Breathing of a coral cay: Tracing tidally driven seawaterrecirculation in permeable coral reef sediments

Isaac R. Santos,1 Dirk Erler,1 Douglas Tait,1 and Bradley D. Eyre1

Received 8 July 2010; revised 29 August 2010; accepted 7 September 2010; published 3 December 2010.

[1] Coral reefs are characterized by high gross productivity in spite of low nutrientconcentrations. This apparent paradox may be partially reconciled if seawater recirculationin permeable sediments over large (meters) and long (hours to days) scales is an importantsource of recycled nitrogen and phosphorus to coral reefs. In this paper we use radon(222Rn, a natural tracer) to quantify tidally driven pore water (or groundwater) exchangebetween (1) an offshore coral cay island and its fringing reef lagoon and (2) a reeflagoon and the surrounding ocean. As seawater infiltrates Heron Island at high tide, itacquires a radon signal that can be detected when pore waters emerge from carbonatesands at low tide. A nonsteady state model indicated that vertical pore water upwellingrates (or saline submarine groundwater discharge) were >40 cm/d within the reef lagoonand >100 cm/d outside the lagoon at low tide. Within the lagoon, tidal pumping andtemperature‐driven convection were the main driving forces of pore water advection. Atlow tide, the reef lagoon level is about 1 m higher than the surrounding ocean. As a result,a steep hydraulic gradient develops at the reef edge, driving unidirectional filtrationthrough the reef framework. Groundwaters were highly enriched in nitrate (average of 530mmol, likely influenced by bird guano) relative to lagoon waters (1.9 mmol). Rough butconservative estimates indicated that groundwater‐derived nitrate fluxes (7.9 mmol/m2/d)can replace the entire lagoon nitrate inventory every <19 days. We speculate that asoffshore coral islands “breath” (inhale seawater at high tide and exhale groundwater at lowtide), they release nutrients that lead to sustained productivity within coral reefs.

Citation: Santos, I. R., D. Erler, D. Tait, and B. D. Eyre (2010), Breathing of a coral cay: Tracing tidally driven seawaterrecirculation in permeable coral reef sediments, J. Geophys. Res., 115, C12010, doi:10.1029/2010JC006510.

1. Introduction

[2] Coral reefs are often characterized by extremely lownutrient concentrations, high gross productivity, and low netproductivity. The mechanisms by which coral reefs obtaintheir nutrients have been debated since Odum and Odum’s[1955] seminal paper. Efficient recycling of “new” nitrogenfrom nitrogen fixation and “new” phosphorus extracted fromlarge volumes of water flowing over reefs have been invokedto explain the apparent low‐nutrient high‐productivity par-adox of coral reefs [Alongi, 1998, and references therein].However, recent investigations have advanced the conceptthat permeable coral reef sediments act as biocatalytical filters,i.e., biogeochemical reactions are stimulated by the advectivetransport of oxygen and organic matter into sediments [Eyreet al., 2008; Wild et al., 2004]. This body of work hasrelied primarily on chamber incubations [Glud et al., 2008]and sediment cores [Werner et al., 2006] and focused on

processes occurring on spatial scales of cm and temporalscales of minutes to hours. We hypothesize that seawaterrecirculation in sediments over larger (i.e., meters) and longer(i.e., hours to days) scales is also important for organic matterrecycling in coral reefs.[3] Seawater recirculation in sediments over large scales

is included in the modern definition of submarine ground-water discharge (SGD). SDG is defined as “any and all flowof water on continental margins from the seabed to the coastalocean, regardless of fluid composition or driving force”[Burnett et al., 2003; Moore, 2010]. The terrestrial compo-nent of SGD (fresh SGD) is a source of new water andnutrients to the coastal ocean. In contrast, the marine com-ponent of SGD (saline SGD or seawater recirculation insediments) is not a source of new water but can be associatedwith dramatic changes in the chemical composition of theoriginal seawater [Santos et al., 2009b].[4] Recent SGD investigations in coral reefs have focused

primarily on Hawaiian nearshore systems and relied onradium isotopes to quantify water fluxes [Paytan et al., 2006;Street et al., 2008]. Because radium sampling can be labor‐intensive and requires the filtration of large volumes ofwater (typically about 100 L), those previous studies reliedon the assumption of steady state SGD fluxes. However,

1Centre for Coastal Biogeochemistry, School of Environmental Scienceand Management, Southern Cross University, Lismore, New South Wales,Australia.

Copyright 2010 by the American Geophysical Union.0148‐0227/10/2010JC006510

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tidal pumping and other seawater recirculation processesmay result in SGD rates to be highly variable over hourlytime scales [Santos et al., 2009a; Taniguchi et al., 2008].[5] The advent of new technology has allowed us to

perform automated, precise, and continuous radon (222Rn; anoble gas) measurements that can provide insights into thetemporal dynamics of fresh and saline SGD [Burnett andDulaiova, 2003]. Radon is an excellent natural groundwatertracer because it is often 2–4 orders of magnitude moreconcentrated in groundwater than surface waters, its half‐life(3.8 days) is on the same order as many coastal processes, andit is conservative except for exchange with the atmosphere[Cable et al., 1996; Swarzenski, 2007].[6] In this paper we use high‐resolution radon time series

measurements to quantify tidally driven groundwater (orpore water) exchange at Heron Island, an offshore system inthe Great Barrier Reef (GBR). We quantify the exchangebetween (1) the coral cay island and its fringing reef lagoonand (2) the reef lagoon and the surrounding ocean. Recentinvestigations in coral reefs mapped radon distributions toidentify potential SGD hotspots along the GBR nearshorezone [Stieglitz, 2005; Stieglitz et al., 2010] and in thePhilippines [Cardenas et al., 2010]. To our knowledge,this is the first investigation to quantify SGD into a GBRecosystem. We also provide preliminary estimates of SGD‐derived nutrient fluxes and speculate that this can play amajor role in coral reef biogeochemistry.

2. Material and Methods

[7] A series of field investigations were performed atHeron Island (23″ 27′S, 151″ 55′E) at the southern end ofthe Great Barrier Reef, Australia. The island is a true coral cay(800 m long, 200 m wide, 3 m high) located about 70 km offthe Australian mainland at Gladstone [see Wild et al., 2004,Figure 1]. Heron Island is surrounded by a shallow and pro-ductive reef lagoon (26 km2) dominated by corals of thegenus Acropora. The island and lagoon bottom are composedof coarse sands that allow seawater to readily flow in and outof the sediments. The sediments median grain size is 800 mm.Permeabilities (∼10−10 m2) and porosities (∼45%) are veryhigh and the organic carbon content (<0.2%) is very low.Living corals cover about 25% of the lagoon bottom [Wildet al., 2004, 2006].[8] Our experimental strategy consisted of performing high‐

resolution radon time series measurements to assess how tidalfluctuations can drive groundwater (or pore water) exchange.In August 2009 (winter) and February 2010 (summer), amoored station was deployed for at least 24 h at two sites:(1) inside the reef lagoon about 10 m off the island to quantifyisland‐lagoon exchange and (2) outside the reef lagoon withina sheltered harbor to quantify lagoon‐ocean exchange throughthe reef framework. The harbor is separated from the lagoonat low tide but connected to the open ocean at all times. Thisprovided excellent experimental conditions as we would notbe able to deploy a radon monitor in wavy open waters. Inaddition, vigorous mixing in open waters would likely pre-vent a radon signal from being detected. In December 2009,we attempted to measure radon for 2 weeks within the lagoonin order to capture a spring‐neap tidal cycle.[9] Radon concentrations (1 h intervals) in seawater were

measured using a portable continuous radon‐in‐air monitor

modified for radon‐in‐water (RAD‐7, Durridge Company)[Burnett et al., 2001]. This system is based on the equili-bration of a stream of flowing water with a stream of air thatis recirculated through an air‐water exchanger and theRAD‐7. The radon equilibration partitioning between thegas and the liquid phase is temperature dependent, so wedetermine the solubility coefficients based on continuoustemperature measurements.[10] Water depths were monitored using a water level

logger (Onset Hobo). Groundwater level, temperature, andsalinity monitoring was conducted using a conductivity‐temperature‐depth diver (Van Essen Instruments®). Windspeeds were determined using a handheld anemometer. Theconcentrations of 226Ra were determined after samplingwith Mn fibers and using a RAD‐7 [Peterson et al., 2009a].Groundwater samples were collected from several wells tocharacterize the radon end‐member concentration. We alsoperformed a 24 h time series in a 7.5 m deep well locatedabout 2 m onshore of the high‐tide mark. Pore water sam-ples were collected using a push‐point piezometer system[Charette and Allen, 2006]. Although we consider pore watera synonym of groundwater [Burnett et al., 2003], here porewater is referred to as the samples collected from submergedlagoon sediments. Groundwater is referred to as the samplescollected from wells on the island.[11] Reef lagoon seawater, island’s groundwater, and reef

lagoon pore water samples were immediately filtered using0.45 mm syringe filters and frozen for nutrient analysis.Ammonium (NH4

+), nitrate + nitrite (NOx), and orthophos-phate (PO4

3−) concentrations were determined colorimetricallyusing a Lachat Flow Injection Analyser (see Eyre andFerguson [2005] for method details, errors, and detectionlimits). Hereafter, the NOx results are referred to as nitrate.Dissolved oxygen concentrations (±0.01 mg/L) and pH(±0.001 units) were measured electrochemically (Hatch 40DLDO Sensor).[12] We applied a nonsteady state radon mass balance to

estimate groundwater (or pore water) advection rates (inunits of cm/d or cm3/cm2/d). A detailed description of thismodel can be found elsewhere [Burnett and Dulaiova,2003]. Briefly, the temporal variability of 222Rn invento-ries in the water column is assumed to be balanced by itssources (groundwater, 226Ra decay, and diffusion fromsediments) and sinks (atmospheric evasion, decay, andmixing with offshore waters). Radon losses to the atmo-sphere were calculated as a function of wind speed and air‐sea concentrations gradients [Dulaiova and Burnett, 2006].The mixing losses were estimated from inspection of thenet radon fluxes over time, i.e., residual negative fluxesafter accounting for other losses were assigned tomixing withlow concentration offshore waters. Assuming that benthicfluxes of radon are driven mainly by groundwater inputs, weestimated groundwater advection rates by dividing the total222Rn fluxes by the estimated groundwater end‐memberconcentration.

3. Results

3.1. Groundwater Observations

[13] Heron Island groundwater was highly dynamic overtidal time scales (Figure 1), reflecting active exchangebetween the island and the reef lagoon. The groundwater

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tidal range was 0.40 m during the neap tide and 0.64 mduring the spring tide. The reef lagoon tidal ranges, in turn,were 1.39 m during neap tide and 2.04 m during springtides. Groundwater levels lagged lagoon high tides by 3 h andlagoon low tides by 1 h. Although temperatures in lagoonwater were variable as a result of day‐night cycles, ground-water temperatures were nearly constant at 25.3°C. In contrast,reef lagoon water salinities were constant and groundwatersalinities ranged from 18.8 to 23.8 during every tidal cycle.[14] Radon concentrations in groundwater (Table 1) were

low relative to more continental sites [Burnett et al., 2006]probably as a result of high water:sediment ratios in HeronIsland’s porous and coarse carbonate sediments. The lowestconcentrations were observed in two wells located 2 monshore of the high‐tide mark. The mixing of low radonlagoon water with high‐radon island groundwater was illus-trated by a 24 h time series in one of those beach groundwaterwells (Figure 2). We observed a dramatic variability in radonconcentrations in groundwater extracted from this well duringa tidal cycle, which represents a challenge for applying aradon mass balance (see below). The low radon concentra-tions at high tide are a result of seawater infiltration intobeach sediments. A twofold increase in radon concentrationat low tide can be explained by rapid seaward advection ofgroundwater from themiddle of the island. If simple ingrowthfrom sediments surrounding the well was the main radonsource at low tide, it would take 3.8 days (one half‐life) forradon to double its concentrations at a given spot. In contrastto groundwater in the middle of the island (Figure 1), thetidal range in beach groundwater was almost as large as thelagoon tidal range (Figure 2). The beach groundwater levellagged the lagoon level by less than 1 h.

[15] Nitrate concentrations in groundwater were extremelyhigh (Table 1). The ammonium concentrations were lowexcept for an outlier (sample GW 12). The average reeflagoon seawater concentrations for NOx, NH4

+, and PO43−

were 1.9, 0.6, and 0.2 mmol, respectively (n = 5). Hence,groundwater nitrate concentrations are 2–3 orders of mag-nitude higher than reef lagoon waters. The shallow porewater samples (presumably away from the direct influenceof island groundwater) had nitrate concentrations comparableto surface waters, but the ammonium values were 1 order ofmagnitude higher.

3.2. Radon Time Series Within the Reef Lagoon

[16] Radon concentrations in the reef lagoon water werehighly variable over hourly time scales (Figure 3), implyingsignificant tidally driven groundwater exchange at HeronIsland. In general, radon starts increasing during the ebb tide,reaches a peak 2–3 h after the lowest tide, and decreases aslow concentration ocean waters flood the lagoon. The con-centrations in seawater were usually threefold higher at lowtide than at high tide. These 12 h cycles were consistentduring the winter and summer experiments, implying a minorseasonal variability in groundwater‐lagoon exchange. In thesummer, constant and strong winds stripped all the radonout of lagoon water, preventing a tidal signal from devel-oping during the first 30 h of observations (Figure 3b). The

Figure 1. Time series of groundwater and lagoon waterlevel, temperature and salinity in December 2009. Thegroundwater data is from a 6.5‐m deep well located in themiddle of the island (sample GW 7 in Table 1). The leveltime series were zero‐averaged.

Figure 2. Beach groundwater and lagoon temperature andlevel time series, and radon in beach groundwater. Thegroundwater observations are from a 7.5 m deep groundwaterwell located 2 m onshore of the high tide mark. The level timeseries were zero‐averaged.

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modeled SGD advection rates followed a trend similar toradon concentrations, with advection rates as high as 40 cm/dtoward the end of the low tide or beginning of flood tide. Anumber of channels (usually about 10 cm deep, up to 20 cmwide) were evident on the beach at low tide. These channelsare erosive features that develop during the “breathing” ofthe island (seawater infiltration at high tide, discharge atlow tide).

3.3. Radon Time Series Outside the Reef Lagoon

[17] Although the radon dynamics outside the lagoon alsofollowed a clear tidal pattern (Figure 4), we observed severaldifferences relative to the patterns within the reef lagoon:(1) the peak concentrations outside the lagoon were not aslagged relative to low tides as they were within the lagoon,(2) the highest radon concentrations were almost twofoldhigher outside the lagoon than within the lagoon, (3) themodeled advection rates were much higher outside the lagoon,and (4) the advection peak occurred exactly at the lowesttide and was wider outside the lagoon. All these differ-ences can be explained by the different mechanisms driv-ing groundwater exchange at the two sites and by the waytides operate within and outside the reef lagoon. At HeronIsland, the tidal range in the open ocean is about 1 m greaterthan within the lagoon. As a result, a very steep hydraulicgradient develops between the reef lagoon and the openocean at low tide. This gradient induces significant filtrationof lagoon water through the reef framework toward the openocean around the reef edge.

3.4. Spring‐Neap Tidal Cycle Within the Reef Lagoon

[18] We attempted to monitor radon uninterruptedly forapproximately 2 weeks in December 2009 in order to gaininsights into how a spring‐neap tidal cycle might influence

groundwater exchange processes between the island and thereef lagoon. However, reliable results were obtained onlyduring the first 4 days and the last 3 days of this experiment(Figure 5). In general, these results were similar to thewinter and summer reef lagoon time series described above.A unique feature in December was that radon tended not todecrease during the low high tide, leading to an apparent24 h cycle inversely related to lagoon water temperatures(rather than the 12 h cycles described above). The modeledadvection rates in December, however, still depicted thedominant 12 h cycles typical of all experiments, demonstratingthat tidal pumping controls most of the exchange within thereef lagoon.[19] No obvious relationships between advection rates and

tidal amplitudes were observed, perhaps because of a 5 daydata gap during this experiment. The gap in radon data wasrelated to a coral mass spawning event that occurred on8 December 2009. In order to quantify radon, we continu-ously pump water at 3 L/min into a water‐air exchanger.Although the air is pumped into the radon monitor in aclosed loop, seawater flows through the exchanger. Spawningevents dramatically increase the concentration of dissolvedorganic matter in the reef lagoon [Wild et al., 2008]. Organic‐rich water foams when subject to turbulence within theexchanger. As a result, the exchanger level raises, preventingradon measurements from being made. About 5 days after thespawning event, organic‐rich waters had completely dissi-pated, allowing us to resume continuous radon observations.

4. Discussion

4.1. Uncertainties in the Radon Mass Balance

[20] Defining the proper groundwater (or pore water) end‐member concentration is the main uncertainty in our non-

Table 1. Concentrations in Groundwater and Pore Water Samplesa

ID DateDepth(m)

Distance(m) Description

222Rn(dpm/L) pH Salinity

Temp.(°C)

NH4

(mmol/L)NOx

(mmol/L)PO4

(mmol/L)

GW 1 27/2/10 7.5 2 North beach 12.4 ± 3.9 7.04 35.9 26.8 0.1 58.3 1.0GW 2 27/2/10 3.5 2 North beach 4.6 ± 2.9 7.31 36.4 27.1 0.1 47.1 1.3GW 3 27/2/10 9 110 Forest walking trail 62.4 ± 16.7 7.05 29.9 25.4 0.2 1280.1 3.2GW 4 27/2/10 7 110 Forest walking trail 70.7 ± 8.3 6.91 28.8 25.2 0.2 1317.9 3.2GW 5 27/2/10 7 110 Forest walking trail 50.3 ± 9.7 6.90 29.3 26.6 0.2 736.3 5.0GW 6 27/2/10 >12 110 Forest walking trail 103.7 ± 25.5 6.88 29.1 25.1 0.2 754.5 3.2GW 7 28/2/10 6.5 80 Boat shed 28.4 ± 9.9 6.97 25.4 25.8 0.2 749.3 3.6GW 8 1/3/10 8 115 Maintenance building 69.5 ± 20.6 7.00 21.4 26.7 0.3 292.1 4.0GW 9 1/3/10 4.5 115 Maintenance building 10.4 ± 10.2 7.20 2.1 29.0 2.5 315.0 3.0GW 10 1/3/10 12 105 Staff house – 7.05 24.1 26.6 0.9 886.7 3.4GW 11 2/3/10 11 92 Petrol pump 26.3 ± 8.8 6.72 28.2 27.9 0.1 0.2 2.3GW 12 2/3/10 12 92 Petrol pump 33.1 ± 8.5 6.68 27.1 27.8 203.3 1.9 21.8Average 42.9 6.98 26.5 26.7 17.3 536.6 4.6Standard error 9.8 0.05 2.5 0.3 16.9 139.5 1.6

PW 1 1/3/10 0.4 −30 Shark bay 7.4 ± 4.4 – – – – – –PW 2 1/3/10 0.5 −32 Shark bay 7.8 ± 6.9 – – – – – –PW 3 1/3/10 0.5 −34 Shark bay 7.2 ± 2.3 – – – – – –PW 4 3/3/10 0.2 −20 Reef lagoon 9.3 ± 5.2 7.89 36.7 25.6 12.1 1.7 1.3PW 5 3/3/10 0.3 −60 Reef lagoon 10.6 ± 4.7 7.83 36.7 25.5 19.3 0.3 1.0PW 6 3/3/10 0.2 −65 Reef lagoon 5.3 ± 3.4 8.01 36.7 25.7 3.5 1.7 0.4Average 7.9 7.91 36.7 25.6 11.6 1.2 0.9Standard error 0.7 0.04 8.2 0.0 3.2 0.3 0.2

aDepth values are below ground value and not necessarily relative to the same vertical datum. “Distance” refers to the approximate horizontal distancefrom the high‐tide mark. The pore water (PW) samples were collected in the subtidal area within the reef lagoon. The average nutrient concentrations ingroundwater (GW) samples GW 1 and GW 2 (the samples located closest to the reef lagoon) were used to estimate fluxes. Here 27/2/10 is read as 27February 2010.

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steady state radon mass balance [Burnett et al., 2007;Dulaiova et al., 2008; Peterson et al., 2009b; Santos et al.,2009a]. Because the radon fluxes (1 h intervals) are dividedby the groundwater end‐member concentration, a change inthis radon end‐member leads to a corresponding but inversechange in pore water advection rates. In order to minimizeuncertainties in the end‐member concentration, one shouldrely on a large number of samples in the area immediatelyprior to the seepage face. In this paper we used the averageradon groundwater concentration (42.9 ± 9.8 disintegrationsper minute [dpm]/L) (Table 1) as the end‐member for mod-eling advection rates.[21] By using the average groundwater concentration, we

are likely providing minimum advection rate estimates.Groundwater radon concentrations in groundwaters nearthe beach were much lower than the average (Table 1) butlikely represent the most important source of radon to thereef lagoon. If the average concentration during the beachgroundwater time series (Figure 2) was used, the radonend‐member concentration would decrease by half, whichwould double the modeled advection rates. Another sourceof uncertainty is related to the temporal variability in radonconcentrations in beach groundwater. Ideally, one should

perform concomitant groundwater and surface water mea-surements, which was not possible during this study.

4.2. Driving Forces of Groundwaterand Pore Water Advection

[22] What physical processes are generating the strongradon signal detected within and outside the reef lagoon? Theradon half life is 3.84 days, so about 20 days are needed forradon in groundwater to fully equilibrate with its sur-rounding sediments. If it is assumed that the local sedimentsare homogeneous and the highest radon concentration ingroundwater (GW 6, the deepest sample; 222Rn = 104 dpm/L)represents a fully equilibrated sample, the time since seawaterinfiltrated these sediments can be roughly estimated. Thisexercise implies that the residence time of the groundwatersamples ranges from several hours (beach groundwaters) to amaximum of 5 days. The average radon concentration inreef lagoon pore waters was only 8 dpm/L, so the residencetime of shallow pore waters would be <10 h.[23] In nearshore systems, radon often traces a mixture of

fresh and saline groundwater [Mulligan and Charette, 2006].At Heron Island, radon seems to be tracing only a recirculatedseawater component (or saline SGD). The remarkable tem-

Figure 3. Temperature, depth, radon and modeled advection rates within the reef lagoon in the winterand summer.

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poral variability in groundwater salinity (Figure 1) indicatesthat a thin freshwater lens floats on top of a denser salinewater layer. The greater tidal range in beach groundwater(Figure 2) relative to island groundwater (Figure 1) appar-ently creates a hydraulic plug that prevents most of thefreshwater lens from immediately draining into the lagoon.This is similar to the beach water table superelevationconcept described by Turner et al. [1997].[24] Seawater recirculation in permeable sediments can

result from several mechanisms: (1) flow‐induced andtopography‐induced pressure gradients [Huettel et al., 2003],(2) wave setup on beaches [Li and Barry, 2000], (3) bioirri-gation [Martin et al., 2006], (4) wave pumping [King et al.,2009], (5) tidal pumping [Li et al., 2009], (6) temperature‐driven convection [Moore and Wilson, 2005], and (7) sea-sonal shifts in the freshwater‐saltwater interface driven bychanges in the water table on land [Michael et al., 2005]. Thefew previous quantitative hydrological investigations incoral reefs were based primarily on artificial tracers that donot distinguish between those driving mechanisms. Forexample, at Davies Reef (Great Barrier Reef), dye tracerexperiments implied that pore water velocities may reach

10 m/d [Oberdorfer and Buddemeier, 1986]. Since processes1–4 occur on time scales of seconds to minutes, they areunlikely to generate a detectable radon signal. The similaritybetween our winter and summer observations imply thatseasonal shifts in the freshwater‐saltwater interface is not amajor mechanism at Heron Island.[25] The radon signal within the lagoon is likely to have

been a result of tidal pumping and temperature‐driven con-vection (Figure 6). Although tidal pumping is clearly thedominant process, convection cannot be ruled out as a sourceof radon. The pore waters of the shallow reef lagoon arelikely to warm up during daytime. At night, surface watersprobably cool off faster than pore waters, creating densityinstability that can drive pore water upwelling. Rocha [2000]demonstrated that this process can dominate benthic fluxesin a sandy tidal flat in Portugal. Unfortunately, we did notcollect information on shallow pore water temperatures atHeron Island to test whether density inversions occurredwithin the reef lagoon at night. However, radon concentra-tions tended to be higher at night in December 2009. Inaddition, the modeled advection rates at the nighttime hightide are often higher than the daytime high tide, especially in

Figure 4. Temperature, depth, radon and modeled advection rates outside the lagoon in the winter andsummer. Notice that the winter time series lasted 1 day, while the summer time series lasted 1.4 days.

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the last 3 days of observations when diel temperature fluc-tuations were more pronounced (Figure 5). We thus suspectthat there is a convection signal overlapping the dominanttidal pumping signal within the reef lagoon.[26] The seepage observed outside the reef lagoon is a

special case of tidal pumping. At low tide, the reef lagoonlevel is about 1 m higher than the surrounding ocean level.Coral frameworks and sands between the corals are charac-terized by extremely high permeabilities [Huettel et al.,2006]. Hence, steep hydraulic gradients associated withhigh permeabilities can drive an extremely fast unidirectionalpore water flow through the reef framework all around thelagoon. The relatively higher radon concentrations outsidethe lagoon may be due to a subterranean “cascading” effect inwhich radon‐enriched lagoon waters are further enrichedduring transit through the reef lagoon framework. The shortresidence time of pore water associated with this process mayprevent significant radon build up. Hence, our groundwaterobservations are likely an overestimation of the end‐memberassociated with this unidirectional filtration, which leads tounderestimated advection rates outside the lagoon.

4.3. Biogeochemical Implications

[27] If we simply multiply the average nutrient con-centrations in beach groundwater (samples GW 1 and 2,the lowest nitrate concentrations in groundwater samples)(Table 1) by the average radon‐derived advection rates withinthe lagoon during the time series investigations (∼15 cm/dor 150 L/m2/d), we obtain SGD nitrate, ammonium, andphosphate fluxes into the reef lagoon of 7.91, 0.02, and0.17 mmol/m2/d, respectively. The nitrate fluxes are amongthe highest ever observed in coastal environments as a resultof both high SGD rates and elevated nitrate concentrationsin the groundwater end‐member (see a comparison table bySlomp and Van Cappellen [2004]).[28] The aerial extent of these fluxes is difficult to esti-

mate, but they are likely comparable to the size of the island(0.24 km2) yielding total SGD nitrate fluxes of about 2 ×103 mol/d into the reef lagoon. Considering the reef lagoonarea (26 km2), average depths (0.74 m during a tidal cycle),and average nitrate concentrations (1.9 mmol), we estimatea reef lagoon nitrate inventory of 37 × 103 mol. Hence,

Figure 6. Conceptual model summarizing the processes discussed here across a coral cay island‐reeflagoon‐open water transect. Distances are not to scale.

Figure 5. Temperature, depth, radon and modeled advec-tion rates within the reef lagoon in December 2009. Noticethe X axis scale brake due to equipment malfunctioning.

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SGD‐derived fluxes can replace the inventory of nitrate inthe entire reef lagoon every <19 days. In spite of largeuncertainties associated with nutrient transformations alongthe transport pathway [Santos et al., 2008], these high fluxesillustrate the magnitude of the process under investigation.Although these are rough calculations, they likely under-estimate the importance of SGD for a number of reasons:(1) our radon‐derived SGD rates are minimum values, (2) ourselection of the groundwater nitrate concentration likelyrepresents minimum values, and (3) the assumption aboutthe seepage area (equal to island’s area) overlooks the factthat temperature‐driven convection can occur throughoutthe entire lagoon.[29] Recent investigations in permeable coral reef sedi-

ments have relied primarily on benthic chambers that simu-late how flow‐induced and topography‐induced pressuregradients stimulate organic matter mineralization [Eyre et al.,2008; Glud et al., 2008; Wild et al., 2005]. This mechanismdrives pore water flows on time scales of minutes and spatialscales of centimeters [Huettel et al., 2003]. As a result,oxygen may be only partially consumed when seawater isrecirculated in permeable sediments driven by flow‐inducedand topography‐induced pressure gradients. The longerspatial and temporal scales associated with tidal pumpingmay allow oxygen exhaustion and a complete mineralizationof seawater organic matter infiltrated in sediments. Althoughmuch lower dissolved nitrogen fluxes have been observed,this process likely occurs over a much larger area than tidalpumping (the lagoon area is ∼100‐fold larger than theisland’s area). Using in situ advective chambers, Eyre et al.[2008] observed net ammonium effluxes from HeronIsland’s permeable sands of <10 mmol/m2/d. Phosphatefluxes approached zero, and nitrate and dissolved organicnitrogen fluxes were negative (influx). When extrapolated tothe lagoon area and assuming that sediments cover 75% ofthe lagoon surface [Wild et al., 2004], flow‐induced andtopography‐induced pressure gradients likely release about195 mol/d of ammonium to the reef lagoon. These ammo-nium fluxes are 1 order of magnitude lower than our con-servatively estimated SGD‐derived nitrate fluxes.[30] Tidal pumping has been suggested to play an impor-

tant role as a nutrient recycling mechanism in other ecosys-tems. For example, in northern Florida, seawater recirculationinto the beach face releases about 4 mmol/m2/d of nitrogeninto the coastal ocean [Santos et al., 2009b]. In the GermanWadden Sea, tidal pumping seems to dampen temporalfluctuations in primary productivity by slowly but continu-ously recycling organic matter and releasing nutrients tonearshore waters [Billerbeck et al., 2006]. Because oxygencan be completely consumed, methanogenesis and otheranaerobic processes can play an important role respiringorganic matter [Røy et al., 2008].[31] External nutrient sources such as river runoff, atmo-

spheric deposition, and terrestrial fresh groundwater inputsare negligible in offshore coral reefs such as Heron Island.Hence, efficient internal recycling mechanisms must operateto sustain high gross coral reef primary productivity. Thenitrogen released as offshore islands “breath” (inhale sea-water and exhale groundwater) with tidal cycles are likelyderived from two main sources: (1) seawater organic matterremineralization and (2) bird guano. The metabolism ofpermeable sediments is largely stimulated by the advective

transport of large amounts of labile organic matter (phyto-plankton [Huettel and Rusch, 2000], coral mucus [Wildet al., 2004], spawning material [Eyre et al., 2008], etc). Theassociated constant supply of oxygen [Rusch et al., 2006], theextremely high microbial activities in pore waters [Pattenet al., 2008], and the large effective surface area of car-bonate grains [Wild et al., 2006] act together to enhanceorganic matter mineralization rates in permeable sediments.[32] In addition to this organic matter uptake →

mineralization → nutrient release sequence, tidal pumpingmay also transfer nutrients from bird guano to the reeflagoon. Considering the large bird densities in several atolls,coral cays, and oceanic islands, guano is likely to be a majorbut unquantified source of nutrients to nearby marine eco-systems. Seabirds deposit up to 1000 kg N ha−1 yr−1 onHeron Island [Schmidt et al., 2010]. Although part of guanonitrogen is likely to be lost during transit, extremely fast“breathing” rates driven by tidal pumping can potentiallydeliver a significant amount of guano nitrogen to coralreefs. Hence, we suggest that tidal pumping contributes tothe retention of nutrients (both from organic matter miner-alization and guano) within coral reef ecosystems. Differentreef configurations (fringing reefs, open lagoons, atolls, etc)are also likely to be influenced by tidal pumping as long aspermeable sediments are exposed at low tide.

5. Conclusions

[33] Figure 6 summarizes the processes discussed in thispaper. Although Heron Island groundwaters are tidal, thetidal range decreases with distance from the beach. A non-steady state radon mass balance model allowed us to estimatepore water upwelling rates (or saline submarine ground-water discharge) of >40 cm/d within the reef lagoon and>100 cm/d outside the reef lagoon at low tide. These areminimum estimates because of our selection of the radonend‐member concentration in groundwater. In addition, theseestimates do not include short and fast seawater recirculationmechanisms in permeable sediments such as flow‐inducedand topography‐induced pressure gradients. The “breathing”of Heron Island was driven by seawater infiltration into theisland at high tide and discharge at low tide. The radon signaloutside the reef lagoon was related to a unidirectional filtra-tion process though the reef framework that occurs as a resultof high hydraulic gradients at the reef edge at low tide.[34] Future investigations should assess how the physical

processes discussed here are responsible for the recycling oforganic matter and the release of nutrients. Because seepageoccurs at low tide when the reef lagoon is isolated from theopen ocean, the nutrients presumably released during the“breathing” process are likely retained within the lagoon.Considering the very fast rates of seawater recirculation inpermeable sediments and the shallow nature of reef lagoons,we suspect that tidally driven seawater recirculation in coralcays can be a major but overlooked factor controlling pro-ductivity in coral reefs.

[35] Acknowledgments. This project was supported by an AustralianResearch Council Discovery grant awarded to BDE (DP0878683) and aLinkage grant awarded to BDE, IRS, and DE (LP100200732). We thankthe staff of the Heron Island Research Station for invaluable support duringour field investigations. The title was inspired on Flip Froelich’s cave

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breathing work. Ronnie Glud and Damien Maher provided assistance duringfield investigations. Richard Peterson and two reviewers provided insightfulcomments.

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