Benthic fluxes of dissolved nutrients in reef communities
are controlled by oceanographic forcing, including local hydrodynamics and
seasonal changes in oceanic nutrient supply. Up to a third of reefs
worldwide can be characterized as having circulation that is predominantly
tidally forced, yet almost all previous research on reef nutrient fluxes has
focused on systems with wave-driven circulation. Fluxes of dissolved
nitrogen and phosphorus were measured on a strongly tide-dominated reef
platform with a spring tidal range exceeding 8 m. Nutrient fluxes were
estimated using a one-dimensional control volume approach, combining flow
measurements with modified Eulerian sampling of waters traversing the reef.
Measured fluxes were compared to theoretical mass-transfer-limited uptake
rates derived from flow speeds. Reef communities released 2.3 mmol m-2 d-1 of nitrate, potentially derived from the remineralization of
phytoplankton and dissolved organic nitrogen. Nutrient concentrations and
flow speeds varied between the major benthic communities (coral reef and
seagrass), resulting in spatial variability in estimated nitrate uptake
rates. Rapid changes in flow speed and water depth are key characteristics
of tide-dominated reefs, which caused mass-transfer-limited nutrient uptake
rates to vary by an order of magnitude on timescales of ∼ minutes–hours. Seasonal nutrient supply was also a strong control on reef
mass-transfer-limited uptake rates, and increases in offshore dissolved
inorganic nitrogen concentrations during the wet season caused an estimated
twofold increase in uptake.
Introduction
Reef organisms remove nutrients from overlying waters for essential
metabolic and biogeochemical processes, which enable them to accumulate
biomass and ultimately support broader marine food webs
(McMahon et al., 2016; Parrish, 1989). Reef waters have carbon
concentrations that are orders of magnitude greater than nitrogen (N) and
phosphorus (P), and thus benthic community productivity is generally limited
by the rates at which organisms can acquire N and P (Atkinson and Falter,
2003; Larned, 1998; Smith, 1984). Suspended N and P can be categorized into
dissolved inorganic (DIN, DIP), dissolved organic (DON, DOP), and
particulate organic (PON, PP) fractions, which are generally utilized by
different groups of organisms. Primary producers take up dissolved inorganic
nutrients in the forms of nitrate and nitrite (NOx), ammonium
(NH4+), and phosphate (DIP), which are found at low concentrations
in reef waters.
The majority of studies on reef nutrient dynamics have focused on the
dissolved inorganic species, as these are tightly coupled to reef
productivity (D'Elia and Wiebe, 1990; Szmant, 2002). Research over the
last 2 decades has shown that the upper limit of DIN and DIP uptake on
reefs is physically constrained by mass transfer, a term that refers to the
transfer of solutes in the water column across diffusive boundary layers
surrounding the tissue surface of an organism (Bilger and Atkinson,
1992; Hurd, 2000). Nutrient uptake in reef waters is typically mass transfer
limited (i.e., the biological demand for nutrients is higher than the
physical rate at which they can be supplied). Therefore, the uptake rate has
a first-order relationship with nutrient concentration and is a function of
water velocity, bottom roughness properties, and diffusion characteristics
of the solute (Atkinson, 2011). Due to the dependency of
mass-transfer-limited nutrient uptake on flow speed, the local hydrodynamic
conditions within a reef directly affect uptake rates of DIN and DIP
(Atkinson and Bilger, 1992; Baird et al., 2004; Falter et al.,
2016; Reidenbach et al., 2006; Thomas and Atkinson, 1997), and these uptake
rates can be predicted for a particular reef given sufficient information
(Falter et al., 2004; Zhang et al., 2011). However, validating these
models with observations from living systems remains a major challenge, as
measurements must occur at spatial and temporal scales relevant to reef
circulation, and in situ uptake is often confounded by
simultaneously occurring biogeochemical processes that release DIN and DIP
into the water column (Atkinson and Falter, 2003; Wyatt
et al., 2012).
Ocean-derived dissolved organic N and P compounds are generally thought to
be refractory or too energetically intensive for organisms to utilize
(Knapp et al., 2005); thus, DON tends to dominate the nitrogen
pool and DOP concentrations are generally low and similar to DIP
(Furnas et al., 2011). However, studies on DON
uptake have provided mixed results: some have measured a net production of
DON by reef communities (Cuet et al., 2011a; Tanaka et al., 2011), while
others have found evidence that primary producers (Vonk
et al., 2008), corals (Grover et al., 2008), and filter feeders
(Rix et al., 2017) can directly utilize some DON compounds.
Finally, particulate N and P pools in reef waters are generally dominated by
small phytoplankton (<2µm) and bacterial cells, and are an important
source of nutrients for reef suspension and filter-feeding organisms
(Houlbrèque et al., 2006; Ribes et al., 2005; Wyatt et al., 2010).
Accurate measurements of nutrient uptake in natural reef communities are
still relatively limited and are just beginning to incorporate spatial and
temporal variability in forcing conditions (Lowe and Falter, 2015),
such as gradients in wave energy across a reef or seasonal changes in local
oceanic nutrient concentrations (e.g., Wyatt et al.,
2012). While many studies have assessed nutrient dynamics in reefs
experiencing long-term nutrient enrichment (Cuet et al., 2011a; Furnas,
2003; Paytan et al., 2006; Tait et al., 2014), relatively little work has
focused on systems experiencing natural pulses in nutrient delivery from
processes such as coastal upwelling (Andrews and Gentien,
1982; Stuhldreier et al., 2015; Wyatt et al., 2012) or internal waves
(Green et al., 2019; Leichter et al., 2003; Wang et al., 2007).
Additionally, the majority of reef research to date has occurred on reefs,
whose circulation patterns and residence times are mainly driven by
wave-breaking on the fore-reef (Monismith, 2007). However, the
circulation of up to a third of reefs worldwide has been estimated to be
tide-dominated, defined as the case where annual mean significant wave
height (offshore of the reef) is less than the mean tidal range
(Lowe and Falter, 2015). Reefs that are strongly tide-dominated can
experience substantial variability in flow speeds and water depths over a
single semidiurnal tidal cycle (Lowe et al., 2015), which
suggests that mass-transfer-limited nutrient uptake rates (and other
biological processes) would also vary throughout the tidal cycle.
The Kimberley coastal region (located in remote northwestern Australia) has a
macrotidal regime where spring tidal ranges can reach 12 m in some locations
(Kowalik, 2004). The region contains thousands of islands with a total
reef area estimated to be ∼2000 km2 (Kordi
and O'Leary, 2016), inhabited by diverse coral reef and seagrass communities
(Richards et al., 2015; Wells et al., 1995). Recent
work has revealed the strongly tide-dominated circulation that can occur on
Kimberley reef platforms (Lowe et al., 2015). When the tidal
amplitude (half the tidal range) is greater than the reef elevation relative
to mean sea level, water levels drop below the reef for portions of each
tidal cycle, and this “truncation” of the semidiurnal tide results in
asymmetric phase durations (∼10 h ebb and ∼2 h flood) and flow speeds (Lowe et al., 2015). Extended
periods of low water depth on reef platforms such as Tallon Island can cause
communities to experience high irradiances that result in diel temperature
changes up to 11 ∘C (Lowe et al., 2016) and dissolved
oxygen fluctuations among the most extreme measured worldwide
(Gruber et al., 2017). Recent measurements of coral
calcification (Dandan et al., 2015), seagrass productivity
(Pedersen et al., 2016), reef community metabolism
(Gruber et al., 2017), and particulate nutrient uptake
(Gruber et al., 2018) have been published from
tide-dominated systems, yet little is currently known about how these large
tides control fluxes of dissolved nutrients. The objectives of this study
were to (1) measure fluxes of dissolved N and P on a tidally forced reef, (2)
compare measured rates to maximum potential uptake predicted by
mass-transfer theory, and (3) compare tidal forcing (velocity and water depth
changes) and oceanic forcing (seasonal changes in nutrient concentration) of
mass-transfer-limited uptake rates. This work will provide some preliminary
insight into the magnitudes, variability, and temporal scales of nutrient
cycling on tide-dominated reefs.
MethodsField site
A series of field experiments were conducted in the western Kimberley region
at Tallon Island, which contains a large intertidal reef platform (surface
area 2.2×106 m2) on its eastern side
(Fig. 1). The platform is elevated slightly (25 cm) above mean sea level, and the seaward rim is 10 cm shallower than the
rest of the platform; this feature, coupled with bottom friction, prevents
reef benthic communities from becoming emersed during low tide
(Lowe et al., 2015). The platform is covered with a series of
regular shore-parallel ridges ∼0.15–0.25 m in height and
contains two benthic communities: a seagrass-dominated inner zone (from the
fringing mangrove shoreline to 400 m landward of the reef crest) and a
coral reef outer zone (200 m wide extending shoreward from the crest).
Between these distinct communities, a 200 m zone of rubble and sand occurs
where the seagrass and coral reef communities mix
(Fig. 1). Enhalus acoroides is found with Thalassia hemprichii in the seagrass zone
(Wells et al., 1995). The coral community contains brown foliose
macroalgae (predominantly Sargassum spp.), a diverse assemblage of small hard corals
(∼5 %–10 % cover), soft coral, coralline macroalgae, and
crustose coralline algae.
Summary of mean (italics indicate standard deviation) conditions in offshore waters during October and February
field experiments. Nutrient species measured are nitrate and nitrite (NOx),
ammonium (NH4+), dissolved inorganic phosphorus (DIP), and
dissolved organic nitrogen (DON). Number of duplicate nutrient samples
collected is shown for offshore (Off), coral (CR), and seagrass (SG) sites.
Deployment locations of hydrodynamic instrumentation and water
sampling locations on the Tallon reef platform and offshore. Inset shows Tallon
Island location in the western Kimberley region of Australia. ADV refers to
acoustic Doppler velocimeter and ADPHR refers to acoustic Doppler profiler.
The Kimberley region experiences a subtropical climate, so field
experiments at Tallon reef were conducted during the dry (5–20 October
2013) and wet seasons (4–9 February 2014). Nutrient concentrations were
measured from duplicate filtered water samples
(Table 1) and were
collected around hydrodynamic instrumentation, forming a one-dimensional
control volume, as detailed below (see also Gruber et al.,
2017). This approach allowed estimation of dissolved nutrient fluxes (the
net uptake or release of nutrients) across the reef benthos. Estimates of
uptake of DIN and DIP at the limits of mass transfer were made using
hydrodynamic data over a spring–neap cycle (∼15 d)
collected during the hydrodynamic study of Lowe et al. (2015) and
nutrient concentrations from water sampling during the October and February field
experiments. Flows on the reef platform are strongly tide-driven and can be
predicted based on water depth and tidal phase (Lowe et al.,
2015); given that spring and neap tidal ranges were very similar between
October
and April experiments, velocity measurements from April can be considered
representative of velocities in October. This paper presents tidal
phase-averaged data as a way to visualize hydrodynamic and biogeochemical
measurements that tend to fluctuate with the phase of tide. Phase-averaged
values in this study are ensemble averages of all measurements occurring at
a given point in the semidiurnal (M2) tidal cycle (e.g., the average of all
measurements taken during low tide).
Dissolved nutrient sampling
Water samples were collected during both field experiments for analysis of
dissolved nutrient concentrations in offshore and reef flat waters. Eulerian
sampling occurred at three stations (Fig. 1): the
coral zone (CR), the seagrass zone (SG), and offshore of the reef in
adjacent waters (Off). Offshore samples were collected throughout the
semidiurnal tidal cycle on days of sampling (Table 1). Collecting water samples on the reef platform
was not feasible during periods of peak flood and ebb, which occurred 0–1
and 4–6 h after the onset of reef flooding, respectively (when
offshore waters first overtopped the reef crest). Rapid changes in water
depth during these tidal phases caused current speeds exceeding 0.8 m s-1 (Fig. 2), which made for unsafe
conditions for sampling by foot or boat. Reef sampling was conducted during
the remaining 9 h of each tidal cycle, either by foot when water depths
were low (∼0.4–0.6 m) or by boat during high tide (1–4 h from the onset of reef flooding).
Selected time series of spring–neap transition showing (a) water
depths (h) on the reef (measured in the seagrass zone) and offshore, with
depth-averaged flow speed u in (b) coral- and seagrass-dominated zones.
Water samples were collected from just beneath the water surface for
analysis of dissolved nutrients. A 50 mL syringe (pre-rinsed with reef
water) was used to collect water, which was immediately filtered (Minisart,
pore size 0.45 µm) into 30 mL pre-rinsed tubes. These samples were placed in
darkness on ice and were frozen upon return to the field station (several
hours); samples were transported and stored frozen until analysis at the
laboratory (<4 weeks from the end of the field experiment).
Analyses of nitrate and nitrite (NOx), ammonium (NH4+), and
inorganic phosphorus (DIP) concentrations were determined on a
flow-injection autoanalyzer (Lachat QuikChem 2500) using standard methods
(Strickland and Parsons, 1972). Total dissolved nitrogen was determined
by persulfate oxidation of filtered samples (Valderrama, 1981), followed
by analysis of nitrate as above. Dissolved organic nitrogen (DON) was
estimated from the total dissolved nitrogen less NOx and
NH4+. All nutrient concentrations presented are the mean of
duplicate samples.
Control volume approach
The control volume (CoVo) technique utilizes flow measurements and modified
Eulerian sampling of solutes or particles to derive in situ benthic flux
estimates. Tallon reef platform is well-suited to a one-dimensional CoVo
approach due to long periods (approximately 10 h of each semidiurnal tidal
cycle) of consistent flow direction; nutrient sampling may thus be conducted
at “upstream” and “downstream” sites during these periods. A similar
approach has previously been used on Tallon reef to estimate its benthic
metabolism (Gruber et al., 2017) and particulate material
uptake (Gruber et al., 2018) rates. A bottom-mounted
acoustic Doppler current profiler (Nortek Aquadopp HR) was stationed near SG
(Fig. 1) and measured current velocity and water
depth (h) at 1 Hz and 0.03 m bins. Depth-averaged flow speeds (u) were
averaged at 5 min intervals. During the reef's extended ∼10 h ebb tide, water drained off the platform in a consistent northeast
direction (80∘±30∘, mean ± standard
deviation), along which the water sampling stations were aligned.
Depth-averaged current velocity was rotated in this ebb flow direction
(ux) and transport qx was estimated as follows:
qx=uxh,
assuming negligible horizontal dispersion. The net flux Jnet (in mmol N
or P m-2 d-1) of each nutrient species (NOx, NH4+,
DIP, and DON) into the benthos was estimated as follows:
-Jnet=h‾dC‾dt+qx(CCR-CSG)dx,
where the distance between sampling stations dx was 540 m and h‾ was
the mean water depth along dx. Nutrient concentrations at CR and SG are
represented by CCR and CSG, respectively; C‾ is the mean of
CCR and CSG at a given time step (Genin et al., 2002).
Positive values of Jnet represent net benthic nutrient uptake and
negative Jnet indicates net release of nutrients to the water column;
these fluxes are the net result of all biogeochemical processes occurring
between SG and CR, and thus represent fluxes from a combination of seagrass
and coral reef communities. The “local” benthic flux (i.e., nutrient uptake
or release occurring in the reference frame of the sampling stations) is
represented by the first right-side term of Eq. (2) and was estimated at
hourly intervals when water sampling occurred. The second term of Eq. (2)
represents the “advective” flux (i.e., nutrient uptake or release during
transit between sampling stations). Transit time between stations changed
throughout the tidal cycle and could be on the order of hours during
periods of slow flow (<5 cm s-1). To better represent the
advective component, advective fluxes were calculated at every point where
nutrient concentrations were available and were then bin-averaged over a
time interval that approximated the transit time. These estimates were then
linearly interpolated to times where local estimates existed.
Uptake rates at the limits of mass transfer
For comparison with the field observations, the theoretical uptake rates of
DIN and DIP at the limits of mass transfer (JMTL) were calculated for
each of the measurements of Jnet above. Assuming nutrient concentrations
at the tissue surface of benthic organisms were near zero, JMTL was
estimated along the study transect (from SG to CR) as follows (Falter et
al., 2004):
JMTL=SC‾,
where S is the mass-transfer velocity (in m d-1). Estimates of
JMTL and S were made for NOx, NH4+, and DIP and were
averaged over the same time intervals as Jnet. Mass-transfer velocity
S was estimated as follows (Falter et al., 2004):
S=uxCD0.5/(Rek0.2Sc0.6),
where CD is the drag coefficient, Rek is the roughness Reynolds
number, and Sc is the Schmidt number. Mass-transfer velocity is a function
of flow speed and is indirectly related to water depth through the drag
coefficient; the magnitude of S depends on the diffusivity of the nutrient
species of interest (through the Schmidt number) yet is unrelated to
nutrient concentration (see below). The Schmidt number is defined as the
kinematic viscosity v divided by the diffusion coefficient D of the nutrient
species, which were 19.05, 19.80, and 7.00×10-6 cm2 s-1 for
NOx, NH4+, and PO43-, respectively (Li and
Gregory, 1974). The drag coefficient CD increases dramatically as reef
water depth decreases (Lentz et al., 2017) and was
estimated from an empirical relationship between h and the mean height of
reef ridges hr as follows (McDonald et al., 2006):
CD=1.01(h/hr)-2.77+0.01,
where hr was determined by measuring the mean height (vertical distance
between the crest and trough of a reef ridge) of all ridges along a 50 m transect. The roughness Reynolds number Rek is defined
as follows:
Rek=u∗ks/v,
where ks, a hydraulic roughness length scale, was 0.5 m (Lowe
et al., 2015) and the shear velocity u∗ is a function of bottom
shear stress τb and seawater density ρ as follows:
u∗≡τb/ρ=uxCD/2.
Estimates of maximum potential nutrient release (Jrelease) represent the
flux of NOx, NH4+, and DIP necessary to match the observed
Jnet assuming uptake occurred at mass-transfer-limited rates and were
estimated as follows (Wyatt et al., 2012):
Jrelease=Jnet-JMTL,
for each of the intervals over which Jnet was calculated.
Large changes in water depth, flow speed, and nutrient concentration
occurred during each tidal cycle, yet measurements of Jnet could only be
made during ebb tide (generally 6–12 h after onset of reef flooding).
In order to understand how the range of flow speeds experienced by this reef
platform could influence maximum potential nutrient uptake rates, we
calculated JMTL continuously over a full ∼15 d
spring–neap cycle at individual stations SG and CR. Flow speed measurements
from an April 2014 experiment were used, which included an acoustic Doppler profiler (ADP) and acoustic Doppler velocimeter
(ADV)
located at SG and CR, respectively; as discussed previously, flows on Tallon
reef can be predicted based on water depth and tidal phase (Lowe
et al., 2015), so measurements from April would be representative of flows
during October and February experiments. Calculations were made as above (Eqs. 3–7)
with the exception of using u instead of ux (Eqs. 4, 7), as we are now
estimating fluxes over the full tidal cycle rather than only the
roughly unidirectional ebb tide portion. Tidal phase-averaged
concentrations of NOx, NH4+, and DIP were approximated for
both sites (CR and SG) and field experiments (October and February) using measured
concentrations (Fig. 3), where available. As it
was not possible to collect water samples during peak ebb tide (due to
hazardous conditions), nutrient concentrations in offshore waters
(Table 1) were assumed to be representative of
concentrations on the reef platform during those times.
In a strongly tide-dominated system such as Tallon reef, each tidal cycle
“refills” the reef by flushing it with fresh oceanic water. In order to
conceptualize the net biogeochemical fluxes that occur over this cycle, we
used tidal cycle averages. Tidal cycle averages of mass-transfer velocities
(Scyc) and mass-transfer-limited nutrient flux (Jcyc) were
calculated as the mean of all S and JMTL, respectively, occurring within
an individual semidiurnal tidal cycle beginning when water flooded the reef
platform.
Measurements of (a, b) nitrate (NOx), (c, d) ammonium
(NH4+), and (e, f) dissolved inorganic phosphorus (DIP) from water
samples during October (a, c, e) and February (b, d, f) field experiments.
Samples were taken at two reef stations; CR- and SG-dominated zones and mean offshore nutrient concentrations are shown (dashed blue
line). Tidal phase-averaged water depth h is also shown (black line).
Uncertainties in estimates of S, Jnet, and JMTL were estimated by
propagating standard deviations using Monte Carlo simulation (10 000 iterations). Error terms for hydrodynamic variables were derived from
bin-averaged data (Lehrter and Cebrian, 2010) and were 0.01 m for h, 0.03 m s-1 for u, 0.05 µM for concentrations of NOx and NH4+,
0.01 µM for DIP, 1.0 µM for DON. Tidal phase-averaged concentrations of
NOx and DIP used in JMTL estimates were assigned standard
deviations of 0.5 and 0.05 µM, respectively.
ResultsNutrient concentrations and measured fluxes
Characteristics of offshore water (temperature, salinity, and nutrient
concentrations) showed some differences between dry and wet season field
experiments. Water temperature was ∼2∘C warmer
during the wet season in February, and levels of DIN were elevated, with NOx
concentrations approximately double those measured during the dry season in
October (Table 1). Salinity and concentrations of DIP
and DON were similar between seasons. Reef platform nutrient concentrations
were similar to offshore concentrations during flood tide and the start of
ebb tide (∼3–6 h after reef flooding,
Fig. 3); during the remaining 6 h of ebb
tide, the concentrations of DIN changed dramatically depending on the reef
zone (benthic community type). In the case of NOx, concentrations
decreased in the seagrass zone (SG) but increased in the coral zone (CR) by
up to 5 times compared to offshore levels (Fig. 3a, b). Increases in NH4+ occurred at both SG and CR during ebb
tide (Fig. 3c, d), while DIP was generally lower
than offshore concentrations but tended to increase at CR during the final
few hours of ebb tide (Fig. 3e, f).
Fluxes (± standard deviation) of (a) nitrate (NOx), (b) ammonium (NH4+), (c) dissolved inorganic phosphorus (DIP), and (d) dissolved organic nitrogen (DON) along the study transect during both field
experiments. Net benthic fluxes (Jnet) were estimated using the CoVo
approach, while mass-transfer-limited uptake (JMTL) was calculated (Eq. 3) from reef platform flow and nutrient concentrations, and nutrient release
(Jrelease) was estimated from net and MTL fluxes.
Fluxes of DIN and DIP estimated using the CoVo technique were generally
negative, indicating a net efflux (release) of nutrients from the benthos to
the water column. This was especially true for NOx, where net nutrient
release (Jnet<0) reached 5 mmol m-2 d-1
(Fig. 4a), and net uptake (Jnet>0) was not observed during any point in either field experiment. Fluxes of
NH4+ and DIP varied between net uptake and release
(Fig. 4b, c), and Jnet for DIP tended to
transition from net uptake to net release over the duration of ebb tide.
There were no substantial differences in overall mean Jnet of dissolved
inorganic nutrients between October and February field experiments
(Table 2). Fluxes of DON did differ between
seasons; Jnet varied between net uptake and net release during October
(Fig. 4d) although mean Jnet was negligible
(Table 2). During February, Jnet of DON transitioned
from net uptake to net release over the ebb tide
(Fig. 4d) but showed a large uptake on average
(Table 2).
Mean (italics indicate standard error) net fluxes (in mmol m-2 d-1) of nutrients
determined by the CoVo approach during the October and February field experiments.
Nutrient species include nitrate and nitrite (NOx), ammonium
(NH4+), dissolved inorganic phosphorus (DIP), and dissolved
organic nitrogen (DON). Mean net (Jnet), mass-transfer-limited
(JMTL), and release (Jrelease) fluxes are from samples taken during
the final 6 h of ebb tide and do not represent fluxes at all phases of
the semidiurnal tidal cycle.
For simplicity, only values of S for NOx are shown, as the values of
other species (NH4+, DIP) differ only in magnitude by a constant
factor (due to diffusivity). Although temperature influences S through
viscosity, changes in temperature on the reef platform had a negligible
effect on S (<0.01 %) compared to reef hydrodynamics. The tidal
phase-averages of S on the reef platform (Fig. 5)
demonstrate the strong influence of flow speed and water depth on S.
Mass-transfer velocities rose sharply during the peak flood and ebb periods
(0–1.5 and 4–6 h after reef flooding, respectively). The largest S each
tidal cycle occurred at the beginning of flood tide, characterized by high
flow speeds (∼0.5 m s-1) and minimum water depths
(∼0.4 m) on the reef platform (Fig. 2); values of S during flood tide were ∼30 % greater at CR
compared to SG, which was due to the larger flow speeds and slightly
shallower (10 cm) water depths that occurred near the reef crest. The lowest S
for each tidal cycle (Fig. 5) occurred at high tide
when flow speeds became negligible and reef water depths were comparatively
large (∼2.5 m). Values of S were relatively small
(∼5 m d-1 for NOx) later in the ebb tide (8–12 h
after reef flooding) and were similar between SG and CR. As S was estimated
over a full spring–neap tidal cycle, the ranges of values shown
(Fig. 5) are from the most (spring) and least
(neap) energetic tidal cycles, which cause S to vary by a factor of <4.
Tidal phase-averages of flow speed u, drag coefficient CD, and
mass-transfer velocity S for nitrate (NOx) in coral- and
seagrass-dominated zones. Phase-averages are the mean of all measurements
occurring at the same point in the tidal cycle (e.g., mean of all S at high
tide), and the range represents conditions during spring and neap tidal
cycles. Hydrodynamic data are from April 2014. Dashed lines in panel (e) indicate upper and lower limits of
S measured from previous studies of reef
communities reviewed by Atkinson and Falter (2003).
The mass-transfer-limited nutrient fluxes JMTL were a function of both
S and the local nutrient concentrations (Eq. 3). Fluxes showed
variability over the tidal cycle associated with S but also showed prominent
differences between benthic communities and seasons related to nutrient
concentrations. Elevated NOx concentrations at CR
(Fig. 3a, b) resulted in rising JMTL during
the final 6 h of ebb tide, while low NOx concentrations at SG
resulted in low JMTL, especially during ebb tide
(Fig. 6). Similar concentrations of DIP
(Fig. 3e, f) between sites resulted in similar
JMTL between CR and SG (Fig. 6c, d). Seasonal
changes in offshore nutrient concentrations, particularly for NOx, have
the potential to enhance nutrient uptake rates. Elevated offshore NOx
during February (Table 1) resulted in a doubling of
estimated JMTL during flood and high tide portions of each tidal cycle,
compared to October (Fig. 6a, b). Seasonal differences
in JMTL were also found for DIP, where elevated fluxes occurred during
October (compared to February) due to higher DIP concentration in the dry season
(Table 1, Fig. 6c, d).
The maximum potential release of DIN and DIP to the water column, assuming
uptake was mass-transfer-limited (Jrelease, Eq. 8), was calculated for
every instance of measured Jnet (Fig. 4). In
the case of NOx, Jrelease was roughly double Jnet
(Fig. 4a), due to the large net NOx release
measured on the reef platform. Whereas for NH4+ and DIP,
Jrelease was on the order of JMTL, due to negligible values of
Jnet (Fig. 4b, c). Overall mean rates of
JMTL and Jrelease for DIN did not show seasonal differences
(Table 2), which was likely a function of these
estimates only occurring during a portion (ebb) of the tidal cycle.
Tidal phase-averaged mass-transfer-limited uptake rates of
JMTL for (a, b)NOx and (c, d) DIP in both coral- and seagrass-dominated
zones over a full spring–neap cycle. Phase-averages are the mean of all
measurements occurring at the same point in the tidal cycle (i.e., mean of
all JMTL at high tide). Shaded areas of JMTL indicate the range where maximum values approximate uptake during spring tides and minimum
values during neap tides. Estimates of JMTL were calculated using tidal
phase-averaged nutrient concentrations from October and February field experiments
(Fig. 3) and mass-transfer velocity S
(Fig. 5e, f).
When S was averaged over individual semidiurnal tidal cycles (e.g., mean of
all S within a tidal cycle, beginning with reef flooding), the difference
between SG and CR was only ∼1 m d-1
(Fig. 7). Mass-transfer velocities for NOx
and NH4+ were of similar magnitude over the tidal cycle, while
those for DIP were ∼50 % lower
(Fig. 7); this was a function of the diffusivity
of each of these solutes (Li and Gregory, 1974). When JMTL was
similarly averaged over individual tidal cycles
(Fig. 8), community and seasonal differences in
JMTL described previously (Fig. 6) were
prominent. Uptake of NOx showed the greatest differences between
seasons and sites, with uptakes rates during the wet season greater than dry
season rates by a factor of ∼2. Similarly, estimates of DIP
uptake were slightly enhanced during the dry season compared to wet season
rates, while uptake of NH4+ was similar between seasons and sites
(Fig. 8).
DiscussionOceanic nutrient supply
The measurements of offshore nutrient concentrations presented in
Table 1 are among the first published for the
Kimberley region (Jones et al., 2014) and are the
only (to our knowledge) published record that includes measurements during
the wet season. Concentrations of dissolved nutrients (NOx,
NH4+, DIP, and DON) were at the upper end of typical values in
coral reef waters worldwide, especially in the case of DON, which far
exceeded the <5µM common in reef waters (Atkinson and
Falter, 2003). Measurements from the coastal Kimberley
(Table 1) also exceeded long-term mean values from
inshore waters of the Great Barrier Reef (GBR) during both the wet and dry
seasons (Furnas et al., 2005; Schaffelke et al., 2012). The Kimberley
region shares similar rainfall patterns, tidal ranges, and low levels of
catchment alteration with the northern GBR (at a similar latitude to the
Kimberley), yet concentrations of DIN and DIP measured in this study were an
order of magnitude greater than those from the wet tropics (Furnas et
al., 2005; Schaffelke et al., 2012). These observations, coupled with
elevated concentrations of chlorophyll a and particulate nutrients
(Gruber et al., 2018) relative to “typical” oligotrophic
reef waters, suggest that some coastal Kimberley reefs may experience
naturally mesotrophic conditions.
Means (± standard deviation) of mass-transfer velocity S for
all individual semidiurnal tidal cycles (n=23) for nitrate (NOx),
ammonium (NH4+), and dissolved inorganic phosphorus (DIP). Values
are from SG- and CR-dominated communities.
Wet season terrestrial discharge events deliver sediment and nutrients to
coastal waters of northern Australia (Brodie et al., 2010; Devlin and
Schaffelke, 2009; Schroeder et al., 2012). Offshore concentrations of
NOx and NH4+ measured in our study approximately doubled
during the February field experiment compared to October, whereas DIP and DON were
similar between seasons (Table 1). Whether this
increase is due to river discharge or coastal oceanographic processes is not
presently clear in the Kimberley region and warrants future study. Ratios
of offshore DIN : DIP were 4.3 and 10.7 in October and February, respectively
(Table 1), with the value during October similar to the
DIN : DIP ratio of ∼3:1 previously found in coastal Kimberley
waters during the dry season (Jones et al., 2014).
These values are below the Redfield ratio (16:1), suggesting that pelagic
production may be N-limited. This is common for reef waters generally,
although long-term averages of inshore GBR waters are generally <3:1 even during the wet season (Furnas et al., 2005; McKinnon et al.,
2013; Schaffelke et al., 2012). This suggests that N-limitation may be less
severe in the Kimberley than in GBR waters, particularly during the wet
season.
Means (± standard deviation) of mass-transfer-limited uptake
JMTL for all individual semidiurnal tidal cycles (n=23) for (a) nitrate (NOx),
(b) ammonium (NH4+), and (c) dissolved inorganic
phosphorus (DIP). Values are from SG- and CR-dominated
communities during October and February field experiments.
Rates and sources of benthic release of DIN and DIP
Benthic nutrient fluxes measured using the control volume technique
(Jnet) showed net release of NOx on Tallon
(Fig. 4a), while NH4+ and DIP fluxes
varied between uptake and release (Fig. 4b, c) but were negligible overall during the ebb tide (Table 2). Previous studies of reef nutrient fluxes in flumes or other controlled
environments have generally shown uptake approaching the limits of
mass transfer for NH4+ (e.g., Atkinson et al., 1994; Cornelisen
and Thomas, 2009; Larned and Atkinson, 1997; Thomas and Atkinson, 1997), DIP
(reviewed in Cuet et al., 2011b), and, less frequently, for
NOx (e.g., Baird et al., 2004); these controlled
environments lack some of the confounding processes present in natural reef
communities. Yet net release of nutrients (especially NOx) clearly
occurs in situ as concentrations on many reefs exceed those offshore
(e.g., Hatcher and Frith, 1985; Leichter et al., 2013; Rasheed et al.,
2002), and release rates up to 20 mmol NOx m-2 d-1, 12 mmol
NH4+ m-2 d-1, and 2 mmol DIP m-2 d-1 have been
measured with in situ studies (Miyajima et al., 2007a, b; Silverman et al., 2012; Wyatt et al., 2012). We have not considered
nitrogen inputs from other sources such as N2 fixation
(Cardini et al., 2014) or reef porewater advection during ebb
tide (Santos et al., 2011), which may result in an overestimation
of DIN release on Tallon. However, given that NOx concentrations
generally approach detection limits in reef porewater (Sansone et al.,
1990; Tribble et al., 1990) and N2 fixation adds to the NH4+
pool, it seems unlikely that either of these processes dominate the observed
nutrient fluxes.
If we assume that the fluxes discussed above (Jnet) simultaneously occur
with uptake of DIN and DIP near the limits of mass transfer, this gives a
gross release (Jrelease) of ∼10 mmol N m-2 d-1
and ∼0.5 mmol P m-2 d-1
(Table 2). Previous work has attributed inorganic
nutrient release to remineralization of particulate material by benthic
filter feeders (Ribes et al., 2005; Wyatt et al., 2012)
and detritivores (Silverman et al., 2012), which can graze
PON on the order of DIN release rates, as well as nitrification by sponge
communities (Southwell et al., 2008). In the case of
Tallon reef, uptake of phytoplankton (0.95 mmol N and 0.20 mmol P m-2 d-1) (Gruber et al., 2018) is on the order of
Jrelease in the case of P but is much smaller than Jrelease of N.
Large particles (such as entire fronds of macroalgae) are rare but can form
a major component of the particulate organic pool on some reefs
(Alldredge et al., 2013); remineralization of similar material
(rather than small particles like phytoplankton) may be the source of the
observed DIN release on Tallon. Finally, fluxes of DON on the order of
Jnet were measured on Tallon, with net uptake occurring during the
February
experiment (Fig. 4d). The dynamics of DON in reef
systems have been addressed in a few studies (e.g., Haas and Wild,
2010; Thibodeau et al., 2013; Ziegler and Benner, 1999), and there is some
evidence that reef organisms including corals (Ferrier, 1991),
sponges (Rix et al., 2017), and seagrasses
(Vonk et al., 2008) can directly utilize DON. In
summary, gross release of DIP may be derived from phytoplankton uptake on
Tallon reef, but released DIN exceeds phytoplankton inputs and is likely
derived from additional sources including remineralization of large
particles and DON.
Tidal and seasonal forcing of mass-transfer-limited fluxes
Few estimates of nutrient uptake rate S exist for in situ reef communities;
the majority of previous estimates come from controlled flume experiments
and are in the range of 2–15 m d-1 (reviewed in Atkinson
and Falter, 2003). Uptake rates are strongly dependent on flow and roughness
characteristics (Falter et al., 2016), and in wave-dominated
systems S can vary by an order of magnitude across the reef (e.g., from 25 m d-1 on the fore-reef to 5 m d-1 in the back-reef), as bottom stress
from wave forcing declines (Wyatt et al., 2012; Zhang
et al., 2011). In wave-dominated systems, S would be expected to be
reasonably consistent while offshore wave forcing remain similar (e.g., at
scales of days–weeks). Estimates of S from Tallon reef show uptake rates
varying rapidly on the scale of hours or even minutes; for instance, uptake
rates for NOx decreased by an order of magnitude (∼30–3 m d-1) over the period of an hour during flood tide
(Fig. 5e). When averaged over longer timescales
(i.e., over individual semidiurnal tidal cycles), estimates of S for DIN and
DIP (∼9 and ∼5 m d-1, respectively) were
similar to the mean of those measured in previous studies and only differed
slightly between seagrass and coral reef zones
(Fig. 7). Tallon reef platform experiences flows
and water depths particular to its geometry and position relative to mean
sea level; therefore, S (and accordingly nutrient uptake) will vary in other
tide-dominated reef communities as a function of these factors.
Estimates of mass-transfer-limited uptake of DIN and DIP varied over a tidal
cycle with S but also showed differences in uptake with reef zone and season
(Fig. 6). Reef zones were similar in DIP uptake
rates, but rising concentrations of NOx in the coral zone during ebb
tide caused estimates of JMTL to increase compared to the seagrass zone
(Fig. 6a, b). Previous work on Tallon reef has
shown that the coral zone is ∼20 % more productive than the
seagrass zone (Gruber et al., 2017), which may be related to
this difference in potential nitrate fluxes. Concentrations of NOx and
NH4+ were elevated in the wet season, while DIP declined compared
to the dry season (Table 1); these seasonal
differences were evident in the mass-transfer-limited nutrient fluxes even
when integrated over individual semidiurnal tidal cycles
(Fig. 8). Ratios of DIN : DIP mass-transfer-limited
uptake during October were 8.6 and 10.8 for seagrass and coral zones,
respectively (Fig. 8). These ratios are well
below the tissue N:P ratio of 30:1 typical of reef primary producers
(Atkinson and Smith, 1983) and suggest that producers on Tallon
reef may be strongly N-limited (at least during the dry season). This is
supported by low N:P ratios (14:1) measured in Thalassia leaf tissue from Tallon reef
during October (Cayabyab, unpublished data). During February, ratios of DIN : DIP
mass-transfer-limited uptake were 21.5 and 21.3 for seagrass and macroalgal
zones, respectively (Fig. 8), which suggests that
N-limitation may be somewhat alleviated due to increases in oceanic DIN
during the wet season.
Comparison of wave and tidal forcing
This study suggests several important differences between wave- and
tide-dominated reef biogeochemistry, which are controlled by the
hydrodynamic regime. Firstly, the “source” of a water parcel overlying a
particular benthic community differs between wave- and tide-dominated
systems. In a simplified wave-driven reef, offshore (oceanic) water moves
from reef crest to back-reef roughly unidirectionally, generally exiting the
reef through channels. Thus, benthic communities are subjected to the
physicochemical water properties present in offshore waters modified by the
communities upstream of them. In a simplified tide-driven reef, flow
direction changes throughout the tidal cycle; during flood tide, offshore
waters enter the reef, while during ebb tide, waters from the back-reef
traverse all downstream communities. These flow patterns control water
residence times within the reef community. In wave-dominated reefs, flow
speeds are driven by wave-breaking on the reef, creating residence times on
the scale of ∼ hours; wave energy can be generally consistent
in time over ∼ days–weeks (Lowe and Falter, 2015).
In tide-dominated systems, reef waters exchange with offshore waters at
timescales greater than or equal to a semidiurnal (or diurnal) tidal cycle; this residence
time will vary depending on the reef's vertical position relative to mean sea
level and its morphology. Finally, there are marked differences in nutrient
uptake rates between wave- and tide-dominated reefs. The consistency of wave
energy at scales of ∼ days–weeks likely drives similarly
consistent mass-transfer-limited nutrient uptakes rates on wave-dominated
reefs. On reefs with strong tidal forcing, however, flow speeds are highly
variable throughout the tidal cycle and mass-transfer-limited uptake can
vary by an order of magnitude within ∼ hours–minutes. Flow
speeds also change over the spring–neap tidal cycle (∼15 d); on Tallon reef, mass-transfer-limited uptake rates were
∼2–4 fold greater during spring tides relative to neap tides.
The ∼8 m tidal range of Tallon reef is typical of tidal
ranges in the Kimberley region, and thus the results presented here are
likely to be broadly representative of conditions experienced by many reefs
(∼2000 km2 of total reef area) in this region. Most
reefs globally do not experience such an “extreme” tidal regime, and
therefore some aspects of this study (such as benthic fluxes varying by an
order of magnitude on scales of minutes to hours) would not necessarily
represent conditions on mesotidal or microtidal reefs. However, approximately
30 % of reefs worldwide have tide-dominated circulation, including iconic
systems such as much of the southern Great Barrier Reef (Lowe and
Falter, 2015); such reefs likely experience a similar, though more
moderated, version of the physical processes that occur in macrotidal
systems. Our work therefore provides some insight into how other researchers may
relate benthic fluxes to tidal processes on other reef systems. Further
process-based studies that incorporate tidal forcing will improve
predictions of reef water temperatures (and coral bleaching), in situ
calcification rates, and many other physically linked biological processes
that affect the health and resilience of coral reef communities.
Conclusions
In conclusion, this study was one of the first to measure rates of in situ
benthic nutrient uptake and release on a tidally forced reef. We found that
reef communities released a moderate amount of DIN, potentially derived from
the remineralization of phytoplankton, large organic material, and DON. The
strong tidal forcing of this reef drives large variability (an order of
magnitude) in mass-transfer-limited nutrient uptake rates at short timescales (minutes–hours), and uptake can be enhanced in reef zones
downstream of where DIN release occurs. Tallon reef displays some
indications of nitrogen-limitation during the dry season, which may be
relieved during the wet season; seasonal increases in offshore nitrate
concentrations increased mass-transfer-limited uptake rates by a factor of
∼2. This work identifies some hydrodynamic properties of
tide-dominated reefs that control their biogeochemistry and help define them
in comparison to wave-dominated reefs.
Data availability
The data used in this paper are publicly accessible and can be downloaded here:
https://data.pawsey.org.au/public/?path=/WA Node Ocean Data Network/WAMSI2/KMRP/2.2/2.2.3 (last access: 8 May 2019).
Author contributions
Field experiments were designed by RKG, RJL, and JLF. Fieldwork was
conducted by RKG and RJL. RKG analyzed the results and prepared the
manuscript with contributions from RJL and JLF.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
This work was conducted on Bardi Jawi sea country and we acknowledge the
Traditional Owners past, present, and emerging who care for this country. We
thank the Bardi Jawi Rangers and Kimberley Marine Research Station staff for
providing assistance and local knowledge during field experiments. We thank
Michael Cuttler, Jordan Iles, Miela Kolomaznik, and Leonardo Ruiz-Montoya
for helping with fieldwork. Three anonymous reviewers gave helpful comments
that improved earlier versions of this paper.
Financial support
This research has been supported by the Australian Research Council (Future Fellowship grant no. FT110100201),
the Australian Research Council Centre of Excellence for Coral Reef Studies (grant no. CE140100020), and the Western Australian
Marine Science Institution (Kimberley Marine Research Program, Project 2.2.3).
Review statement
This paper was edited by Jack Middelburg and reviewed by three anonymous referees.
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