                   Submarine groundwater discharge
                                   impacts on coastal nutrient
                                   biogeochemistry
                                   Isaac R. Santos 1,2 ✉, Xiaogang Chen 3, Alanna L. Lecher4, Audrey H. Sawyer5,
                                   Nils Moosdorf 6,7, Valentí Rodellas 8, Joseph Tamborski9, Hyung-​Mi Cho10,
                                   Natasha Dimova11, Ryo Sugimoto12, Stefano Bonaglia1, Hailong Li13,
                                   Mithra-​Christin Hajati6 and Ling Li3
                                   Abstract | Submarine groundwater discharge (SGD) links terrestrial and marine systems, but
                                   has often been overlooked in coastal nutrient budgets because it is difficult to quantify. In this
                                   Review, we examine SGD nutrient fluxes in over 200 locations globally, explain their impact on
                                   biogeochemistry and discuss broader management implications. SGD nutrient fluxes exceed
                                   river inputs in ~60% of study sites, with median total SGD fluxes of 6.0 mmol m−2 per day for
                                   dissolved inorganic nitrogen, 0.1 mmol m−2 per day for dissolved inorganic phosphorus and
                                   6.5 mmol m−2 per day for dissolved silicate. SGD nitrogen input (mostly in the form of ammonium
                                   and dissolved organic nitrogen) often mitigates nitrogen limitation in coastal waters, since SGD
                                   tends to have high nitrogen concentrations relative to phosphorus (76% of studies showed N:P
                                   values above the Redfield ratio). It is notable that most investigations do not distinguish saline
                                   and fresh SGD, although they have different properties. Saline SGD is a ubiquitous, diffuse pathway
                                   releasing mostly recycled nutrients to global coastal waters, whereas fresh SGD is occasionally
                                   a local, point source of new nutrients. SGD-​derived nutrient fluxes must be considered in water
                                   quality management plans, as these inputs can promote eutrophication if not properly managed.

Submarine groundwater
                                  Excessive anthropogenic nutrient inputs drive wide-           SGD occurs on timescales of hours to millennia, spa-
discharge                         spread eutrophication in global coastal waters 1,2.           tial scales of metres to kilometres and as a low flux over
The flow of water through         Despite large investments to reduce nutrient inputs           large areas, making it challenging to quantify28 and, thus,
continental margins from the      from wastewater and urban and agricultural runoff3,4,         sometimes misinterpreted. As a result, SGD has often
seabed to the coastal ocean,
                                  coastal eutrophication and hypoxia continue intensify-        been considered a nutrient source to coastal waters
with length scales of metres to
kilometres, regardless of fluid   ing worldwide, even where these conventional nutrient         only after the ‘standard’ pathways, such as atmospheric
composition or driving force.     sources have decreased5–7. Alternative nutrient sources       deposition, rivers and sewage, are ruled out.
                                  and pathways such as submarine groundwater discharge              SGD is ubiquitous in sandy, muddy and rocky shore-
                                  (SGD) also contribute to persistent water quality issues      lines and represents a combination of fresh and saline
                                  in the coastal ocean2. Pioneering local-​scale research in    groundwater interacting with coastal surface waters29,30
                                  the 1980s revealed extremely high nitrate concentra-          (Fig. 1). Fresh SGD is driven by a positive terrestrial hydrau-
                                  tions in fresh coastal groundwater in Western Australia8,     lic gradient and emerges from shallow or deep aquifers
                                  where fresh SGD fluxes exceeded river nitrate loads and       intersecting the shoreline31,32 carrying natural and anthro-
                                  explained ~50% of local primary productivity9.                pogenic nutrients from land. Saline SGD (sometimes also
                                      Quantitative investigations have since revealed that      referred to as seawater circulation in sediments) is defined
                                  SGD delivers nutrients and affects water quality in           as the advection of saline groundwater through inter-
                                  diverse coastal ecosystems, such as estuaries10,11, coral     tidal zone sediments and/or across the coastal seafloor,
                                  reefs12–14, coastal embayments and lagoons15–17, intertidal   and/or advective porewater exchange on scales larger
                                  wetlands such as mangroves18,19 and saltmarshes20–22,         than one metre28,30,33. Saline groundwater also mixes with
✉e-​mail: isaac.santos@gu.se      the continental shelf23–25 and even the global ocean26.       fresh SGD owing to the interactions of tides and waves,
https://doi.org/10.1038/          Nevertheless, nutrient fluxes via SGD remain overlooked in    density-​driven flow and dispersion processes34, with the
s43017-021-00152-0                most coastal nutrient budgets and water quality models27.     resulting brackish SGD transporting both land-​derived

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                                                                                                 new water and dissolved species from the marine per-
 Key points
                                                                                                 spective. In contrast, saline SGD often flushes out
 • Submarine groundwater discharge (SGD) is an essential component of biogeochemical             recycled nutrients generated during the degradation
   budgets. Fresh SGD is a source of new nutrients, whereas saline SGD often releases            of sediment organic matter, as well as external nutrient
   recycled nutrients from sediments.                                                            sources entrained from the mixing of fresh and saline
 • SGD-​derived nitrogen fluxes exceeded river inputs in ~60% of the reviewed cases and          waters35,52. Saline SGD has a net zero water volume
   usually counteracted nitrogen limitation in coastal waters due to high N:P exceeding          exchange over timescales longer than the cyclic pressure
   the Redfield ratio.
                                                                                                 oscillations driving it. Seawater that infiltrates coastal
 • Positive impacts of SGD on coastal ecosystems include enhanced coral calcification,           sediments eventually returns to the ocean with a differ-
   primary productivity, fisheries, denitrification and pollutant attenuation.
                                                                                                 ent chemical composition53 on timescales ranging from
 • Negative impacts of SGD include eutrophication, algal blooms, deoxygenation and               days to weeks when driven by tides or storms35,54,55, and
   localized ocean acidification, depending on site-​specific conditions.                        from seasons to years when driven by convection or
 • Considering SGD is crucial to reach the United Nations Sustainable Development                sea-​level oscillations56–59. Much emphasis has been given
   Goals pollution targets. The US Supreme Court decision to consider SGD under the              to ubiquitous nearshore tidally driven saline SGD with
   Clean Water Act represents a positive policy change, signalling broader appreciation
                                                                                                 semi-​diurnal, diurnal or fortnightly variations34,60. Fewer
   of SGD impacts.
                                                                                                 studies have addressed irregular forcing, such as varying
                                                                                                 wave conditions61, storms62, estuarine density inversions63
Permeability                       and marine-​derived nutrients30,35. Brackish SGD occurs       or sea-​level anomalies64, that can flush the upper few
A measure of the ability of        further offshore, where confined aquifers intersect embay-    metres of coastal permeable sediments and produce
unconsolidated rocks and           ments and on the continental shelf31,36. These deeper aqui-   large episodic pulses or seasonal offshore saline SGD65
sediments to allow                 fers are less vulnerable to nutrient contamination from       and deliver both new and recycled nutrients.
groundwater flow.
                                   onshore activities because of geological isolation. Where         The volume of fresh SGD entering the global ocean
Hydraulic heads                    land-​derived nutrients are present in confined aquifers,     is relatively small compared with rivers66,67, accounting
Vertical and horizontal pressure   travel times offshore can reach centuries or longer37.        for ~1% of total freshwater inputs to the ocean and
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                               a Sandy coasts: permeable sediments

                                    Anthropogenic sources                           N2 fixation
                                                                               N2
                                                                                        POM infiltration                                             High tide

                                              NO3–                          Mineralization                               Brackish SGD
                                                                                                          NO3–
                                                     Denitrification
                                                                            NH4+                                        NH4+ ~ DON > NO3–           Low tide
                                                                                    Nitrification
                                                       DNRA
                                Soil OM                                     NH4+
                                             Mineralization
                                                                 DON
                                            Leaching

                               b Muddy coasts: secondary permeability created by burrows

                                                   NO3–                                      N2 fixation
                                                                                                                                                    High tide
                                                                             N2
                                                                                             POM

                                                           Denitrification
                                    Plant uptake                                   Aerobic mineralization        NO3–

                                High                          DNRA                    Suboxic burrows
                                                                                          Nitrification           Saline SGD >> fresh SGD
                                soil      Anaerobic                            NH4+
                                OM        mineralization                                                                                            Low tide
                                                                   DON
                                                   Leaching
                                                                                                                                   DON + NH4+

                               c Rocky coasts: fractures and/or conduits in karstified carbonate or volcanic rocks

                                  NO3– sources
                                  Oxic conditions
                                  Low OM
                                  Minor NH4+ and DON production
                                  Ineffective NO3– attenuation                                                                                       High tide

                                                                                                                                                    Low tide

                                                                                                                               Fresh SGD > saline SGD
                                                                                      Submarine springs                           NO3– > DON ~ NH4+

                                             Fresh SGD                   Saline SGD

                               Fig. 1 | the nitrogen cycle in sandy, muddy and rocky coastal aquifers. The sizes of the background arrows qualitatively
                               indicate the relative magnitude of fresh and saline submarine groundwater discharge (SGD). a | Sandy coasts are often
                               characterized as having brackish SGD with higher concentrations of ammonium (NH4+) and dissolved organic nitrogen
                               (DON) than nitrate (NO3−). b | Muddy coasts often host burrowing fauna, which create secondary sediment permeability
                               and promote aerobic mineralization, nitrate reduction and saline SGD. c | Rocky coast SGD tends to be dominated by
                               freshwater, with relatively high concentrations of NO3− relative to DON and NH4+. DNRA, dissimilatory nitrate reduction
                               to ammonium; OM, organic matter; POM, particulate organic matter.

                               saline groundwater concentrations, then saline SGD can              SGD inputs of dissolved inorganic nitrogen (DIN), dis-
                               enhance microbial denitrification by consuming nitrate              solved inorganic phosphorus (DIP) and DSi seem to be
Denitrification                and, thus, attenuate nitrogen pollution90. For example,             derived from saline SGD26, with fresh SGD represent-
Microbial process in the
nitrogen cycle that converts
                               saline groundwater flow through intertidal sediments                ing a minor contribution66. However, at sites where fresh
nitrate to nitrogen gas that   removes nitrogen from surface waters in coastal wet-                SGD is volumetrically important (usually karst or vol-
flows to the atmosphere.       lands receiving high nitrogen loads91. Most of the global           canic landscapes with high permeability) (Fig. 1), nutrient

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Karst                             fluxes supplied by fresh SGD dominate the local nutrient      Global distribution of SGD studies
Landscape formed by               sources to coastal waters49,92,93.                            Here, we compiled fresh and/or saline SGD-​derived
carbonate rocks often                 Fresh and saline SGD pathways vary between sandy,         fluxes of at N, P and/or Si reported by 239 study cases
weathered by dissolution          muddy and rocky coastlines, owing to the unique hydro-        from 31 countries (Fig. 2, Supplementary Table 1). Most
and with abundant conduits
for fast groundwater flow.
                                  geological characteristics of coastal aquifers. Sandy         of the flux data relied on radon (27%) and radium (45%)
                                  coasts generally consist of highly permeable sediments        isotope measurement of SGD rates. These methods
Unconfined aquifers               that effectively connect aquifers to the coastal ocean        result in SGD rates that are, on average, a factor of two
Surficial aquifers situated       (Fig. 1a). A typical unconfined surficial sandy aquifer       greater than estimates based on modelling approaches
above a low-​permeability layer
                                  stores fresh groundwater from upland regions, dis-            (Supplementary Table 2), likely reflecting the large num-
of sediment or rock, and with
the upper water layer at
                                  charging to the sea within or below the intertidal zone.      ber of marine processes driving (mostly saline) SGD that
atmospheric pressure.             Tidal or wave dynamics can create seawater circulation        are captured by radon and radium isotopes34,118, whereas
                                  cells nearshore within beach sediments94,95, while var-       hydrological models quantify specific driving forces and
Oxidation-​reduction              ious forcing mechanisms can drive saline SGD farther          components of fresh and saline SGD33,119,120.
potential
Measure of the tendency of
                                  offshore52,65,96–98. In contrast, muddy coasts dominated by       From a climatic zone perspective, SGD nutrient
a chemical species to acquire     mangroves and saltmarshes (Fig. 1b) are characterized         investigations are similarly split between the tropics
electrons, to be reduced or       by lower permeability sediments that facilitate saline        (27%), subtropics (30%) and temperate (32%) regions
to lose electrons, or to          SGD once the secondary permeability has been enhanced         (Fig. 2). Polar regions remain severely understudied, with
be oxidized.
                                  by burrows, root structures or buried vegetation99–102.       only two studies quantifying SGD-​derived nitrogen
                                  Rocky coasts (Fig. 1c) contain fractures and/or conduits      fluxes in Alaska121. Of all studies in the tropics, 50% are
                                  that allow direct fresh SGD flows to the sea with no or       located in Asia and 25% are from the Hawaiian Islands.
                                  minor biogeochemical transformations14,69,103,104. The        In the subtropics, 37% of the studies are from the USA
                                  fresh SGD component is usually expected to exceed             alone, and only 19% of the study sites are located in the
                                  saline SGD in karst and volcanic coastal aquifers, with       Southern Hemisphere (primarily Australia). Temperate
                                  fresh groundwater flows susceptible to regulation by          regions between 35° and 60° are mainly represented by
                                  tidal forcing mechanisms46,104.                               Europe (38%) and the east coast of the USA (26%), and
                                      Topography and geomorphology can also influence           are highly skewed to the Northern Hemisphere (93%).
                                  SGD, but the effects remain largely unquantified. For         In total, 38% (n = 79) of the compiled studies were from
                                  example, the regional topography of the coastal zone dic-     Asia, followed by North America (33%), Europe (16%)
                                  tates the slope of the water table and the inland hydraulic   and Australia/Oceania (11%). Only two investigations
                                  gradient in coastal unconfined aquifers, which, in turn,      quantified SGD-​d erived nitrogen inputs in South
                                  influences fresh SGD105,106. Nearshore morphological          America (bay and lagoon ecosystems in Brazil25,122)
                                  features, such as beach slope breaks, tidal creeks and        and three in Africa (estuary and lagoon ecosystems
                                  heterogeneous stratigraphy, affect seawater circulation       in Egypt123 and South Africa124). Thus, there is a clear
                                  in beaches and saline SGD, as observed and modelled in        need to conduct SGD investigations in poorly repre-
                                  a coarse carbonate sand aquifer on the Cook Islands107,108    sented areas in Africa, South America and high latitudes
                                  and in saltmarshes in China100,109.                           across all ecosystem types. The limited existing datasets
                                      Fresh SGD carries land-​derived nutrients that are        and large uncertainties in individual estimates prevent
                                  an external nutrient source to coastal waters, with con-      inferring any specific pattern across different climates
                                  siderable variability between sandy, muddy and rocky          (Supplementary Table 3).
                                  coastlines. For example, seagrass, mangrove and salt-             Several interesting inferences emerge comparing
                                  marsh vegetation assimilate nutrients directly from           measurements between ocean basins. Median (and inter-
                                  groundwater (Fig. 1b). Sediment properties like organic       quartile range) SGD rates and inorganic nutrient fluxes
                                  matter content control oxidation-​reduction potential         are greatest for the Indian Ocean (SGD = 17, 5–48 cm
                                  and the energetic favourability of denitrification.           per day; DIN = 11, 3–29 mmol m−2 per day), where there
                                  Phosphorus or silicate-​bearing minerals in rocks can         was the smallest number of study cases (Supplementary
                                  act as a natural source of DIP and DSi, whereas iron          Table 4). For the Pacific Ocean, median SGD rates
                                  oxides immobilize DIP through sorption87. Phosphorus          (9, 2–22 cm per day) and DIN (8, 2–27 mmol m−2 per
                                  can be released back to porewater when iron oxides            day) and DSi (9, 2–60 mmol m−2 per day) fluxes exceed
                                  are reduced, as observed in saltmarshes110,111 and sandy      those of the Atlantic Ocean (SGD = 4, 1–10 cm per day;
                                  aquifers87 exposed to both fresh and saline SGD. SGD          DIN = 2, 2–60 mmol m−2 per day; DSi = 2, 0–12 mmol m−2
                                  nutrient inputs are also conditioned by the discharge         per day), in spite of a large natural variability. The dif-
                                  type. Slow, diffusive fresh and saline SGD through            ferences in DSi fluxes are likely driven by differences in
                                  sandy permeable sediments allow for greater nutrient          continental lithology and the presence of active (Pacific)
                                  transformations in subterranean estuaries82,112,113, but      and passive (Atlantic) margins125. The median DIP flux
                                  rapid fresh groundwater discharges through conduits           for the Mediterranean Sea (0.03, 0.01–0.10 mmol m−2
                                  (for example, karstic or volcanic aquifers) prevent sub-      per day; n = 24) is approximately three times lower
                                  stantial nutrient attenuation114,115. Fresh and saline SGD    than that of the Atlantic and Pacific oceans (0.10, 0.02–
                                  ultimately deliver regenerated nutrients associated with      0.48 mmol m−2 per day), because the Mediterranean
                                  the decomposition of organic matter in soils and sedi-        coastline hosts many karstified aquifers that retain
                                  ments, and these natural and internal nutrient sources        phosphate126.
                                  are also a component of nutrient budgets in coastal               From the synthesis here, sites with high SGD-​
                                  marine waters116,117.                                         derived DIN fluxes are often located in regions with

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a

                                     d                             c                                                   e

    b

                                                                                                                                   f
 Ecosystem type             SGD rate (cm per day)
    Estuary, bay and lagoon    0–1
    Mangrove and marsh         1–5
    Karst aquifer              5–15
    Coral reef
    Sandy beach                15–40
    Marginal bay and shelf     40–280
    Others

                b                                    c

                        200 km                             1,000 km

d                                                    e                                                            f

                                 500 km                                                   1,000 km                                  1,000 km

                           Fig. 2 | SGD rates from study cases reviewed here. a | Submarine groundwater discharge (SGD) fluxes globally, colour-​
                           coded by ecosystem type, where the size of the circle represents the reported SGD rate. Similar maps for each nutrient are
                           shown in the supplementary material. Investigations where SGD rates are reported without any nutrient fluxes were not
                           included in the compilation. b | SGD in Hawaii, USA, with ecosystems coloured and rates scaled as above. c | SGD in the
                           Mediterranean. d | SGD on the east coast of the USA. e | SGD in East Asia. f | SGD on the eastern coast of Australia.

                           contaminated coastal aquifers. These sites include            macroalgal growth and eutrophication have been linked
                           groundwater flowing across septic systems in Hawaii127,       to SGD from multiple perspectives and methods41,130,131.
                           heavily fertilized catchments in the northeast USA128,        However, fresh and saline SGD can sustain relatively
                           urban embayments in China129 and coastal aquifers with        high nitrogen fluxes, even at sites with no apparent
                           naturally high nitrate due to large bird populations13.       anthropogenic contamination sources, such as protected
                           High DIN fluxes in coral reefs and estuaries (Fig. 3) might   saltmarshes on the USA east coast22,110,132.
                           be due to measurement bias towards ecosystems that are            The study sites considered ranged from small near-
                           already known to be impacted by nutrient enrichment.          shore sites that spanned ~100 m2 along beaches133,134 to
                           For example, in Waquoit Bay (MA, USA), excessive              large regions that spanned marginal seas such as the

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Subterranean estuaries           Mediterranean Sea 126 and the Yellow Sea 135, or the               Nutrient ratios and speciation
The locations in coastal         global ocean26. Although there was no direct corre-                Biogeochemical transformations within coastal aqui-
aquifers where there is mixing   lation between the area covered by individual study                fers and subterranean estuaries (where fresh and saline
between fresh groundwater        cases and SGD rates or related nutrient fluxes, group-             groundwater mix136–138) dramatically modify nutrient
and seawater, and chemical
reactions modify the
                                 ing the available data into three major classes revealed           concentrations and chemical speciation along SGD flow
composition of submarine         greater nutrient fluxes on the small (
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a Nutrient limitation                                                                            b Nitrogen speciation          0
          10,000                                                                                                                    100          SGD

                                                         N:Si = 16:15
                                                                                                                                                 Ten largest rivers
                                                                                                                                                 Rivers sampled
                                                                                                                                                 with SGD
                                                                                                                         25
           1,000                                                                                                                           75
                                                                                            5                                   NH4+
                              DSi rich                                                   =1                                   dominated
                                                                                    :P
                                                                                  Si
                                                                                                          DON
DIN:DIP

                                                                                                                50                                        NH4+
            100                                                               N rich                                                                 50

                   N:P = 16
                                                                                                         75
             10                                                                                                                                              25
                                                                                                                DON                            NOx
                                                                                                              dominated                      dominated
                                                                         P rich

                                                                                                 100
              1                                                                                                                                                      0
              0.001            0.01          0.1                1        10                100     0             25             50              75                100
                                                   DIN:DSi                                                                      NOx

                                      Fig. 4 | nutrient limitation and speciation in SGD versus rivers. a | Dissolved inorganic nitrogen (DIN):dissolved
                                      inorganic phosphorus (DIP) versus DIN:dissolved silicate (DSi) ratios in submarine groundwater discharge (SGD) from
                                      our global compilation, with the same ratios in the ten largest rivers globally included for comparison. b | The relative
                                      contribution of the three main nitrogen species in SGD and rivers, showing that SGD is often dominated by ammonium
                                      (NH4+) and dissolved organic nitrogen (DON), whereas rivers are often dominated by nitrate (represented as NOx)
                                      and DON.

                                      Soil organic matter is remineralized by microorganisms            primary producer uptake, microbial mineralization and
                                      in oxic or anoxic conditions149, resulting in ammonium            sediment denitrification162,163. As a result, groundwater
                                      release. Ammonium is readily oxidized to nitrate through          inputs with a high N:P or N:Si ratio can encourage the
                                      nitrification in the presence of oxygen (Fig. 1a). Because        growth of certain phytoplankton groups163. For example,
                                      of oxygen paucity in many organic-​rich coastal aquifers,         diatom blooms often occur at N:Si ratios lower than 1,
                                      nitrification is generally constrained to the sediment            whereas harmful species (usually dinoflagellates) usu-
                                      surface, but can become very important in the presence            ally bloom at higher ratios164. The DIN:DIP ratios in
                                      of burrowing animals in muddy sediments150 (Fig. 1b).             SGD were above the Redfield ratio of 16:1 in 75% of
                                      In sandy and muddy coastal areas, nitrogen fixation               the study sites, demonstrating that SGD often atten-
                                      related to abundant sulfate-​reducing bacteria in inter-          uates nitrogen limitation and stimulates primary pro-
                                      tidal sediments can eventually turn atmospheric N2 into           ductivity in coastal waters (Fig. 4a). The DIN:DIP ratios
                                      ammonium151,152, which can be easily incorporated                 in SGD study cases ranged from 1 to 12,100 (aver-
                                      into organic matter and infiltrate subterranean estuaries,        age ± standard deviation = 259 ± 1,090; n = 169) and
Nitrogen fixation                     owing to waves and tides (Fig. 1a,b).                             the DIN:DSi ratios ranged from 0.1 to 47.5 (2.0 ± 5.4;
Microbial process that leads to
the conversion of nitrogen gas
                                          Nitrate is removed by the microbial conversion to             n = 96). Based on those ratios, SGD in 58% of the com-
into ammonia/ammonium.                N2 through denitrification in the absence of oxygen               piled study sites had Si-​enriched conditions, 36% were
                                      and the presence of organic carbon in muds and sand               N-​enriched and 6% were P-​enriched relative to the
Dissimilatory nitrate                 aquifers90,140,153. Nitrate can be converted back to ammo-        Redfield ratio (Fig. 4a). DIN:DIP ratios were usually
reduction to ammonium
                                      nium by the dissimilatory nitrate reduction to ammonium           >16, even at sites classified as Si-​enriched, demonstrat-
Microbial process in the
nitrogen cycle that converts          (DNRA)154, both of which can be enhanced by tidally               ing that SGD counters N-​limited conditions in most
fixed nitrogen from nitrate           driven SGD in muddy intertidal marshes155 or permea-              coastal waters.
to ammonium.                          ble sands156–158. Moreover, both ammonium and nitrate                 High DIN:DIP ratios in SGD are expected, as phos-
                                      are also temporarily removed by microbial and plant               phorus is often immobilized through adsorption to min-
Diatom
Microscopic algae (unicellular
                                      uptake (Fig. 1b). In contrast to muddy and sandy coasts,          eral surface sites of Fe/Mn oxides87,89,165 or scavenged by
and non-​flagellate) with a           however, high nitrate loading and oxygen presence in              co-​precipitation with calcium carbonate166. Hence, in
characteristic wall made up of        volcanic and karst coasts (as in Hawaii, Yucatan and              hypoxic and anoxic aquifers, including saltmarshes and
silica and are one of the most        in the Mediterranean) lead to a simplified nitrogen               mangroves, DIN:DIP ratios in SGD can be controlled
important groups of planktonic
                                      cycle, with little nitrate attenuation and high export to         by the seasonal reduction and oxidation cycling of Fe
marine microalgae.
                                      the sea72,115,159,160 (Fig. 1c).                                  oxides driving DIP88,167,168. Particularly high DIN:DIP
Dinoflagellates                           The ratio of nutrients supplied to coastal waters             ratios are observed in coastal aquifers contaminated by
Group of microscopic algae            (Fig. 4a) can limit primary production and influence              sewage and fertilizers because the phosphorus source is
(mostly unicellular and               biological communities if the source differs sub-                 often attenuated faster than nitrogen along groundwa-
flagellate) representing one of
the most important groups
                                      stantially from the Redfield ratio161. In the absence             ter flow paths145. Moreover, groundwater nitrogen from
of both marine and freshwater         of anthropogenic sources, the coastal ocean is often              fertilizers applied in the last century can still be found in
phytoplankton.                        nitrogen-​limited, owing to efficient coupling between            coastal aquifers37,169. Despite substantial improvements

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          in fertilizer management in some European countries,            Comparing SGD and river fluxes
          nitrate concentrations in groundwater have not shown            Rivers are often assumed to be the primary nutrient
          any immediate decreasing trend following reductions in          source to coastal waters, so riverine nutrient fluxes pro-
          fertilizer application170,171.                                  vide a valuable reference frame for contextualizing SGD
              Our data compilation supports earlier model pre-            (Fig. 5). Global estimates of nutrient fluxes supplied by riv-
          dictions145 that the discharge of legacy N-​contaminated        erine discharge to the coastal ocean184–186 are on the order
          groundwater will eventually change the coastal ocean            of ~40 Tg N per year, ~9 Tg P per year and ~140 Tg Si per
          from the current N-​limited to a P-​limited state. Such a       year, although these estimates vary widely depending on
          pattern has been observed in a SGD-​dominated urban             the model used187,188. River nutrient fluxes vary greatly
          embayment in China, where surface water DIN:DIP                 among the continents, reflecting the regional differences
          ratios have increased from 25 to 96 between the 1980s           in population, the associated anthropogenic nutrient
          and the mid-2010s, owing to seepage of contaminated             inputs and the hydrological cycle189,190. For instance,
          SGD172. In the Po river estuary in Italy, a notable increase    natural sources are the main contributor to N fluxes sup-
          of DIN:DIP ratios from 47 to 100 between 1970 and 2016          plied by rivers in Africa, Oceania and South America,
          was linked to the discharge of nitrogen-​polluted ground-       whereas most of the N is supplied by anthropogenic
          water173. Increasing anthropogenic nitrogen inputs in           sources in Asia, North America and Europe188.
          coastal regions could lead to an increasing N:Si ratio,             Basin-​w ide or global-​s cale assessments of SGD
          which provides an unfavourable environment for dia-             have suggested that total SGD-​derived nutrient inputs
          toms, while enhancing the likelihood of dinoflagellates         are comparable to or higher than river-​derived nutri-
          and cyanobacteria blooms174,175.                                ent fluxes in the Mediterranean Sea126, the coast of
              Although nitrogen is often the nutrient of greatest         China172 and in the global ocean26. For example, total
          concern in SGD, few studies have reported detailed              SGD-​derived (19 × 1010 mol per year) nitrogen fluxes into
          nitrogen speciation data. Only 31 studies reported              the Mediterranean Sea exceed river fluxes (5 × 1010 mol
          the three major nitrogen species, and 13 studies also           per year)126 by a factor of ~4. Fresh SGD from karstic
          reported N speciation in nearby rivers (Fig. 4b). Previous      springs in the Mediterranean, a dominant regional fea-
          studies often focused on DIN145 (such as nitrate and            ture, account for 8–31% of these river-​derived nitrogen
          ammonium, which are more readily available to pri-              fluxes72. In China, an upscaling of local case studies to
          mary producers) and overlooked SGD-​derived DON                 the entire coastal zone revealed that total SGD-​derived
          (which is assimilated at slower rates176) because the con-      fluxes of nitrogen, phosphorus and silicate account for
          tribution of DON to primary production is unknown.              >50% of all known sources, including rivers, atmospheric
          Additionally, many SGD studies emphasize nitrate                deposition and diffusion from sediments172.
          because anthropogenic activities often contribute large             At a local scale, SGD-​derived nutrient fluxes exceeded
          nitrate loads115,177,178, yet, only six of the 31 SGD studies   river fluxes in >48% of the compiled study cases, and
          reporting ammonium, nitrate and DON found nitrate               SGD-​derived nutrient fluxes were at least 10% of the
          to be the dominant form of nitrogen. All of those sites         river fluxes in >90% of the study sites (Fig. 5). Note
          were heavily influenced by local contamination sources.         that several SGD studies did not report riverine fluxes
              Groundwater and seawater DON is often derived               of nutrients, perhaps because they were conducted in
          from soil leachates, zooplankton excretion and leach-           areas with no or minor surface runoff114,191. Furthermore,
          ing from microbial and algal biomass that infiltrate            we highlight that any comparison between rivers and
          subterranean estuaries112,176,179,180. DON increases along      SGD at a local scale can be biased, owing to a poten-
          the coastal ocean and in surface estuaries, where it            tial selection of sites where fresh SGD is expected to be
          often constitutes the largest fraction (73 ± 23%) of            high and groundwater pollution is known or expected.
          the total dissolved nitrogen pool180. Only 40 out of the        Direct comparisons of SGD fluxes across hydrolog-
          239 study sites included here reported DON data, and            ical or land-​use gradients using the same method are
          no study revealed the composition and bioavailability of        uncommon, despite observations in Hawaii 160 and
          DON in SGD. On average, DIN accounted for 57 ± 28%              northeast USA176,192 showing a clear impact of land use
          (median 61%) and DON accounted for 43 ± 27%                     on SGD-​derived nitrogen fluxes.
          (median 39%) of total dissolved nitrogen fluxes via SGD.            Global patterns of SGD and river distributions show
          DON and ammonium are relatively more abundant in                a similar dependency on land use, with higher nutri-
          non-​contaminated groundwater181, but DON may also              ent concentrations and N:P ratios in densely populated
          originate from anthropogenic sources176. Refractory             and agricultural areas145,172,193,194. However, nutrient
          DON uptake is often attributed to heterotrophic bacte-          fluxes supplied by SGD and rivers might be consid-
          ria over timescales of millennia, but the less abundant         erably different, depending on the magnitude of dis-
          labile DON compounds such as amino acids and urea               charge. For instance, about 70% of global SGD occurs
          are used up by autotrophic microbes and phytoplank-             in the Indo-​Pacific Oceans, while less than half of the
          ton on timescales of hours to days180. Because of high          river waters are discharged in the Indo-​Pacific30. River
          DON contributions via SGD (Fig. 4b), even a small               and SGD fluxes are also considerably different at a local
          labile portion could make a difference to the amount            or regional scale. In contrast to river discharge that is
          of N ultimately available to primary producers. Overall,        restricted to specific point sources along the coast such
          our compilation supports earlier suggestions that               as river mouths, SGD (particularly the saline compo-
          DON represents a significant portion of nitrogen in             nent) is ubiquitous along permeable sediment and
          SGD141,176,179,182,183.                                         muddy shorelines, and is relatively diffuse. Therefore,

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                                            a                                                                           Water flow     DIN     DIP        DSi
                                                                                                                        m3 per year       Tmol per year
                                                                                                           River         3.8 × 1013   1.35   0.045      0.045
                                                                                                           Fresh SGD     3.3 × 1011   0.03   0.001      0.001
                                                                                                           Total SGD     1.2 × 1014   2.30   0.060      0.060

                                                                     River inputs

                                                                                        Fresh SGD                Saline SGD

                                    b
                                                                                          SGD < river    SGD > river
                                                                                                                              DIN
                                                                                                         DIN 59%
                                                        25                                               DIP 53%              DIP
                                                                                                         DSi 48%              DSi

                                                        20
                                Number of study cases

                                                        15

                                                        10

                                                         5

                                                         0
                                                             100
                                                                                        SGD:river nutrient flux ratios

                                   Fig. 5 | river and SGD-derived nutrient inputs to the ocean. a | A summary of global-​scale fluxes compiled from
                                   river163,187,188, fresh submarine groundwater discharge (SGD)63 and total (mostly saline) SGD27,65 estimates. b | Histogram
                                   of ratios between SGD and river-​derived dissolved inorganic nitrogen (DIN), dissolved inorganic phosphorus (DIP) and
                                   dissolved silicate (DSi) fluxes summarized from the global study cases reviewed here. In >48% of the global study cases,
                                   SGD-​derived nutrient fluxes exceeded river fluxes. In ~90% of the study cases, SGD nutrient fluxes were >10% of river
                                   fluxes, making SGD a non-​negligible nutrient pathway in nearly all study sites.

                                   SGD is likely to affect larger coastal areas than river          in anthropogenic nitrogen loads in rivers in recent
                                   discharges195.                                                   decades198,199. Although rivers are usually dominated by
                                      Both SGD-​derived and river-​derived fluxes of water          a mixture of nitrate and DON, nitrogen in SGD (par-
                                   and dissolved nutrients to the coastal ocean are affected        ticularly saline and brackish) is mostly composed of
                                   by seasonal patterns in the hydrological cycle. Seasonal         DON and ammonium, owing to reducing conditions in
                                   changes in recharge, evapotranspiration and groundwater          organic-​rich shallow coastal sediments and mineraliza-
                                   extraction drive water-​level changes onshore that pro­          tion of organic matter (Fig. 1). The contrasting nitrogen
                                   pagate offshore by pressure diffusion. As a result, SGD          speciation in SGD and rivers highlights the need for
                                   typically experiences a delayed response to seasonal             including the three major dissolved nitrogen species in
                                   fluctuations relative to river fluxes66. Fresh and saline        future investigations.
Evapotranspiration                 SGD rates and associated nutrient fluxes can lag peak                The river nutrient transport to the ocean has more
The quantity of water that         recharge periods by several months, depending on flow            than doubled during the twentieth century184,186,187,200, as
moves to the atmosphere            path lengths, aquifer transmissivity, storage properties         a result of increases in population and fertilizer use201.
from the plants and soil;          and recharge volume59,196,197.                                   Although no similar datasets exist for long-​term changes
describes the joint effect of
transpiration, through the
                                      Rivers and SGD are characterized by unique sto-               in total SGD, modelled fresh SGD-​d erived nitrate
plants, and evaporation,           ichiometric ratios and nutrient speciation (Fig. 4) .            fluxes increased by about 40% over the second half
directly from the soil.            Nitrate accounts for much of the global increase                 of the twentieth century193. Given the slower response of

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Microphytobenthos                groundwater to anthropogenic nutrient inputs, ground-          change, depending on the specific location or time of
Living organisms, such as        water polluted several decades ago can continue to             the year.
unicellular eukaryotic algae     discharge, releasing legacy nutrients that impact water            The most documented response to SGD-​derived
(mainly diatoms) and             quality in rivers and the coast even after pollution           nutrient loading is related to increasing primary pro-
cyanobacteria, growing in the
upper layers of illuminated
                                 sources cease to exist2,202. For instance, recent investiga-   ductivity of phytoplankton or microphytobenthos205.
aquatic sediments.               tions at the mouth of the Mississippi River revealed that      Chlorophyll is often measured as a proxy for primary
                                 most of the N in surface water had been in the water-          productivity derived from SGD206 and most attempts
Cyanobacteria                    shed for >30 years, as a consequence of the time spent         to link SGD and chlorophyll have revealed a positive
Ubiquitous phylum of
                                 both in the soils and travelling along slow groundwater        response207 (Fig. 6). The increase in primary productivity
single-​celled bacteria that
carry out photosynthesis.
                                 transport pathways2,145,193. Therefore, despite the poten-     by SGD inputs from uncontaminated aquifers has been
                                 tial mitigation measures aimed at decreasing terrestrial       linked to diatom abundance that effectively use up the
Macrophytes                      nutrient loads in polluted areas, it can take decades to       nitrogen, particularly in areas where SGD can alleviate
Large aquatic plants and         achieve the desired reduction of SGD-​derived nutrient         co-​limitation of N and Si (ref.208). A trend towards larger
multicellular algae widespread
in marine, brackish and
                                 loads2,145,193.                                                phytoplankton cell sizes, such as diatoms, in response
freshwater environments,             The contribution of groundwater-​borne nutrients to        to SGD was noted in Hawaiian coastal waters receiving
which are referred to as         coastal ocean budgets will likely increase as human activity   fresh SGD209. However, it is clear that increased primary
macrophytes to distinguish       in coastal watersheds increases181. Climate-​change-           production resulting from SGD nutrient supply does not
from unicellular algae
                                 derived alterations of precipitation and evapotranspi-         always exert a positive response in the ecosystem (Fig. 6).
(phytoplankton).
                                 ration regimes, as well as land-​use change, are known         Dinoflagellate and cyanobacteria blooms can occur when
                                 to modify the quantity, the quality and the availability       ammonium is present in SGD or when inorganic nitro-
                                 of groundwater resources203. Climate-​driven sea-​level        gen is transformed by diatoms into organic nitrogen210.
                                 rise is also known to modify SGD and biogeochemical            As observed in Korea211,212 and Florida (USA)213, SGD
                                 cycling within coastal aquifers, and will likely affect the    can trigger, fuel and sustain harmful algal blooms, with
                                 magnitude of SGD-​driven nutrient inputs56,64 and its          devastating consequences to coastal ecosystems. In some
                                 impact on coastal biological communities. However,             cases, however, no response was found near sites receiv-
                                 long-​term quantitative predictions about the effects of       ing fresh groundwater springs, indicating that SGD
                                 climate change on SGD are unavailable.                         loading does not always induce an increase in primary
                                                                                                productivity214.
                                 Biological impacts of SGD nutrients                                Macrophyte cover can increase or decrease in response
                                 Research on how SGD nutrients impact marine biota has          to SGD. The most studied macrophyte in a SGD con-
                                 increased in recent years204, with nearly 90% of all arti-     text are Ulva spp., a leafy alga commonly known as
                                 cles on this topic having been published in the last dec-      sea lettuce, which grows faster and increases in abun-
                                 ade (see the supplementary material). The documented           dance in response to SGD-​derived nitrogen inputs191,215.
                                 response of marine organisms to SGD is quite variable          Moreover, nitrogen-​rich SGD can also increase the N:P
                                 and site-​specific, and can be positive or negative from       ratio in macrophyte tissues, which can reduce herbivory
                                 species, community or ecosystem perspectives (Fig. 6).         because fish prefer macrophytes with lower N:P ratios216.
                                 The response to SGD is sometimes unclear and could             However, macrophytes can also reduce reproduction to

                                                                                                         Response to SGD nutrients
                                                         Biological response                       Increase      Decrease         Unclear/mixed

                                 Species scale           Organism abundance                           17                2                    9
                                                         Growth and biomass                            9                1                    2
                                                         Tissue N:P ratio                              5                1                    2
                                                         Disease                                       1                –                    –
                                 Community scale         Richness                                      1                1                    1
                                                         Chlorophyll a                                20                –                    6
                                                         Diversity                                     3                5                    2
                                                         N sourcing                                   21                –                    1
                                                         Benthic density                               –                1                    3

                                 Ecosystem scale         Productivity/photosynthesis                  11                –                    2
                                                         Respiration                                   2                1                    1
                                                         Anoxia/deoxygenation                          1                –                    –
                                                         Calcification                                  3                1                    –

                                 Fig. 6 | the biological impacts of SGD. The table counts the number of studies demonstrating responses at the species,
                                 community and ecosystem scales to submarine groundwater discharge (SGD). SGD can drive multiple biological
                                 responses, depending on local conditions. The original references are summarized in the supplementary online material.

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Acid sulfate soils                prioritize growth and take advantage of a nitrogen-​rich          which was observed off a Korean volcanic island with
Naturally occurring soils         environment created by SGD217. In Hawaii, for instance,           large, fresh SGD inputs244. Alternatively, high CO2 from
usually found in coastal          oligotrophic waters receiving N-​enriched SGD had                 sediment organic matter decomposition54,245,246 or H2SO4
wetlands with a high content of   increased macroalgae coverage from
Reviews

Table 1 | a summary of key research topics that require further investigation in the field of submarine groundwater discharge
topic             research question         major obstacles and challenges                   research priorities                                    Key
                                                                                                                                             references
Fresh vs saline   What are the local and    Geochemical tracer investigations often          Combine tracers and other approaches                 51,79,112

SGD               global contributions      quantify total SGD. Multiple techniques are      to quantify both fresh and saline
                  of fresh vs saline SGD    required to separate fresh from saline SGD.      SGD. Integrate marine and terrestrial
                  and new vs recycled                                                        investigations. Adopt a nomenclature that
                  nutrients?                                                                 better represents the different processes.
Spatial and     What are the temporal       Models quantify specific driving forces,         Understand the role of spatio-​temporal            31,34,56,120

temporal scales and spatial scales          whereas geochemical tracers integrate            heterogeneity in regional-​scale estimates
                represented by specific     multiple processes on timescales                 to allow predictions in space and time.
                SGD estimates?              comparable to the tracer residence time.
Nutrient        What biogeochemical         Defining the nutrient endmember in SGD           Identify how microbial communities drive           145,148,266

transformations processes control           requires understanding of sources and            nutrient cycling. Quantify the effect of
                nutrient transformation     pathways. Transformations are governed by        subterranean estuaries in regional-​scale
                in the subsurface?          dynamic hydrological and biogeochemical          land–ocean nutrient budgets.
                                            processes at multiple scales.
Long-​term      How will ongoing            Poor quantitative understanding of drivers       Make long-​term observations. Enhance              193,203,267

observations    climate change,             of SGD. No straightforward typological           collaborations with climate change experts
and predictions sea-​level rise and         classification is available for both fresh and   and modellers to estimate uncertainty and
                land-​use intensification   saline SGD. Case studies often represent         improve the compatibility between
                modify SGD?                 snapshot estimates.                              observations and predictions.
Spatial bias      Is our current            Ongoing focus on areas of known SGD,             Quantify SGD in poorly represented regions.              66,67

                  knowledge of SGD          such as visible springs or locations with        Representative regional-​scale quantification
                  biased owing to           polluted groundwater. Poorly represented         of SGD to understand occurrence,
                  spatial gaps and          areas (such as South America, Africa and         heterogeneity and/or patchiness.
                  site selection?           the poles).
Management        How can SGD               Groundwater and surface water often seem Promote outreach activities and exchange                   138,170,232

                  be incorporated           disconnected. SGD perceived to be a highly knowledge on SGD with society and local/
                  into water quality        specialized research niche.                regional managers. Develop best-​practice
                  management plans?                                                    recommendations for management.
Biological        Is supply of nutrients    SGD effects are complex and site-​specific.      Include biota assessments in SGD studies.          204,215,216

effects           via SGD beneficial        Most investigations focus on individual          Explore effects of SGD from the base of
                  or harmful to marine      species or small-​scale organisms.               food webs through the entire ecosystem.
                  ecosystems?                                                                Use manipulative experiments to explore
                                                                                             biological effects.
Uncertainties     What are the              Uncertainties of methods used to derive          Report real uncertainties in SGD estimates,              70,75

                  uncertainties             SGD are difficult to constrain and often not     including errors in model conceptualization.
                  associated with local     reported. Uncertainties linked to spatial or     Apply mathematical methods to express
                  and global SGD            temporal integrations are unknown.               uncertainties based on unavertable
                  estimates?                                                                 limitations in the representation of SGD.

                            For example, the flow of groundwater from a large                been shown to be particularly high in urbanized areas
                            septic system in California (USA) has been managed               in developing countries such as Indonesia 194, the
                            to prevent pollution of popular swimming beaches256              Philippines261 and China172. Because SGD can enhance
                            affected by groundwater-​borne faecal contamination257.          primary productivity and fish abundance229,230, it would
                            Engineering solutions have been attempted to reduce              also connect to Goal 2 ‘Zero Hunger’ (Target 2.3), par-
                            fresh SGD and secure onshore groundwater use. In par-            ticularly in the context of regional-​scale fisheries that
                            ticular, attempts to close karstic caves or tap subma-           are sometimes sustained by SGD-​d erived nutrient
                            rine springs were made in the French Mediterranean               inputs231. SGD affects artisanal fisheries in small-​island,
                            coast 258. In China’s Bohai Sea, underground con-                tropical developing countries262, where fresh SGD is
                            crete dams were constructed to prevent connections               also especially relevant66,69. Interventions like China’s
                            between seawater and fresh groundwater, reducing SGD             underground dams that are intended to increase drink-
                            and seawater intrusion, and improving local freshwater           ing water availability also link SGD management to
                            availability259.                                                 Goal 6’s Target 6.4 to “ensure sustainable (water) with-
                                SGD is relevant to a wide range of the United Nations        drawals” and Target 6.6 to “protect and restore (fresh-)
                            Sustainable Development Goals. For example, SGD con-             water-​related ecosystems” that could exist around
                            nects clearly to Goal 14 ‘Life Below Water; and Target           submarine springs 263. Through sustaining marine
                            14.1 to reduce pollution in marine ecosystems. Hence,            ecosystems as well as releasing alkalinity and carbon
                            SGD-​derived nutrient fluxes should be considered par-           dioxide to surface waters264, SGD is relevant to Goal 13
                            ticularly when sensitive coastal ecosystems degrade194 or        ‘Climate Action’.
                            during coastal development modifying groundwater–                    The cultural value of places is traditionally recog­
                            surface water connectivity, such as the construction             nized in planning and legislation. In addition to
                            of drains and canals260. Nutrient fluxes via SGD have            apparent links to the Sustainable Development Goals,

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                                     SGD also has local cultural relevance232. Many subma-                          how it contributes to coastal nutrient budgets, a number
                                     rine springs have significant spiritual value and relate                       of major research questions remain open (Table 1).
                                     to local legends. For example, the magical Hawaiian sea                           Our growing knowledge in the last decade shows
                                     turtle Kauila has been told to have dug local springs for                      that considering SGD is clearly essential for developing
                                     its offspring. The Kaurna Aboriginal people in Australia                       coastal and marine nutrient budgets on local and global
                                     tell of Tjilbruke, a magical spirit who wept at the beach                      scales. About 60% of the reviewed investigations revealed
                                     and made the springs flow. In Bali, the Tanah Lot tem-                         that total SGD-​derived nutrient fluxes exceed rivers on
                                     ple, which was built on a submarine spring to worship                          local, regional or global scales. However, SGD studies are
                                     a magical being (Dang Hyang Nirartha) that moved the                           generally site-​specific and fixed in time, without predic-
                                     spring from land to the sea, attracts around 2 million                         tive power. Climate and land-​use change are expected
                                     visitors annually232. We do not know the abundance of                          to modify patterns of global water use, drive sea-​level
                                     such cases, since the cultural significance of SGD has not                     rise, push or pull seawater into coastal aquifers and
                                     been documented in detail.                                                     modify the chemical composition of groundwater93,203.
                                         The connections to multiple Sustainable Development                        Combined, these changes are expected to modify fresh
                                     Goals and their cultural relevance illustrate the complex-                     and saline SGD. A better understanding of SGD fluxes,
                                     ity with which SGD can be intertwined to livelihoods.                          drivers and pathways is essential for determining the
                                     These connections should justify the assimilation of                           carrying capacity of coastal seas and their response to
                                     SGD into coastal management plans, but assimilation                            increased anthropogenic pressures (Table 1). Nutrient
                                     has seldom occurred. A more integrated approach con-                           budgets considering SGD are required for the effective
                                     sidering SGD, not only rivers, is needed to maximize                           interpretation of natural and anthropogenic sources,
                                     coastal water quality management outcomes250. The slow                         as well as creating management solutions in highly
                                     movement of SGD relative to rivers implies that current                        modified coastal systems.
                                     contaminant and nutrient flows reflect past inputs, and                           Large investments have been made on the mitigation
                                     management approaches must prepare for increasing                              of coastal eutrophication and the protection of marine
                                     loads in the decades to come93.                                                biodiversity. However, recent reductions in river and
                                                                                                                    atmospheric nutrient inputs in developed countries
                                     Summary and outlook                                                            have not been enough to reduce coastal eutrophication
                                     Quantifying SGD-​derived nutrient fluxes is challeng-                          and related hypoxic events in key areas such as the Baltic
                                     ing and involves nuanced assumptions and interpre-                             Sea7, the shelf off the Mississippi River265 and the China
                                     tations, and a wide range of skills in oceanography,                           coast172. As SGD fluxes, pathways and drivers are better
                                     hydrology and biogeochemistry. A disciplinary frag-                            understood, it will be possible to detect how changes in
                                     mentation, time lags in groundwater flows and slow                             SGD relate to disturbances such as land-​use change,
                                     management responses have created barriers to scientific                       habitat clearing and climate change.
                                     progress and incorporation of SGD in coastal nutrient
                                     budgets. To further build the SGD field and understand                         Published online xx xx xxxx

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