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Oceanic Forcing of Coral Reefs
Ryan J. Lowe and James L. Falter
ARC Centre of Excellence for Coral Reef Studies, School of Earth and Environment,
and UWA Oceans Institute, University of Western Australia, Crawley 6009, Australia;
email: [email protected], [email protected]
Annu. Rev. Mar. Sci. 2015. 7:43–66
Keywords
First published online as a Review in Advance on
September 17, 2014
coral reefs, waves, tides, circulation, temperature, nutrients
The Annual Review of Marine Science is online at
marine.annualreviews.org
Abstract
This article’s doi:
10.1146/annurev-marine-010814-015834
c 2015 by Annual Reviews.
Copyright All rights reserved
Although the oceans play a fundamental role in shaping the distribution and
function of coral reefs worldwide, a modern understanding of the complex
interactions between ocean and reef processes is still only emerging. These
dynamics are especially challenging owing to both the broad range of spatial
scales (less than a meter to hundreds of kilometers) and the complex physical
and biological feedbacks involved. Here, we review recent advances in our
understanding of these processes, ranging from the small-scale mechanics
of flow around coral communities and their influence on nutrient exchange
to larger, reef-scale patterns of wave- and tide-driven circulation and their
effects on reef water quality and perceived rates of metabolism. We also
examine regional-scale drivers of reefs such as coastal upwelling, internal
waves, and extreme disturbances such as cyclones. Our goal is to show how
a wide range of ocean-driven processes ultimately shape the growth and
metabolism of coral reefs.
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1. INTRODUCTION
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Upwelling: the
upward movement of
water resulting from
wind-driven Ekman
transport or flow
curvature in the
vicinity of islands
Internal waves:
wave motions that
propagate within the
interior of a
density-stratified
ocean
44
The physics, chemistry, and biology of the world’s oceans have long been known to play a critical
role in shaping the growth, diversity, and distribution of coral reefs. Darwin (1842) first hypothesized that the surrounding oceans provide a major source of nutrition to coral reef communities
and that reefs therefore grow best at their most seaward edges. More than a century later, Munk &
Sargent (1954) proposed that the energy dissipated by waves on shallow fore reefs and reef crests
facilitates the rapid exchange of nutrients and other metabolites necessary to support the robust
growth of reef communities in otherwise nutrient-poor environments. This basic idea would stimulate modern research aimed at understanding how hydrodynamic processes in benthic boundary
layers control the uptake of dissolved nutrients by reef communities (Atkinson & Bilger 1992,
Falter et al. 2004, Hearn et al. 2001, Lowe et al. 2005b, Thomas & Atkinson 1997). Additional
work has since provided more direct evidence of how reefs also feed off the living plankton washed
over them from the surrounding ocean (Ayukai 1995, Charpy & Blanchot 1999, Fabricius et al.
1998, Wyatt et al. 2010). Nevertheless, the same ocean waves driving the circulation and material
exchange that are beneficial to the growth of reef organisms can also act as a destructive force
when large enough, especially when they are generated by large storms such as tropical cyclones
(Massel & Done 1993, Woodley et al. 1981). Extreme wave events can act as an additional source
of physical stress on reef systems already contending with other forms of environmental disturbance (De’ath et al. 2012) and may also lead to long-term changes in reef community structure
and diversity (Dollar & Tribble 1993, Madin & Connolly 2006).
The environment in which reefs live is further shaped by ever-changing ocean conditions at
scales much greater than the reef itself. At the shelf or island scale, coastal upwelling caused by
wind-driven Ekman transport or generated in the lee of islands can bring up cooler, more nutrientand particle-rich water. Such environments can support higher rates of nutrient acquisition (Gove
et al. 2006, Wyatt et al. 2010), create adverse chemical conditions for the formation of biogenic carbonate minerals (Manzello 2010), and offer potential refugia against ocean warming (Karnauskas
& Cohen 2012). Nonlinear internal waves propagating up continental shelf and island slopes
provide another potential mechanism for transporting cool water and nutrients to shallow coral
reefs (Leichter et al. 1996, Wang et al. 2007). At even larger scales, regional circulation patterns
control the widespread dispersal of reef larvae and, therefore, the biogeographical distribution of
reef organisms (e.g., Richmond 1987, Shulman & Bermingham 1995).
In the future, the oceans will continue to play an important role in determining how global
climate trends such as increased warming and the dissolution of CO2 will manifest themselves, or
“downscale,” at the regional, coastal, shelf, reef, community, and ultimately organism scales. For
example, although mean global temperatures are expected to increase by ∼4◦ C by the end of the
century under a business-as-usual scenario (Meinshausen et al. 2009), seasonal warming events
driving sea surface temperature anomalies of several degrees are already a regular occurrence. Such
intense ocean warming events occurred across the western Pacific and Caribbean in 1998 owing to
particularly intense El Niño conditions (e.g., Bruno et al. 2001, McClanahan et al. 2004) and along
Western Australia in 2010–2011 owing to the intensification of a warm eastern boundary current
during an intense La Niña period (Depczynski et al. 2013, Moore et al. 2012). Within the reef
systems themselves, benthic production, respiration, and net calcification can alter the chemistry
of circulating water (Kinsey 1978, Odum & Odum 1955, Sargent & Austin 1949, Smith 1973);
however, the magnitudes of these changes depend just as much on the degree of hydrodynamic
forcing and the morphologies of the reef systems as they do on rates of benthic metabolism
(Falter et al. 2013, Venti et al. 2012, Zhang et al. 2012). Thus, changes in the global wave and
storm climate that are expected to occur over the next century (Young et al. 2011) will no doubt
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lead to concomitant changes to many of the above biogeochemical and ecological processes on
reefs.
It is clear that the growth, metabolism, and community structure of coral reefs are heavily influenced by the oceanic environment in which they live. Unfortunately, it is not possible for a single
review to cover all important aspects of the coupling between physical and biological processes on
coral reefs. There have been some prior efforts to summarize the influence of oceanic processes on
coral reefs, although these either were published several decades ago (Hamner & Wolanski 1988)
or focused mainly on the details of the prevalent hydrodynamic processes (Monismith 2007). To
provide what we think is a good balance between breadth and detail, the present review focuses
first on the small- and reef-scale hydrodynamic processes affecting the transport and transfer of
mass (nutrients and carbon, dissolved and particulate), heat (temperature), and momentum (drag
and dissipation) on reefs, and second on how offshore ocean processes affect the physical and
chemical properties of nearshore reef waters. The review is thus organized by scale, starting with
the smallest scales (individual reef organisms and canopies; Section 2), moving to intermediate
scales (reef communities and systems; Section 3), and concluding with the largest scales that influence the growth and development of reefs along the continental margins and oceanic island
groups (regional and global; Section 4). For reference, Table 1 summarizes the variables used
throughout the review.
Canopy flow:
a region of flow inside
the bottom roughness
layer created by reef
organisms
2. ORGANISM TO REEF CANOPY SCALES (0.1–10 m)
The flow structure in and around reef organisms depends on the complex interactions between the
overlying water motion and the typically large, three-dimensional bottom roughness (or canopies)
formed by reef organisms (Figure 1a,b). The flow dynamics throughout reef canopies are highly
analogous to other, more well-studied canopy flows, particularly those through seagrasses and
other aquatic vegetation (for a recent review, see Nepf 2012). The common challenge for understanding the flow dynamics in all natural canopies is properly accounting for the highly variable
spatial flow structure that arises within even the simplest morphologies. There have been some
attempts to directly observe or numerically simulate the full three-dimensional turbulent flow
structure through individual branching coral colonies (Chang et al. 2009, Chindapol et al. 2013,
Kaandorp et al. 2003); however, such efforts are extremely expensive computationally, requiring
flows to be resolved down to scales on the order of millimeters. Thus, it remains impractical to
resolve the roughness geometries of reef organisms at the scale of entire reef communities or
systems.
To account for how such unresolved small-scale hydrodynamic processes influence the largerscale macroscopic properties of a canopy flow (e.g., mean velocity profiles), the traditional
Reynolds-averaged Navier-Stokes momentum equations are spatially averaged over a horizontal plane that excludes the solid canopy elements (Raupach & Shaw 1982):
1 ∂P
1 ∂τxy
Du
=−
+
− fx ,
Dt
ρ ∂x
ρ ∂z
(1)
where x is the streamwise direction, z is the vertical direction, ρ is the seawater density, u is the
streamwise velocity, P is the pressure, τxy is the shear stress, and the brackets indicate spatially
averaged variables. Importantly, the term fx represents a spatially averaged canopy resistance term
that arises from forces exerted by the canopy onto the surrounding flow (Lowe et al. 2005a).
Ultimately, the fundamental challenge in predicting flow through coral reef canopies via Equation 1 remains how to most accurately relate fx to the complicated three-dimensional structure of
reef communities, especially given their abundant variation in morphologies and roughness scales.
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Table 1 Summary of variables used in this review
Variable
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Unit
Description
m
Wave orbital excursion amplitude
C
mol m−3
Water column species concentration
Cd,c
—
Canopy element drag coefficient
CD
—
Total bed-form drag coefficient
CM
—
Canopy element inertial force coefficient
fx
m s−1
Spatially averaged canopy resistance
A∞
h
m
Water depth
hc
m
Canopy height
hr
m
Depth of the reef flat
H0
m
Offshore wave height
Hs
m
Significant wave height
J
mol m−2 h−1
W m−2
Net flux of heat or mass across the benthic and/or air-sea interface
K
m2 s−1
Horizontal dispersion coefficient
Lr
m
Length of the reef flat from crest to backreef
MTR
m
Mean tidal range
P
kg m−1 s−2
Pressure
q
m2 s−1
Depth-integrated transport
q
m2 s−1
Two-dimensional depth-integrated transport vector
Rek
—
Roughness Reynolds number
S
m d−1
First-order nutrient uptake rate coefficient
Sc
—
Schmidt number
T
◦C
Temperature
TA
μeq kg−1
Total alkalinity
u
m s−1
Horizontal spatially averaged streamwise velocity
Ū
m s−1
Depth-averaged current velocity
U∞
m s−1
Free stream velocity
Û
m s−1
Canopy depth-averaged streamwise velocity
α
—
Canopy flow attenuation parameter
β
m−1
Porous media drag parameter
η
m
Dynamic sea level or wave setup
λf
—
Frontal area canopy geometry parameter
τcan
kg m−1 s−2
Shear stress at the top of the canopy
τw
s
Wave period
τRT
h
Residence time of water within the reef domain
For natural canopies with simple morphologies (e.g., seagrasses), these form-drag forces can be
readily parameterized using a quadratic drag law that depends on the local in-canopy velocity, the
integrated frontal area of the canopy elements per unit area of the seafloor (λf ), and an empirical
drag coefficient (Cd,c ) (for details, see Nepf 2012). Such approaches have been applied to coral reef
canopies with well-defined branch geometries (e.g., Figure 1a) (Lowe et al. 2005a); however, the
complex morphologies of most reef canopies (e.g., Figure 1b) make assigning a representative λf
difficult or even impossible because of the challenge of identifying singular, well-defined geometric parameters. As an alternative approach to address this issue, Lowe et al. (2008) used turbulent
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a
b
Currents
c
Waves
‹u›(z)
τcan
d
‹u›
(z)
rms
τcan
dP/dx
Figure 1
(a,b) Examples of bottom roughness on reefs, showing a homogeneous community of Porites compressa forming a canopy of regular
cylindrical branches (panel a; photograph by R.J. Lowe) and a more complex reef canopy of plating and branching Acropora spp. (panel
b; photograph by the Western Australia Department of Parks and Wildlife). (c,d ) Flow structure under different conditions. Under
unidirectional flow (panel c), the shear stress at the top of the canopy (τcan ) transfers momentum from the overlying flow field into the
canopy and is opposed by the canopy drag forces that attenuate the flow (u) inside the canopy. Under wave-driven oscillatory flow
(panel d ), the unsteady wave-induced pressure gradient (dP/dx) provides an additional source of momentum that substantially
increases the rms flow (urms ) inside the canopy for a given flow speed.
porous media flow theory to parameterize fx . The advantage of the porous media approach is that
it has already been applied to a number of complex geometrical arrays and tested with a wealth
of empirical data (Macdonald et al. 1979). Although this approach has worked well for predicting
flow through a community of Porites compressa coral (Lowe et al. 2008), further work is needed to
parameterize flow resistance across a broader spectrum of natural reef canopy types.
2.1. Unidirectional Flow
For a unidirectional current over a submerged reef canopy, the discontinuity in form drag fx near
the top of the canopy generates a region of strong shear in the mean velocity profile (Equation 1),
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Unconfined flow: the
flow that occurs when
the water depth is
much greater than the
canopy height; the
canopy flow is driven
by a shear layer
Depth-limited flow:
the flow that occurs
when the water depth
is comparable to the
canopy height; the
canopy flow is
enhanced by the
pressure gradient
Emergent flow: the
flow that occurs when
the canopy reaches the
water surface; the
canopy flow is driven
solely by the pressure
gradient
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resulting in a local peak in the turbulent shear stress τcan (Ghisalberti 2009) (Figure 1c). The shear
layer transfers momentum from the overlying water column down into the canopy, thus driving
flow inside the canopy. This is the dominant form of momentum transfer that occurs when the
flow is unconfined, or when the canopy height hc occupies only a small fraction of the total water
depth h. When hc becomes an appreciable fraction of the water depth, the underlying canopy
flow becomes depth limited, and the background pressure gradient driving the overlying flow also
starts to directly drive flow within the canopy itself (Nepf & Vivoni 2000). As h c / h increases, the
pressure gradient term continues to increase the in-canopy flow, reaching a limit where the reef
canopy becomes emergent (h c ∼ h) such that the shear layer is no longer present and flow is driven
entirely through the canopy by the external pressure gradient (Nepf 2012).
At typical reef canopy heights (ranging from tens of centimeters to meters), many or most
flows on coral reef flats (h typically 1–2 m) must experience some degree of depth limitation.
This seemingly local effect can also have important consequences for the broader circulation
patterns on reefs (hundreds to thousands of meters), as the larger drag forces that arise from more
water being driven through a canopy under depth-limited conditions increases the resistance
experienced by the overlying flow. This was well illustrated by McDonald et al. (2006), who
found that the community bottom-drag coefficient CD , which relates the total drag force to the
overlying flow speed (not to be confused with the canopy element drag coefficient Cd,c , described
above), increased by roughly two orders of magnitude (from ∼0.01 to 1) as the depth over a
canopy of P. compressa coral approached the emergent limit (see figure 3 in McDonald et al. 2006).
Furthermore, there appears to be a relatively abrupt transition to high (order 0.1–1) values of CD
when h c / h increases above ∼0.3 (Lowe et al. 2008, McDonald et al. 2006). Collectively, these
studies emphasize that careful consideration of the in-canopy momentum dynamics—a factor that
has been largely ignored in traditional coastal ocean models—is critical to accurately parameterize
the effects of bottom drag on reefs (Rosman & Hench 2011).
2.2. Wave-Driven Flow
The dynamics of wave-driven flows through canopies have historically received limited attention,
owing largely to the lack of analogous terrestrial canopy models on which to build. Although the
momentum equations describing water motion in canopies under oscillatory and unidirectional
flows are fundamentally similar, there are two key differences: (a) Surface waves can generate
large oscillatory pressure gradients at the dominant wave period T (Figure 1d ), and (b) flow
accelerations inside the canopy can add an inertial force that increases the overall flow resistance
fx in Equation 1. To account for these effects, Lowe et al. (2005a, 2008) developed a simple model
describing the momentum dynamics within submerged canopies under wave-driven oscillatory
flow by depth integrating Equation 1 over the canopy region:
dÛ
dt
acceleration
=
−
1 dP
ρ dx
pressure gradient
+
Cf
CM (1 − φ) dÛ
|U ∞ |U ∞ − β|Û |Û −
.
2h c
φ
dt
form drag
shear stress
(2)
inertial force
Here, Û denotes the spatially averaged in-canopy velocity, Cf is a friction coefficient that relates
the magnitude of the shear stress at the canopy interface to the free stream velocity U ∞ , β is a
dimensional drag parameter based on a porous media formulation that depends on the internal
bed geometry, and CM is an inertial force coefficient (for details, see Lowe et al. 2008). Equation 2
predicts that the acceleration of the in-canopy flow (term 1) depends on the pressure gradient
and shear stress terms responsible for driving the flow (terms 2 and 3) and the form drag and
inertial forces that oppose it (terms 4 and 5). Lowe et al. (2005a) further defined a flow attenuation
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rms
parameter α ≡ Û rms /U ∞
to be the ratio of the rms wave velocity inside the canopy (Û rms ) to
rms
that in the free stream (U ∞ ). Above the canopy, where the wave-driven flow is assumed to be
inviscid (i.e., above the wave boundary layer), the wave-driven pressure gradient is related solely
to the acceleration of the free stream oscillatory flow. Simple scaling arguments show that the
importance of this pressure gradient term to the shear stress term increases with the ratio of the
wave orbital excursion amplitude (Arms
∞ ) to the roughness height of the canopy (Lowe et al. 2005a):
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U rms T
Arms
shear stress
∼ ∞
∼ ∞ .
pressure
hc
hc
(3)
Thus, similar to the case of severely depth-limited unidirectional flow, the pressure gradient
imposed by waves substantially enhances flow inside a reef canopy over a pure unidirectional flow
of the same magnitude (Figure 1d ). This theory has been supported by experimental studies using
both idealized reef canopies and experimental assemblages of real branching coral reef canopies
(Lowe et al. 2005a, 2008; Reidenbach et al. 2007), which have all shown that unsteady wave motion
substantially enhances the in-canopy flow (by a factor of 5–10 in these particular studies).
Mass-transfer
limited: describes
conditions under
which the rate of
uptake or release of a
compound is limited
by convective
transport across a
concentration
boundary layer
2.3. Nutrient Uptake
Pioneering work by Atkinson and others demonstrated that the biological demand for nutrients
on reefs is generally so high that rates of nutrient uptake by reef communities are limited by
their convective transfer across turbulent boundary layers formed on the surfaces of benthic reef
autotrophs (Atkinson & Bilger 1992, Baird & Atkinson 1997, Thomas & Atkinson 1997). Bilger &
Atkinson (1992) described these conditions as being “mass-transfer limited,” and adapted a theory
originally developed to describe heat and mass transfer to rough surfaces (from the engineering
literature) to instead describe nutrient uptake by coral reef communities. Under conditions of
mass-transfer limitation, the maximum mass-transfer-limited nutrient uptake rate (Jmax , in mmol
m−2 d−1 ) is first order with respect to the concentration of nutrients in the water column (C,
in mmol m−3 ), i.e., Jmax = Smax C, where Smax (in m d−1 ) is the first-order nutrient uptake rate
coefficient. On coral reefs, the conditions of mass-transfer limitation tend to break down only
when dissolved nutrient concentrations are more than two orders of magnitude greater than those
naturally occurring in tropical reef waters (Atkinson & Falter 2003).
The application of these mass-transfer formulations to the problem of nutrient uptake kinetics
in reef communities was an important step because (a) it approached the problem at the more
hydrodynamically relevant spatial scale of entire reef communities acting as canopies (see above),
rather than just that of individual organisms, and (b) it provided for the first time some predictive
capability for how water motion controls nutrient uptake by reef communities. Subsequent experimental work demonstrated the utility of these mass-transfer relationships to predict rates of
nutrient uptake for natural reef communities in laboratory flumes simulating pure unidirectional
flow (Baird & Atkinson 1997, Thomas & Atkinson 1997). Falter et al. (2004) later simplified Bilger & Atkinson’s (1992) original nutrient uptake formulations, which also incorporated additional
experimental data sets:
√
CD U ∞
(4)
Smax = 0.2 0.58 ,
Re k Sc
where U ∞ is the free stream flow speed, Sc is the Schmidt number of the dissolved nutrient, Re k
is the roughness Reynolds number of the flow, and is an empirical constant equal to ∼4 × 104 .
It is important to emphasize that CD in Equation 4 is a bulk drag coefficient that relates the total
flow resistance exerted by a reef community to the free stream flow speed U ∞ (see above). Owing
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to the practical size limitations of the experimental flumes that were used to develop Equation 4,
most of the experimental reef communities reported in the literature occupied up to 50% of the
water depth. Thus, these nutrient relationships have been developed almost exclusively under
conditions of substantial depth limitation. This explains the high CD values of ∼0.1–0.2 reported
in those studies (see summary in McDonald et al. 2006), suggesting that flow, and perhaps nutrient
uptake, would be enhanced within the interior regions of those experimental communities.
There are still substantial gaps in our understanding of dissolved nutrient uptake by reef communities under oscillatory flow conditions. However, a growing number of reports—including
several direct flume observations (Lowe et al. 2005b, Reidenbach et al. 2006, Thomas &
Cornelisen 2003, Weitzman et al. 2013) and inferences based on field studies (Bilger & Atkinson
1992, Falter et al. 2004)—have shown that wave-driven oscillatory flows substantially enhance
mass-transfer rates, increasing them by factors of 3 or more. Lowe et al. (2005b) asserted that the
relevant velocity scale to describe mass transfer should be the in-canopy flow velocity Û rather
than the free stream U ∞ because this is the velocity that more directly interacts with the surfaces
of organisms within the interior of the canopy. Thus, the enhancement of nutrient uptake under
oscillatory flow can be explained by the higher flow speeds induced within coral reef canopies
under these conditions. A similar argument can be made for the enhancement of nutrient uptake
under depth-limited flow. Nevertheless, further data are needed, especially for live natural coral
reef communities, to develop better nutrient uptake relationships that can be universally applied
across a broad range of flow regimes.
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2.4. Particle Uptake
The uptake of organic particles by reef heterotrophs can constitute a source of allochthonous
nutrients to coral reefs that is as important as the uptake of dissolved nutrients by reef primary
producers (Houlbrèque & Ferrier-Pagès 2009), especially for corals recovering from a recent
bleaching event (Ferrier-Pagès et al. 2003, Houlbrèque & Ferrier-Pagès 2009, Houlbrèque et al.
2004, Hughes & Grottoli 2013). There is now abundant evidence of living phytoplankton being
actively grazed by whole communities of reef organisms as water flows over reefs (Genin et al. 2009;
Monismith et al. 2010; Wyatt et al. 2010, 2012; Yahel et al. 1998); however, the phytoplankton
biomass within the oligotrophic tropical waters of most coral reefs is generally dominated by
the smallest size fraction (i.e., picoplankton <2 μm in size). Several studies have thus suggested
that most of these small phytoplankton are consumed by cryptic filter feeders such as sponges,
bivalves, and ascidians rather than by passive suspension feeders such as coral (Ribes & Atkinson
2007, Ribes et al. 2005).
Picoplankton feeding by scleractinian corals has been controversial, in part because the tentacle
sizes of these corals (0.1–1 mm) tend to be two to three orders of magnitude larger than these
cells, thus raising questions about whether such small particles can be physically captured (S.
Humphries, personal communication). However, recent studies have confirmed that at least some
species of scleractinian coral are capable of feeding on phytoplankton (Leal et al. 2014) and in
some cases even feeding on detrital fragments of macrophytes such as seagrass (Lai et al. 2013).
Theory suggests that very small suspended particles such as picoplankton should move with some
Brownian diffusion, implying that these particles can be assigned a diffusivity analogous to that
of a dissolved tracer (Espinosa-Gayosso et al. 2012). In this particle diffusion regime, it may
thus be reasonable to assume that the same mass-transfer formulations for predicting dissolved
nutrient uptake (e.g., Equation 4) could serve as a useful foundation for predicting the uptake of
small particles by coral reef communities. Although only very limited data are available to assess
these dynamics, some observations suggest that the uptake rate coefficients (S) for picoplankton,
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bacteria, and viruses are of magnitudes similar to those for dissolved nutrients (Patten et al. 2011,
Ribes & Atkinson 2007, Wyatt et al. 2012), which may lend some support to this hypothesis.
Larger particles (e.g., zooplankton and larger-sized phytoplankton) are fed on by active consumers (e.g., planktivorous fish; Yahel et al. 2005) yet are also large enough to be directly intercepted by passive suspension feeders such as corals (Humphries 2009). Several studies have
examined the particular mechanics of zooplankton feeding by coral polyps in unidirectional flowing water (e.g., Sebens & Johnson 1991; Sebens et al. 1997, 1998). Although zooplankton feeding
rates (often referred to as capture efficiency rates) vary with coral species, coral colony morphology, and type of zooplankton prey, most studies have shown that capture rates are dependent on
flow speed. In many cases, these particle capture rates initially increase with higher flow as a result
of higher particle encounter rates but may eventually decrease at higher flow speeds when tentacles
are no longer able to fully extend against the strong flow (Sebens et al. 1997). Although particle
capture rates should also depend on the magnitude of a wave-driven oscillatory flow, there is a lack
of similar detailed studies under wave-dominated flow that are necessary to accurately quantify
these rates. Finally, an important fraction of suspended organic matter crossing through reef systems is remineralized in permeable reef sediments, whose pore-water chemistry and reaction rates
are also driven as much by hydrodynamics (i.e., wave and tidal pumping) as by infaunal metabolism
(Cyronak et al. 2013, Falter & Sansone 2000, Huettel & Rusch 2000, Santos et al. 2010).
Residence time: the
length of time that a
water parcel remains
within a domain (the
complement of water
age)
3. COMMUNITY TO REEF SYSTEM SCALES (10 m–10 km)
3.1. Reef Circulation
One of the most direct mechanisms by which physical ocean processes can influence the biology
and chemistry of coral reefs is through the circulation and residence time of reef waters (Figure 2).
For many reefs across the Indo-Pacific and Caribbean, circulation is driven mainly by breaking
surface waves (Hearn 1999, Hench et al. 2008, Lowe et al. 2009b, Munk & Sargent 1948,
Symonds et al. 1995). As open-ocean waves approach a reef, they break when the wave height
becomes a significant fraction of the water depth (Nelson 1994), although the exact break point is
msl
ηcr
η(x)
qr
qr
qc
Figure 2
Wave-driven circulation of a coastal reef-lagoon system. Waves approach the reef, shoal, and break near the reef crest. This generates a
rise in the dynamic sea level (η) relative to the offshore mean sea level (msl), referred to as wave setup, as well as an associated shoreward
flow of water (
q r ) across the shallow reef. The flow across the reef is balanced by the seaward flow of water (
q c ) through narrow
channels that perforate the reef structure.
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Wave setup: a local
elevation in mean sea
level that arises to
balance wave radiation
stress gradients
6:57
further affected by the nonlinearity of the waves and local bottom steepness (Buckley et al. 2014,
Massel & Gourlay 2000). The loss of wave energy via breaking through the surf zone leads to a
subsequent reduction in the radiation stress, or the excess momentum flux carried by the incident
waves (Longuet-Higgins & Stewart 1962). The resulting wave force generated by the radiation
stress gradient through the surf zone is opposed in part by an increase, or setup, of mean sea level
through the surf zone that raises the water level over the reef.
Shoreward of the surf zone, where wave dissipation becomes comparatively small, the dominant
momentum balance instead tends to be between the wave setup gradient (resulting from a decrease
in mean water level across the reef ) and the opposing bottom stress associated with the mean flow
of water driven across the reef (Gourlay & Colleter 2005, Lowe et al. 2009b, Symonds et al. 1995).
Although many one-dimensional analytical models have been developed to predict wave setup and
wave-driven flows on reefs, Gourlay & Colleter (2005) showed that the amount of wave setup at
the reef crest ηcr tends to be roughly proportional to the onshore deepwater wave energy flux and,
therefore, proportional to the offshore wave height H0 and period τw according to ηcr ∝ H 02 τw .
Assuming a quadratic dependency of bottom drag on flow speed with drag coefficient CD (see
Section 2), this implies that the cross-reef transport q is proportional to the square root of the
incident wave energy flux, or
q≡
√
H 0 τw
U (z)dz ≡ U h ∝ √
,
CD
−h
η
(5)
where h is the local water depth, η is the local free-surface height relative to the mean offshore
water level, and U is the depth-averaged flow speed. Therefore, the strength of the wave-driven
circulation tends to increase roughly linearly with the offshore wave height but also depends more
weakly on the wave period and the bottom-drag coefficient. Observations tend to generally support
the scaling of q in Equation 5 (e.g., Lowe et al. 2009b, Monismith et al. 2013), although the exact
magnitude of q that is generated in response to incident wave forcing can also vary substantially
among reef systems owing to the particular morphology of a reef-lagoon system and the degree
to which its channels restrict the return flow of water back to the surrounding ocean (Lowe et al.
2010, Monismith 2013, Taebi et al. 2011).
Tides can also play a secondary role influencing wave-driven circulation on wave-exposed
reef systems by modulating how and where waves break (Becker et al. 2014, Taebi et al. 2011).
Changes in tidal elevation can alter the position and width of the surf zone and therefore the rate
at which wave energy is dissipated, which in turn influences the magnitude of the wave setup. The
resistance experienced by cross-reef currents can also be substantially enhanced at lower phases of
the tide when flow becomes depth limited, significantly increasing the bottom-drag coefficients
(see Section 2) (McDonald et al. 2006, Pomeroy et al. 2012, Rosman & Hench 2011). Tidal forcing
may play a more direct role in driving reef circulation when the tidal range is large (e.g., >3 m)
and local tidal water level gradients can exceed those induced by wave setup fields.
In addition, tides can play a more direct role in driving circulation in larger and more enclosed
lagoons where the channels connecting the lagoon with the open ocean are relatively narrow. The
constricted exchange of water between these lagoons and the open ocean can cause significant
phase lags between a lagoon and offshore water levels (e.g., Dumas et al. 2012). Historically, most
reef studies have found that wind stresses often play only a minor role in driving the circulation
of shallow reefs; however, wind forcing can be important or even dominant in the circulation of
deeper and more isolated lagoons (Atkinson et al. 1981, Delesalle & Sournia 1992, Douillet et al.
2001, Lowe et al. 2009a). Unfortunately, the extent to which buoyancy forcing helps drive reef
circulation through either temperature- or salinity-driven stratification has received only limited
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study; however, this forcing may also be important in certain reef systems (Hoeke et al. 2013,
Monismith et al. 2006).
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3.2. Biogeochemical Transformation of Reef Waters
The degree to which any local process occurring within a reef (physical, chemical, or biological)
can affect the spatial and temporal variation in water quality is dependent as much on the strength
and pattern of circulation as on the process itself. These relationships can be understood either
from an Eulerian perspective, in which circulation and changing water quality are considered
within a fixed reference frame, or from a Lagrangian perspective, in which changes in water quality are observed within a defined water parcel flowing through a reef system. From an Eulerian
perspective, these relationships are best illustrated by the depth-integrated nonconservative transport equation, which shows the mutual dependence of spatial (∂/∂ x,∂/∂ y) and temporal (∂/∂t)
changes in water quality on both the transport q and the net flux of heat or mass into the water
column J (Falter et al. 2008):
J = h
flux
∂C
+ q · ∇C − K ∇ 2 C ,
dispersion
∂t
advection
Eulerian: examining a
dynamic flow field
from the perspective of
a fixed frame of
reference
Lagrangian:
examining a dynamic
flow field from the
perspective of a water
parcel moving with the
flow
(6)
local
where C is some nonconservative water quality parameter of interest (nutrient concentration,
alkalinity, temperature, etc.) and K is a horizontal dispersion coefficient. J can represent the sum of
all biogeochemical processes responsible for the uptake or release of nutrients, particles, dissolved
inorganic carbon, alkalinity, etc. It can also represent the net exchange of heat, moisture, and
gasses across the air-sea interface. Limited field measurements have shown that mass transport
resulting from advection is much greater than that resulting from horizontal dispersion (i.e.,
q·∇C K ∇ 2 C) on shallow, wave-driven reefs (Falter et al. 2008); however, horizontal dispersion
could be more important in reefs with strongly sheared two-dimensional circulation patterns.
Furthermore, a fully three-dimensional nonconservative transport equation may be necessary to
budget the uptake, release, and transport of mass in deeper and more stratified sections of a reef
(Genin et al. 2009, Monismith et al. 2010, Teneva et al. 2013).
The application of the nonconservative transport equation to model changes in water quality
has proven robust for inversely calculating benthic fluxes in shallow reef environments for more
than half a century (e.g., Odum & Odum 1955, Smith 1973), albeit through the use of simplified
versions of Equation 6. Earlier methodologies discriminated between flow respirometry, which
measures changes in water chemistry along one axis (generally oriented in the cross-reef direction)
and assumes that J ≈ q x ∂C/∂ x (Barnes & Devereux 1984, Gattuso et al. 1993, Kraines et al. 1997),
and the slack-water method, which considers only the time-dependent changes in water chemistry
at a specific site and assumes that J ≈ h∂C/∂t (Kinsey 1978, McMahon et al. 2013, Shaw et al.
2012). Both approaches constitute selective simplifications of the same Eulerian nonconservative
transport equation shown in Equation 6. The simplification of upstream-downstream applications
of flow respirometry tends to be most robust on shallow reef flats where the flow is both reasonably steady and strong (>5 cm s−1 ) and chemical gradients vary only weakly in time such that
q x ∂C/∂ x h∂C/∂t. The slack-water simplification generally requires flow speeds to be on the
order of ∼1 cm s−1 or less so that the time-dependent term dominates over the advective terms
(i.e., h∂C/∂t q ·∇C). This latter condition is particularly difficult to meet for two reasons. First,
it requires that the predominant current is very weak yet still strong enough to provide the necessary turbulent stirring to vertically mix the water column, a criterion that can easily be violated
(Kinsey 1978). Second, it requires that the horizontal gradients in water quality also be relatively
small, a criterion that is difficult to meet for many reefs given that the spatial distributions of
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Water age: the age of
a water parcel relative
to when it entered a
domain (the
complement of
residence time)
biomass and metabolism are known to vary by an order of magnitude or more (Andréfouët et al.
2001, Atkinson & Falter 2003, Kinsey 1985, Tanaka et al. 2011).
One additional process contributing to transport in reef systems is Stokes drift, or the excess
mass transport induced by the nonlinearity of waves (Longuet-Higgins & Stewart 1962). Stokes
drift is a depth-dependent, Lagrangian property of wave motion and thus cannot be directly
measured by time-averaging fixed-point current meter data; however, it can be estimated from
local wave measurements at a specific reef site. Stokes drift within the coastal zone can range from
several centimeters per second to tens of centimeters per second depending on the water depth,
wave height, and wave period (Monismith & Fong 2004). This can cause the total transport to be
far greater than that measured by fixed current meters alone, thus potentially distorting perceived
rates of material exchange (Falter et al. 2008). Which terms within the general transport equation
above (Equation 6) can or cannot be ignored, and whether Stokes drift should be considered, must
be carefully assessed for each reef environment on a case-by-case basis.
From a Lagrangian perspective, changes in water quality can also be understood by examining
the age and history of a water parcel after it enters a reef system (Figure 3a). Spatial circulation
patterns control the spatial distribution of local water ages or residence times across reefs and,
therefore, the time under which the water’s chemistry can be altered (Andréfouët et al. 2001,
Jouon et al. 2006, Lowe et al. 2009a, Zhang et al. 2012). The average water age can range from as
short as a few hours in shallower and more seaward reef habitats to days or weeks in deeper and
more interior sections of reef systems (Lowe et al. 2009a, Venti et al. 2012, Zhang et al. 2012).
The residence times within very deep (>20 m) atoll lagoons can reach several months depending
on the size of the atoll and how closed it is with respect to exchange with the ocean (Atkinson et al.
1981, Callaghan et al. 2006, Delesalle & Sournia 1992, Tartinville et al. 1997). Most importantly,
Residence
time (h)
40
τRT
a
6:57
ΔT
b
Change in
temperature (ºC)
0.8
35
0.7
30
0.6
25
0.5
20
0.4
15
0.3
10
0.2
5
0.1
0
0
ΔTA
c
Change in total
alkalinity (μeq kg–1)
100
80
60
40
20
0
Figure 3
Simulations of (a) residence time (τRT ) as well as changes in (b) daily average water column temperature (T ) and (c) daily average
water column total alkalinity (TA), both relative to offshore values across Coral Bay, Ningaloo Reef, under typical summer conditions
(Zhang et al. 2012, 2013). All simulations shown were performed using the Regional Ocean Modeling System (ROMS) coupled with
the spectral wave model Simulating Waves Nearshore (SWAN). The black lines highlight the 4-m isobath. For additional details, see
Zhang et al. (2012). Note that the high degree of similarity between T and TA in this application is largely the result of unusually
high coral cover within the Coral Bay lagoon—a feature not common in other sections of Ningaloo Reef or in many other Indo-Pacific
reef systems.
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residence times at any reef site can never be considered a static quantity because they are driven
by ever-changing wind, wave, and tide conditions.
Changes to the properties of a flowing water mass depend not only on the simple age of a water
parcel but also on the specific trajectory or streamline that determines the various reef habitats
the parcel is exposed to. Without explicit knowledge of the flow path that a given water mass
took prior to the measurement of its changed chemistry relative to some reference point (typically
offshore waters), it is not possible to know which sections or areas of reef habitat to assign these
observed changes to. This is particularly problematic when attempting to calculate benthic fluxes
and reaction rates for entire reef systems using bulk estimates of water residence time and local
measurements of water chemistry made at specific reef sites (Falter et al. 2013, Venti et al. 2012,
Zhang et al. 2012). Nonetheless, changes in the chemistry of offshore waters are generally most
rapid over the most seaward several hundred meters of shallow reef flat. These changes can be well
described by a simple analytical equation that depends on offshore wave forcing, reef morphology,
and the net benthic and surface mass fluxes (Falter et al. 2013):
2 3/4
Lr
J
,
(7)
C ∝
√
H 0 τw h r
Albedo: the fraction
of solar radiation that a
surface or object
reflects
where Lr and hr are the length and depth of the reef flat, respectively, and advection is assumed to
be the dominant transport term (q · ∇C ∂C/∂t).
3.3. Temperature Variations in Reef Waters
The dynamics driving spatial and temporal changes in water temperature across reefs
(Figure 3b) are analogous to those driving changes in water chemistry (Figure 3c) because they
are both governed by the same fundamental nonconservative transport equation (Equation 6)
(Davis et al. 2011, Falter et al. 2014, McCabe et al. 2010, Zhang et al. 2013). The additional heat
gained by reef waters from atmospheric exchange can have profound effects on local temperature
anomalies and cumulative thermal stresses on reefs (Davis et al. 2011, Falter et al. 2014, McCabe
et al. 2010, Pineda et al. 2013, Zhang et al. 2013). In contrast to rates of benthic reef metabolism,
which can vary by more than an order of magnitude (Andersson & Gledhill 2013, Kinsey 1985),
net heat fluxes are far less spatially variable across reefs. First, spatial variations in atmospheric
conditions (e.g., air temperatures, humidity, and wind speeds) that drive net surface and bottom
heat fluxes (J ) are limited over the scale of an individual reef (McGowan et al. 2010, Weller
et al. 2008). Second, the capacities of different reef communities to absorb shortwave radiation
(dependent on their albedo) generally vary by less than a factor of 2 (Hochberg et al. 2003).
Third, a substantial fraction of shortwave radiation is absorbed by the water column itself, and
this proportion increases with water depth. The end result is that spatial variation in bottom
albedo resulting from a changing benthic reef habitat usually has only a secondary effect on the
net heating or cooling of reef waters, even for very shallow reef systems (Zhang et al. 2013).
4. REGIONAL TO GLOBAL SCALES (>10 km)
4.1. Global Distribution of Wave and Tidal Forcing
With only a few exceptions, studies have found that the circulation of reefs is dominantly forced
by waves, or in some cases by tides (Andréfouët et al. 2006, Falter et al. 2013, Monismith 2007).
Although the three-dimensional circulation of reef slopes and lagoons can be strongly influenced by
local wind forcing (Atkinson et al. 1981, Wolanski & Thomson 1984) as well as by buoyancy forcing
from thermal gradients (Monismith et al. 2006) or freshwater discharge (Hoeke et al. 2013), these
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Hs (m)
3
a
2
0°
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Latitude
0°
20°N
60°E
120E°
180°
120°W
60°W
0°
0
MTR (m)
3
c
2
0°
1
20°S
0°
20°N
10
1
20°S
60°E
120E°
180°
120°W
60°W
0°
e
0°
0
b
20
0
Frequency (%)
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20
1
Hs (m)
2
3
2
3
2
3
d
10
0
MTR/Hs
3
20
2
10
0
1
MTR (m)
f
1
20°S
0°
60°E
120E°
180°
Longitude
120°W
60°W
0°
0
0
0
1
MTR/Hs
Figure 4
Global spatial distributions and frequency distributions of (a,b) annual mean significant wave height (Hs ), (c,d ) mean tidal range (MTR),
and (e,f ) relative tidal range (MTR/Hs ) for warm-water coral reef systems. Global coral reef distributions are from the 1-km-resolution
data set from UNEP-WCMC (2003) and were joined with global wave height and tide distributions. Annual significant wave heights
were derived using data from Young et al. (2011). Mean tidal ranges were computed from tidal harmonics derived from the Oregon
State University Tidal Inversion Software (OTIS) (Egbert & Erofeeva 2002). Note that the values in all panels are capped at a
maximum of 3, so some reefs may experience larger mean values.
Macrotidal reef
system: a reef system
where the tidal range
exceeds 3 m
56
effects tend to be dominant only on reefs protected from ocean swell or within the relatively deep
lagoons of barrier reefs and atolls. There are strong regional differences in the global distribution of
significant wave heights Hs within the ± 30◦ latitude band where warm-water coral reefs are found
(Figure 4). Reefs in the Pacific and Indian Oceans tend to be dominantly wave forced (annual mean
Hs > 1.5 m), whereas reefs in the Caribbean, Southeast Asia, and northern parts of Australia tend
to experience only weak to moderate wave forcing (typical annual mean Hs < 1 m). These patterns
likely drive substantial regional-scale differences in the wave-driven flows and residence times
within reefs, depending, of course, on the morphologies of individual reefs within each region (see
Section 3).
Despite the dominance of wave-driven reef systems globally, there are still numerous reef
systems worldwide that can be considered tide dominated, defined here simply as locations where
the ratio of the mean tidal range (MTR) to the annual mean Hs is greater than 1 (Figure 4).
Such systems have for the most part remained neglected in the literature; they include some
extreme examples of macrotidal reef systems (MTR > 3 m) in regions off northern Australia, off
east Africa, and off Central and South America (Figure 4). For example, in the Kimberley region
of northwestern Australia, where numerous reefs are subject to tidal ranges greater than 10 m,
water frequently drains off reef terraces as “waterfalls” during ebb phases of the tide (Figure 5).
The dynamics of these tide-dominated reef systems, where the strongly varying flows lead to a
critical flow point at the reef terrace that restricts flow, are fundamentally different from those of
traditional wave-driven coral reef flows, in which flow resistance is due solely to bottom drag. A
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a
b
Figure 5
(a) A macrotidal reef system in the Kimberley region of northwestern Australia, where the spring tidal range reaches up to 10 m
(photograph by R.J. Lowe). The photograph shows the reef at low tide with water draining off the coralline algal reef platform as a
“waterfall.” (b) A schematic of water draining off an emergent macrotidal reef island at low tide.
much-improved understanding of tide-dominated reef systems is necessary to ultimately develop
appropriate predictive models of these very distinct coastal flows.
Whereas tidal forcing is predictable and quasi-stationary over long timescales (i.e., governed by
set tidal harmonics), wave forcing on reefs is often episodic and subject to extreme events. Extreme
wave events generated by tropical cyclones may be rare and short lived; however, the large wave
heights and storm surges generated can have a profound and long-lasting impact on coral reef
ecosystems. In addition, large extratropical cyclones in the major ocean basins may also transmit
large swell across the ocean to remote reef systems thousands of kilometers away—as occurs, for
example, when large waves generated by remote storms impart substantial wave energy to Pacific
island reefs (Hench et al. 2008). Overall, it appears that, for many reefs, these extreme wave events
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play a primary role in shaping the reef community composition and zonation by establishing the
mechanical limits of various reef organisms (Dollar & Tribble 1993, Grigg 1998, Lugo-Fernández
& Gravois 2010, Madin & Connolly 2006). Other investigators have also argued that long-term
trends in the frequency of extreme wave events can drive associated declines in coral coverage
of reefs. For example, De’ath et al. (2012) argued that one major cause for the decline in coral
coverage across the Great Barrier Reef over the past ∼30 years was the number of unusually strong
tropical cyclones.
4.2. Offshore Ocean Interactions with Reefs
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Offshore ocean dynamics are gaining increasing recognition for the critical role they play in
driving many reef ecosystem processes (Freeman et al. 2012, Gove et al. 2013, Wyatt et al. 2012).
Nevertheless, our quantitative understanding of how reefs are connected to the surrounding ocean
remains poor owing to both the complex nature of these interactions and the lack of comprehensive
studies that simultaneously consider reef ecosystem dynamics over a broad range of relevant scales
(from regional down to community scales). At the broadest scale—that of entire ocean basins—the
presence of major ocean boundary currents has long been known to regulate the distribution of
many tropical coral reef systems globally. The general lack of major coral reef systems on the
continental shelves of eastern ocean basins has been attributed largely to persistent upwellingfavorable conditions generated by wind-driven, equatorward-flowing eastern boundary currents
that can inhibit the formation of oligotrophic tropical reefs (Birkeland 1997). In fact, many reefs
across the globe depend on regional ocean currents to provide thermal conditions favorable for
reef growth. Some good examples are the high-latitude coral reefs found between 28◦ S and 32◦ S
off the coasts of eastern and western Australia (Lord Howe Island and the Houtman-Abrolhos
Islands, respectively); these reef systems exist much farther south than those in other parts of the
Southern Hemisphere owing to the poleward transport of heat by the East Australian Current
and the Leeuwin Current. Nevertheless, predictions of how coral reef systems respond to global
climate variability have tended to neglect how subtle changes in regional ocean circulation patterns
may locally affect reefs in the future, instead tending to assume that reefs will be exposed only to
ocean-basin-scale changes in temperature and carbonate chemistry (e.g., Hoegh-Guldberg et al.
2007, Silverman et al. 2009).
A growing body of literature has described how a wide range of transient hydrodynamic processes on the shelf or slopes offshore of reefs influence shallow inshore reef systems. Multiple
studies have identified coastal upwelling in particular as an important mechanism driving the
cross-shelf exchange of nutrients between the ocean and many reefs; these studies include several that have examined how wind- or current-driven upwelling contributes substantial fluxes of
subsurface nutrients to the Great Barrier Reef (Andrews & Gentien 1982, Brinkman et al. 2002,
Wolanski et al. 1988) and to Ningaloo Reef off western Australia (Wyatt et al. 2010, 2012) as well
as through the secondary flows generated by island wakes in the Pacific (Gove et al. 2006). Studies
have also demonstrated that coastal upwelling significantly cools the coastal waters surrounding
some coral reefs, suggesting that these regions could provide some refuge from increased ocean
warming (e.g., Chollett & Mumby 2013, Karnauskas & Cohen 2012, Riegl & Piller 2003, Van
Hooidonk et al. 2013). Indeed, frequent, episodic upwelling can locally reduce water temperatures
by up to several degrees in reef systems ranging from northwestern Australia (Lowe et al. 2012)
to the Caribbean, the Red Sea, and the eastern coastlines of Africa (Riegl & Piller 2003).
Higher-frequency internal waves are similarly well known to drive substantial cross-shelf fluxes
of nutrients, plankton, and heat both to and from many coral reefs. The most comprehensive
observations of these dynamics have come from studies of internal waves off the Florida Keys (Davis
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et al. 2008; Leichter et al. 1996, 2003) and in French Polynesia (Leichter et al. 2012, Wolanski &
Delesalle 1995). Despite the clear importance of internal waves to cross-shelf exchange in these
regions, their specific influence on the nutrient and heat budgets of reefs in other parts of the
world remains poorly known. Ultimately, our understanding of how shallow reef systems respond
to the larger-scale dynamics of the surrounding ocean (including those driven by coastal upwelling,
internal waves, coastal eddy fields, and episodic extreme events such as tropical cyclone mixing)
remains primitive.
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SUMMARY POINTS
1. The oceans influence the structure and function of coral reefs through a variety of mechanisms, ranging from small-scale boundary-layer dynamics occurring on submillimeter
scales to regional circulation patterns spanning hundreds of kilometers.
2. Mass and momentum exchange within and above coral reef canopies can differ substantially depending on the prevailing flow regime. Under unconfined, unidirectional flow,
flow within the canopy is driven primarily by a shear layer at the top of the canopy and is
relatively weak. Under severely depth-limited flow or wave-driven oscillatory flow, flow
within the canopy is driven primarily by pressure gradients and is much stronger.
3. Rates of dissolved nutrient and particle uptake by reef communities are heavily influenced
by the predominant boundary-layer physics; however, mechanisms of particle trapping
and feeding are highly varied, and their physics are still not well understood.
4. Circulation across most shallow reef systems is wave driven, with the tides acting as a
secondary variable modulating wave-driven flows. However, in some regions the direct
forcing of reef circulation by tides is much stronger than by waves.
5. Spatial and temporal changes in reef water temperature and chemistry are intrinsically
linked through a balance between the net fluxes of heat or mass that drive their nonconservative behavior and the circulation of reef waters. The circulation, residence times,
and ages of reef waters are, in turn, dependent on the hydrodynamic forces driving the
flow as well as the particular morphology of a given reef system.
6. Episodic upwelling and internal waves can provide short-term (days) and intermediatescale (kilometers) mechanisms through which coral reefs are exposed to cooler and more
nutrient- and/or plankton-rich waters. Longer-term changes in regional circulation patterns (weeks to months) can either provide conditions favorable for reef growth or help
foment large-scale thermal stress events (tens to hundreds of kilometers).
FUTURE ISSUES
1. Predicting flow and drag forces within the complex and varied morphologies of reef
canopies remains a major challenge. New experimental data sets and modeling approaches
are needed to further advance predictions of reef canopy flows under both unidirectional
and wave-driven conditions.
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2. Likewise, existing nearshore models neglect how bottom drag under waves and currents is
influenced by in-canopy momentum dynamics. Improving the parameterizations of these
canopy-scale dynamics, including coupling them within wave and circulation models,
would no doubt substantially improve hydrodynamic models in reef applications.
3. Although existing mass-transfer formulations provide some ability to predict rates of
dissolved nutrient uptake by reef communities, there are still major gaps in our knowledge
of nutrient mass transfer under wave-driven oscillatory flow.
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4. Some empirical data on particle uptake rates by reef communities are available, but
mechanistic approaches for modeling these dynamics are virtually nonexistent. The dependency of uptake rates on the mechanism of particle capture, as well as on the size and
composition of the particles themselves, makes this a particularly challenging research
endeavor.
5. Little is known about circulation around reefs with relatively large tidal ranges (mean tidal
range of >3 m) and how this affects the spatial and temporal variation in reef metabolism
and water quality. Such systems should be given greater attention.
6. Multiple studies over the past two decades have documented the short-term (days) impact
of coastal upwelling and internal waves on the temperature, chemistry, and plankton
communities of reef waters. However, our understanding of how important these episodic
events are to the growth and structure of reef communities over the long term (months
to years) is very limited, as is our understanding of how they are mechanistically linked
to climate-driven changes in regional ocean dynamics.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We dedicate this review to Marlin Atkinson (1951–2013), who will be remembered as a pioneer
in the study of ocean forcing of reef ecosystems and who helped inspire our own interest in
this subject more than a decade ago. Through the years, we have learned much about coral
reefs through collaboration with colleagues and friends in the research community, especially
Stephen Monismith, Jeff Koseff, Eric Hochberg, Graham Symonds, Greg Ivey, Steve Smith,
Frank Sansone, Mark Merrifield, Carlos Coimbra, Pascale Cuet, Alex Wyatt, Zhenlin Zhang,
Malcolm McCulloch, Richard Brinkman, Chari Pattiaratchi, Dan Schar, Jerome Aucan, Christine
Pequignet, Uri Shavit, Geno Pawlak, Serge Andréfouët, Frazer McGregor, Andrew Pomeroy,
Mark Buckley, Ap van Dongeren, Dano Roelvink, Stuart Humphries, Ben Radford, Nicole Jones,
Curt Storlazzi, Renee Gruber, Mike Cuttler, Gundula Winter, Edwin Drost, Soheila Taebi, Cecile
Rousseaux, Jim Hench, Johanna Rosman, Sam Kahng, Matt Reidenbach, and Sandy Chang. We
also thank Stefan Zieger and Ian Young for providing the mean global wave height data used in
Figure 3. Support for this work was provided by the Australian Research Council (ARC) Centre
of Excellence for Coral Reef Studies (CE140100020). R.J.L. is also grateful for support from
ARC under both the Future Fellowship (FT110100201) and Discovery Projects (DP140102026)
60
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schemes. This work was also partially supported by a grant from the Western Australia Marine
Science Institution (WAMSI) under the Kimberley Marine Research Program.
Annu. Rev. Marine. Sci. 2015.7:43-66. Downloaded from www.annualreviews.org
Access provided by University of Western Australia on 01/30/15. For personal use only.
LITERATURE CITED
Andersson AJ, Gledhill D. 2013. Ocean acidification and coral reefs: effects on breakdown, dissolution, and
net ecosystem calcification. Annu. Rev. Mar. Sci. 5:321–48
Andréfouët S, Ouillon S, Brinkman R, Falter JL, Douillet P, et al. 2006. Review of solutions for 3D hydrodynamic modeling applied to aquaculture in South Pacific atoll lagoons. Mar. Pollut. Bull. 52:1138–55
Andréfouët S, Pagès J, Tartinville B. 2001. Water renewal time for classification of atoll lagoons in the Tuamotu
Archipelago (French Polynesia). Coral Reefs 20:399–408
Andrews JC, Gentien P. 1982. Upwelling as a source of nutrients for the Great Barrier Reef ecosystems: a
solution to Darwin’s question? Mar. Ecol. Prog. Ser. 8:257–69
Atkinson MJ, Bilger RW. 1992. Effect of water velocity on phosphate uptake in coral reef-flat communities.
Limnol. Oceanogr. 37:273–79
Atkinson MJ, Falter JL. 2003. Coral reefs. In Biogeochemistry of Marine Systems, ed. KP Black, GB Shimmield,
pp. 40–64. Boca Raton, FL: CRC
Atkinson MJ, Smith S, Stroup E. 1981. Circulation in Enewetak atoll lagoon. Limnol. Oceanogr. 26:1074–83
Ayukai T. 1995. Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier
Reef, Australia. Coral Reefs 14:141–47
Baird ME, Atkinson MJ. 1997. Measurement and prediction of mass transfer to experimental coral reef
communities. Limnol. Oceanogr. 42:1685–93
Barnes D, Devereux M. 1984. Productivity and calcification on a coral reef: a survey using pH and oxygen
electrode techniques. J. Exp. Mar. Biol. Ecol. 79:213–31
Becker J, Merrifield M, Ford M. 2014. Water level effects on breaking wave setup for Pacific Island fringing
reefs. J. Geophys. Res. 119:914–32
Bilger RW, Atkinson MJ. 1992. Anomalous mass transfer of phosphate on coral reef flats. Limnol. Oceanogr.
37:261–72
Birkeland C, ed. 1997. Life and Death of Coral Reefs. New York: Springer
Brinkman R, Wolanski E, Deleersnijder E, McAllister F, Skirving W. 2002. Oceanic inflow from the Coral
Sea into the Great Barrier Reef. Estuar. Coast. Shelf Sci. 54:655–68
Bruno JF, Siddon CE, Witman JD, Colin PL, Toscano MA. 2001. El Niño related coral bleaching in Palau,
Western Caroline Islands. Coral Reefs 20:127–36
Buckley M, Lowe RJ, Hansen J. 2014. Evaluation of nearshore wave models in steep reef environments. Ocean
Dyn. 64:847–62
Callaghan DP, Nielsen P, Cartwright N, Gourlay MR, Baldock TE. 2006. Atoll lagoon flushing forced by
waves. Coast. Eng. 53:691–704
Chang S, Elkins C, Alley M, Eaton J, Monismith SG. 2009. Flow inside a coral colony measured using magnetic
resonance velocimetry. Limnol. Oceanogr. 54:1819
Charpy L, Blanchot J. 1999. Picophytoplankton biomass, community structure and productivity in the Great
Astrolabe Lagoon, Fiji. Coral Reefs 18:255–62
Chindapol N, Kaandorp JA, Cronemberger C, Mass T, Genin A. 2013. Modelling growth and form of the
scleractinian coral Pocillopora verrucosa and the influence of hydrodynamics. PLoS Comput. Biol. 9:e1002849
Chollett I, Mumby PJ. 2013. Reefs of last resort: locating and assessing thermal refugia in the wider Caribbean.
Biol. Conserv. 167:179–86
Cyronak T, Santos I, McMahon A, Eyre B. 2013. Carbon cycling hysteresis in permeable carbonate sands
over a diel cycle: Implications for ocean acidification. Limnol. Oceanogr. 58:131–43
Darwin C. 1842. The Structure and Distribution of Coral Reefs. London: Smith Elder & Co.
Davis KA, Leichter JJ, Hench JL, Monismith SG. 2008. Effects of western boundary current dynamics on the
internal wave field of the Southeast Florida shelf. J. Geophys. Res. 113:C09010
Davis KA, Lentz SJ, Pineda J, Farrar JT, Starczak VR, Churchill JH. 2011. Observations of the thermal
environment on Red Sea platform reefs: a heat budget analysis. Coral Reefs 30:25–36
www.annualreviews.org • Oceanic Forcing of Coral Reefs
61
ARI
29 October 2014
6:57
De’ath G, Fabricius KE, Sweatman H, Puotinen M. 2012. The 27-year decline of coral cover on the Great
Barrier Reef and its causes. Proc. Natl. Acad. Sci. USA 109:17995–99
Delesalle B, Sournia A. 1992. Residence time of water and phytoplankton biomass in coral-reef lagoons. Cont.
Shelf Res. 12:939–49
Depczynski M, Gilmour J, Ridgway T, Barnes H, Heyward A, et al. 2013. Bleaching, coral mortality and
subsequent survivorship on a West Australian fringing reef. Coral Reefs 32:233–38
Dollar SJ, Tribble GW. 1993. Recurrent storm disturbance and recovery: a long-term study of coral communities in Hawaii. Coral Reefs 12:223–33
Douillet P, Ouillon S, Cordier E. 2001. A numerical model for fine suspended sediment transport in the
southwest lagoon of New Caledonia. Coral Reefs 20:361–72
Dumas F, Gendre RL, Thomas Y, Andréfouët S. 2012. Tidal flushing and wind driven circulation of Ahe atoll
lagoon (Tuamotu Archipelago, French Polynesia) from in situ observations and numerical modelling.
Mar. Pollut. Bull. 65:425–40
Egbert GD, Erofeeva SY. 2002. Efficient inverse modeling of barotropic ocean tides. J. Atmos. Ocean. Technol.
19:183–204
Espinosa-Gayosso A, Ghisalberti M, Ivey GN, Jones NL. 2012. Particle capture and low-Reynolds-number
flow around a circular cylinder. J. Fluid Mech. 710:362–78
Fabricius KE, Yahel G, Genin A. 1998. In situ depletion of phytoplankton by an azoothanthallae soft coral.
Limnol. Oceanogr. 43:354–56
Falter JL, Atkinson MJ, Merrifield MA. 2004. Mass-transfer limitation of nutrient uptake by a wave-dominated
reef flat community. Limnol. Oceanogr. 49:1820–31
Falter JL, Lowe RJ, Atkinson MJ, Monismith SG, Schar DW. 2008. Continuous measurements of net production over a shallow reef community using a modified Eulerian approach. J. Geophys. Res. 113:C07035
Falter JL, Lowe RJ, Zhang Z, McCulloch M. 2013. Physical and biological controls on the carbonate chemistry
of coral reef waters: effects of metabolism, wave forcing, sea level, and geomorphology. PLoS ONE
8:e53303
Falter JL, Sansone FJ. 2000. Hydraulic control of pore water geochemistry within the oxic-suboxic zone of a
permeable sediment. Limnol. Oceanogr. 45:550–57
Falter JL, Zhang ZL, Lowe RJ, McGregor F, Keesing J, McCulloch M. 2014. Assessing seasonal and spatial
temperature variability within coral reefs through in situ observations and global climate data. Limnol.
Oceanogr. 59:1241–55
Ferrier-Pagès C, Witting J, Tambutté E, Sebens K. 2003. Effect of natural zooplankton feeding on the tissue
and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–40
Freeman LA, Miller AJ, Norris RD, Smith JE. 2012. Classification of remote Pacific coral reefs by physical
oceanographic environment. J. Geophys. Res. 117:C02007
Gattuso J-P, Pichon M, Delesalle B, Frankignoulle M. 1993. Community metabolism and air-sea CO2 fluxes
in a coral reef ecosystem (Moorea, French Polynesia). Mar. Ecol. Prog. Ser. 96:259–67
Genin A, Monismith SG, Reidenbach MA, Yahel G, Koseff JR. 2009. Intense benthic grazing of phytoplankton
in a coral reef. Limnol. Oceanogr. 54:938–51
Ghisalberti M. 2009. Obstructed shear flows: similarities across systems and scales. J. Fluid Mech. 641:51–61
Gourlay M, Colleter G. 2005. Wave-generated flow on coral reefs: an analysis for two-dimensional horizontal
reef-tops with steep faces. Coast. Eng. 52:353–87
Gove JM, Merrifield MA, Brainard RE. 2006. Temporal variability of current-driven upwelling at Jarvis Island.
J. Geophys. Res. 111:C12011
Gove JM, Williams G, McManus M. 2013. Quantifying climatological ranges and anomalies for Pacific coral
reef ecosystems. PLoS ONE 8:e61974
Grigg RW. 1998. Holocene coral reef accretion in Hawaii: a function of wave exposure and sea level history.
Coral Reefs 17:263–72
Hamner W, Wolanski E. 1988. Hydrodynamic forcing functions and biological processes on coral reefs: a
status review. In Proceedings of the 6th International Coral Reef Symposium, Vol. 1: Plenary Addresses and Status
Review, ed. JH Choat, D Barnes, MA Borowitzka, JC Coll, PJ Davies, et al., pp. 103–13. Townsville, Aust.:
Int. Coral Reef Symp. Exec. Comm.
Annu. Rev. Marine. Sci. 2015.7:43-66. Downloaded from www.annualreviews.org
Access provided by University of Western Australia on 01/30/15. For personal use only.
MA07CH03-Lowe
62
Lowe
·
Falter
Annu. Rev. Marine. Sci. 2015.7:43-66. Downloaded from www.annualreviews.org
Access provided by University of Western Australia on 01/30/15. For personal use only.
MA07CH03-Lowe
ARI
29 October 2014
6:57
Hearn CJ. 1999. Wave-breaking hydrodynamics within coral reef systems and the effect of changing relative
sea level. J. Geophys. Res. 104:30007–19
Hearn CJ, Atkinson MJ, Falter JL. 2001. A physical derivation of nutrient-uptake rates in coral reefs: effects
of roughness and waves. Coral Reefs 20:347–56
Hench JL, Leichter JJ, Monismith SG. 2008. Episodic circulation and exchange in a wave-driven coral reef
and lagoon system. Limnol. Oceanogr. 53:2681–94
Hochberg E, Atkinson M, Andréfouët S. 2003. Spectral reflectance of coral reef bottom-types worldwide and
implications for coral reef remote sensing. Remote Sens. Environ. 85:159–73
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. 2007. Coral reefs under rapid
climate change and ocean acidification. Science 318:1737–42
Hoeke RK, Storlazzi CD, Ridd PV. 2013. Drivers of circulation in a fringing coral reef embayment: a wave-flow
coupled numerical modeling study of Hanalei Bay, Hawaii. Cont. Shelf Res. 58:79–95
Houlbrèque F, Ferrier-Pagès C. 2009. Heterotrophy in tropical scleractinian corals. Biol. Rev. Camb. Philos.
Soc. 84:1–17
Houlbrèque F, Tambutté E, Allemand D, Ferrier-Pagès C. 2004. Interactions between zooplankton feeding,
photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J. Exp. Biol. 207:1461–69
Huettel M, Rusch A. 2000. Transport and degradation of phytoplankton in permeable sediment. Limnol.
Oceanogr. 45:534–49
Hughes AD, Grottoli AG. 2013. Heterotrophic compensation: a possible mechanism for resilience of coral
reefs to global warming or a sign of prolonged stress? PLoS ONE 8:e81172
Humphries S. 2009. Filter feeders and plankton increase particle encounter rates through flow regime control.
Proc. Natl. Acad. Sci. USA 106:7882–87
Jouon A, Douillet P, Ouillon S, Fraunié P. 2006. Calculations of hydrodynamic time parameters in a semiopened coastal zone using a 3D hydrodynamic model. Cont. Shelf Res. 26:1395–415
Kaandorp JA, Koopman EA, Sloot PM, Bak RP, Vermeij MJ, Lampmann LE. 2003. Simulation and analysis
of flow patterns around the scleractinian coral Madracis mirabilis (Duchassaing and Michelotti). Philos.
Trans. R. Soc. Lond. B 358:1551–57
Karnauskas KB, Cohen AL. 2012. Equatorial refuge amid tropical warming. Nat. Clim. Change 2:530–34
Kinsey DW. 1978. Productivity and calcification estimates using slack-water periods and field enclosures. In
Coral Reefs: Research Methods, ed. DR Stoddart, RE Johannes, pp. 439–68. Paris: UNESCO
Kinsey DW. 1985. Metabolism, calcification, and carbon production: I. Systems level studies. In Proceedings of
the Fifth International Coral Reef Congress, Vol. 4: Symposia and Seminars, ed. C Gabrie, B Salvat, pp. 505–26.
Moorea, Fr. Polyn.: Antenne Mus.–EPHE
Kraines S, Suzuki Y, Omori T, Shitashima K, Kanahara S, Komiyama H. 1997. Carbonate dynamics of the
coral reef system at Bora Bay, Miyako Island. Mar. Ecol. Prog. Ser. 156:1–16
Lai S, Gillis LG, Mueller C, Bouma TJ, Guest JR, et al. 2013. First experimental evidence of corals feeding
on seagrass matter. Coral Reefs 32:1061–64
Leal MC, Ferrier-Pagès C, Calado R, Thompson ME, Frischer ME, Nejstgaard JC. 2014. Coral feeding on
microalgae assessed with molecular trophic markers. Mol. Ecol. 23:3870–76
Leichter JJ, Stewart HL, Miller SL. 2003. Episodic nutrient transport to Florida coral reefs. Limnol. Oceanogr.
48:1394–407
Leichter JJ, Stokes MD, Hench JL, Witting J, Washburn L. 2012. The island-scale internal wave climate of
Moorea, French Polynesia. J. Geophys. Res. 117:C06008
Leichter JJ, Wing SR, Miller SL, Denny MW. 1996. Pulsed delivery of subthermocline water to Conch Reef
(Florida Keys) by internal tidal bores. Limnol. Oceanogr. 41:1490–501
Longuet-Higgins MS, Stewart RW. 1962. Radiation stress and mass transport in gravity waves, with application
to surf beats. J. Fluid Mech. 13:481–504
Lowe RJ, Falter JL, Monismith SG, Atkinson MJ. 2009a. A numerical study of circulation in a coastal reeflagoon system. J. Geophys. Res. 114:C06022
Lowe RJ, Falter JL, Monismith SG, Atkinson MJ. 2009b. Wave-driven circulation of a coastal reef-lagoon
system. J. Phys. Oceanogr. 39:873–93
Lowe RJ, Hart C, Pattiaratchi CB. 2010. Morphological constraints to wave-driven circulation in coastal
reef-lagoon systems: a numerical study. J. Geophys. Res. 115:C09021
www.annualreviews.org • Oceanic Forcing of Coral Reefs
63
ARI
29 October 2014
6:57
Lowe RJ, Ivey GN, Brinkman RM, Jones NL. 2012. Seasonal circulation and temperature variability near the
North West Cape of Australia. J. Geophys. Res. 117:C04010
Lowe RJ, Koseff JR, Monismith SG. 2005a. Oscillatory flow through submerged canopies: 1. Velocity structure. J. Geophys. Res. 110:C10016
Lowe RJ, Koseff JR, Monismith SG, Falter JL. 2005b. Oscillatory flow through submerged canopies: 2. Canopy
mass transfer. J. Geophys. Res. 110:C10017
Lowe RJ, Shavit U, Falter JL, Koseff JR, Monismith SG. 2008. Modeling flow in coral communities with and
without waves: a synthesis of porous media and canopy flow approaches. Limnol. Oceanogr. 53:2668–80
Lugo-Fernández A, Gravois M. 2010. Understanding impacts of tropical storms and hurricanes on submerged
bank reefs and coral communities in the northwestern Gulf of Mexico. Cont. Shelf Res. 30:1226–40
Macdonald IF, Elsayed MS, Mow K, Dullien FAL. 1979. Flow through porous media—the Ergun equation
revisited. Ind. Eng. Chem. Fundam. 18:199–208
Madin JS, Connolly SR. 2006. Ecological consequences of major hydrodynamic disturbances on coral reefs.
Nature 444:477–80
Manzello DP. 2010. Ocean acidification hot spots: spatiotemporal dynamics of the seawater CO2 system of
eastern Pacific coral reefs. Limnol. Oceanogr. 55:239–48
Massel SR, Done TJ. 1993. Effects of cyclone waves on massive coral assemblages on the Great Barrier Reef:
meteorology, hydrodynamics and demography. Coral Reefs 12:153–66
Massel SR, Gourlay MR. 2000. On the modelling of wave breaking and set-up on coral reefs. Coast. Eng.
39:1–27
McCabe RM, Estrade P, Middleton JH, Melville WK, Roughan M, Lenain L. 2010. Temperature variability
in a shallow, tidally isolated coral reef lagoon. J. Geophys. Res. 115:C12011
McClanahan TR, Baird AH, Marshall PA, Toscano MA. 2004. Comparing bleaching and mortality responses
of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar. Pollut. Bull. 48:327–35
McDonald CB, Koseff JR, Monismith SG. 2006. Effects of the depth to coral height ratio on drag coefficients
for unidirectional flow over coral. Limnol. Oceanogr. 51:1294–301
McGowan HA, Sturman AP, MacKellar MC, Wiebe AH, Neil DT. 2010. Measurements of the local energy
balance over a coral reef flat, Heron Island, southern Great Barrier Reef, Australia. J. Geophys. Res.
115:D19124
McMahon A, Santos IR, Cyronak T, Eyre BD. 2013. Hysteresis between coral reef calcification and the
seawater aragonite saturation state. Geophys. Res. Lett. 40:4675–79
Meinshausen M, Meinshausen N, Hare W, Raper SC, Frieler K, et al. 2009. Greenhouse-gas emission targets
for limiting global warming to 2◦ C. Nature 458:1158–62
Monismith SG. 2007. Hydrodynamics of coral reefs. Annu. Rev. Fluid Mech. 39:37–55
Monismith SG. 2013. Flow through a rough, shallow reef. Coral Reefs 33:99–104
Monismith SG, Davis KA, Shellenbarger GG, Hench JL, Nidzieko NJ, et al. 2010. Flow effects on benthic
grazing on phytoplankton by a Caribbean reef. Limnol. Oceanogr. 55:1881–92
Monismith SG, Fong DA. 2004. A note on the potential transport of scalars and organisms by surface waves.
Limnol. Oceanogr. 49:1214–17
Monismith SG, Genin A, Reidenbach MA, Yahel G, Koseff JR. 2006. Thermally driven exchanges between a
coral reef and the adjoining ocean. J. Phys. Oceanogr. 36:1332–47
Monismith SG, Herdman LM, Ahmerkamp S, Hench JL. 2013. Wave transformation and wave-driven flow
across a steep coral reef. J. Phys. Oceanogr. 43:1356–79
Moore JA, Bellchambers LM, Depczynski MR, Evans RD, Evans SN, et al. 2012. Unprecedented mass
bleaching and loss of coral across 12 of latitude in Western Australia in 2010–11. PLoS ONE 7:e51807
Munk WH, Sargent MC. 1948. Adjustment of Bikini Atoll to ocean waves. Trans. Am. Geophys. Union 29:855–
60
Munk WH, Sargent MC. 1954. Adjustment of Bikini Atoll to ocean waves. In Bikini and Nearby Atolls: Part
2. Oceanography (Physical), pp. 275–80. US Geol. Surv. Prof. Pap. 260. Washington, DC: US Gov. Print.
Off.
Nelson RC. 1994. Depth limited design wave heights in very flat regions. Coast. Eng. 23:43–59
Nepf HM. 2012. Flow and transport in regions with aquatic vegetation. Annu. Rev. Fluid Mech. 44:123–42
Annu. Rev. Marine. Sci. 2015.7:43-66. Downloaded from www.annualreviews.org
Access provided by University of Western Australia on 01/30/15. For personal use only.
MA07CH03-Lowe
64
Lowe
·
Falter
Annu. Rev. Marine. Sci. 2015.7:43-66. Downloaded from www.annualreviews.org
Access provided by University of Western Australia on 01/30/15. For personal use only.
MA07CH03-Lowe
ARI
29 October 2014
6:57
Nepf HM, Vivoni ER. 2000. Flow structure in depth-limited vegetative flow. J. Geophys. Res. 105:28547–57
Odum HT, Odum EP. 1955. Trophic structure and productivity of a windward coral reef community on
Eniwetok atoll. Ecol. Monogr. 25:291–320
Patten NL, Wyatt ASJ, Lowe RJ, Waite AM. 2011. Uptake of picophytoplankton, bacterioplankton and
virioplankton by a fringing coral reef community (Ningaloo Reef, Australia). Coral Reefs 30:555–67
Pineda J, Starczak V, Tarrant A, Blythe J, Davis K, et al. 2013. Two spatial scales in a bleaching event:
Corals from the mildest and the most extreme thermal environments escape mortality. Limnol. Oceanogr.
58:1531–45
Pomeroy A, Lowe RJ, Symonds G, van Dongeren A, Moore C. 2012. The dynamics of infragravity wave
transformation over a fringing reef. J. Geophys. Res. 117:C11022
Raupach MR, Shaw RH. 1982. Averaging procedures for flow within vegetation canopies. Bound. Layer Meteorol. 22:79–90
Reidenbach MA, Koseff JR, Monismith SG. 2007. Laboratory experiments of fine-scale mixing and mass
transport within a coral canopy. Phys. Fluids 19:075107
Reidenbach MA, Koseff JR, Monismith SG, Genin A. 2006. Effects of waves, currents and morphology on
mass transfer in branched reef corals. Limnol. Oceanogr. 51:1134–41
Ribes M, Atkinson M. 2007. Effects of water velocity on picoplankton uptake by coral reef communities. Coral
Reefs 26:413–21
Ribes M, Coma R, Atkinson MJ, Kinzie RA. 2005. Sponges and ascidians control removal of particulate organic
nitrogen from coral reef water. Limnol. Oceanogr. 50:1480–89
Richmond R. 1987. Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora
damicornis. Mar. Biol. 93:527–33
Riegl B, Piller WE. 2003. Possible refugia for reefs in times of environmental stress. Int. J. Earth Sci. 92:520–31
Rosman JH, Hench JL. 2011. A framework for understanding drag parameterizations for coral reefs. J. Geophys.
Res. 116:C08025
Santos IR, Erler D, Tait D, Eyre BD. 2010. Breathing of a coral cay: tracing tidally driven seawater recirculation
in permeable coral reef sediments. J. Geophys. Res. 115:C12010
Sargent M, Austin T. 1949. Organic productivity of an atoll. Trans. Am. Geophys. Union 30:245–49
Sebens KP, Grace SP, Helmuth B, Maney EJ, Miles JS. 1998. Water flow and prey capture by three scleractinian
corals, Madracis mirabilis, Montastrea cavernosa and Porites porites, in a field enclosure. Mar. Biol. 131:347–60
Sebens KP, Johnson A. 1991. Effects of water movement on prey capture and distribution of reef corals.
Hydrobiologia 226:91–101
Sebens KP, Witting J, Helmuth B. 1997. Effects of water flow and branch spacing on particle capture by the
reef coral Madraci mirabalis (Duchassaing and Michelotti). J. Exp. Mar. Biol. Ecol. 211:1–28
Shaw EC, McNeil BI, Tilbrook B. 2012. Impacts of ocean acidification in naturally variable coral reef flat
ecosystems. J. Geophys. Res. 117:C03038
Shulman M, Bermingham E. 1995. Early life histories, ocean currents, and the population genetics of
Caribbean reef fishes. Evolution 49:897–910
Silverman J, Lazar B, Cao L, Caldeira K, Erez J. 2009. Coral reefs may start dissolving when atmospheric
CO2 doubles. Geophys. Res. Lett. 36:L05606
Smith SV. 1973. Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification
in the Eniwetok reef flat community. Limnol. Oceanogr. 18:106–20
Symonds G, Black KP, Young IR. 1995. Wave-driven flow over shallow reefs. J. Geophys. Res. 100:2639–48
Taebi S, Lowe RJ, Pattiaratchi CB, Ivey GN, Symonds G, Brinkman R. 2011. Nearshore circulation in a
tropical fringing reef system. J. Geophys. Res. 116:C02016
Tanaka Y, Miyajima T, Watanabe A, Nadaoka K, Yamamoto T, Ogawa H. 2011. Distribution of dissolved
organic carbon and nitrogen in a coral reef. Coral Reefs 30:533–41
Tartinville B, Deleersnijder E, Rancher J. 1997. The water residence time in the Mururoa atoll lagoon:
sensitivity analysis of a three-dimensional model. Coral Reefs 16:193–203
Teneva L, Dunbar RB, Mucciarone DA, Dunckley JF, Koseff JR. 2013. High-resolution carbon budgets
on a Palau back-reef modulated by interactions between hydrodynamics and reef metabolism. Limnol.
Oceanogr. 58:1851–70
www.annualreviews.org • Oceanic Forcing of Coral Reefs
65
ARI
29 October 2014
6:57
Thomas FIM, Atkinson MJ. 1997. Ammonium uptake by coral reefs: effects of water velocity and surface
roughness on mass transfer. Limnol. Oceanogr. 42:81–88
Thomas FIM, Cornelisen CD. 2003. Ammonium uptake by seagrass communities: effects of oscillatory versus
unidirectional flow. Mar. Ecol. Prog. Ser. 247:51–57
UNEP-WCMC (UN Environ. Programme World Conserv. Monit. Cent.). 2003. Global distribution of coral
reefs (version 7). A 1 km resolution grid produced by UNEP-WCMC from an updated version of the data
layer used in Spalding et al. (2001). Data Set, UNEP-WCMC, Cambridge, UK. http://data.unepwcmc.org/datasets/14
Van Hooidonk R, Maynard J, Planes S. 2013. Temporary refugia for coral reefs in a warming world. Nat.
Clim. Change 3:508–11
Venti A, Kadko D, Andersson AJ, Langdon C, Bates NR. 2012. A multi-tracer model approach to estimate
reef water residence times. Limnol. Oceanogr. Methods 10:1078–95
Wang YH, Dai CF, Chen YY. 2007. Physical and ecological processes of internal waves on an isolated reef
ecosystem in the South China Sea. Geophys. Res. Lett. 34:L18609
Weitzman JS, Aveni-Deforge K, Koseff JR, Thomas FIM. 2013. Uptake of dissolved inorganic nitrogen by
shallow seagrass communities exposed to wave-driven unsteady flow. Mar. Ecol. Prog. Ser. 475:65–83
Weller E, Nunez M, Meyers G, Masiri I. 2008. A climatology of ocean–atmosphere heat flux estimates over the
great barrier reef and coral sea: implications for recent mass coral bleaching events. J. Clim. 21:3853–71
Wolanski E, Delesalle B. 1995. Upwelling by internal waves, Tahiti, French Polynesia. Cont. Shelf Res. 15:357–
68
Wolanski E, Drew E, Abel KM, O’Brien J. 1988. Tidal jets, nutrient upwelling and their influence on the
productivity of the alga Halimeda in the Ribbon Reefs, Great Barrier Reef. Estuar. Coast. Shelf Sci. 26:169–
201
Wolanski E, Thomson R. 1984. Wind-driven circulation on the northern Great Barrier Reef continental shelf
in summer. Estuar. Coast. Shelf Sci. 18:271–89
Woodley J, Chornesky E, Cliffo P. 1981. Hurricane Allen’s impact on a Jamaican coral reef. Science 214:749–54
Wyatt ASJ, Falter JL, Lowe RJ, Humphries S, Waite AM. 2012. Oceanographic forcing of nutrient uptake
and release over a fringing coral reef. Limnol. Oceanogr. 57:401–19
Wyatt ASJ, Lowe RJ, Humphries S, Waite AM. 2010. Particulate nutrient fluxes over a fringing coral reef:
relevant scales of phytoplankton production and mechanisms of supply. Mar. Ecol. Prog. Ser. 405:113–30
Yahel G, Post AF, Fabricius K, Marie D, Vaulot D, Genin A. 1998. Phytoplankton distribution and grazing
near coral reefs. Limnol. Oceanogr. 43:551–63
Yahel R, Yahel G, Berman T, Jaffe JS, Genin A. 2005. Diel pattern with abrupt crepuscular changes of
zooplankton over a coral reef. Limnol. Oceanogr. 50:930–44
Young IR, Zieger S, Babanin AV. 2011. Global trends in wind speed and wave height. Science 332:451–55
Zhang Z, Falter JL, Lowe RJ, Ivey G. 2012. The combined influence of hydrodynamic forcing and calcification
on the spatial distribution of alkalinity in a coral reef system. J. Geophys. Res. 117:C04034
Zhang Z, Falter JL, Lowe RJ, Ivey G, McCulloch M. 2013. Atmospheric forcing intensifies the effects of
regional ocean warming on reef-scale temperature anomalies during a coral bleaching event. J. Geophys.
Res. 118:4600–16
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Volume 7, 2015
Annu. Rev. Marine. Sci. 2015.7:43-66. Downloaded from www.annualreviews.org
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Reflections on My Career as a Marine Physical Chemist, and Tales of
the Deep
Frank J. Millero p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Regional Ocean Data Assimilation
Christopher A. Edwards, Andrew M. Moore, Ibrahim Hoteit,
and Bruce D. Cornuelle p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p21
Oceanic Forcing of Coral Reefs
Ryan J. Lowe and James L. Falter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p43
Construction and Maintenance of the Ganges-Brahmaputra-Meghna
Delta: Linking Process, Morphology, and Stratigraphy
Carol A. Wilson and Steven L. Goodbred Jr. p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p67
The Dynamics of Greenland’s Glacial Fjords and Their Role in
Climate
Fiamma Straneo and Claudia Cenedese p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p89
The Role of the Gulf Stream in European Climate
Jaime B. Palter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 113
Long-Distance Interactions Regulate the Structure and Resilience of
Coastal Ecosystems
Johan van de Koppel, Tjisse van der Heide, Andrew H. Altieri,
Britas Klemens Eriksson, Tjeerd J. Bouma, Han Olff, and Brian R. Silliman p p p p p p p 139
Insights into Particle Cycling from Thorium and Particle Data
Phoebe J. Lam and Olivier Marchal p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 159
The Size-Reactivity Continuum of Major Bioelements in the Ocean
Ronald Benner and Rainer M.W. Amon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 185
Subsurface Chlorophyll Maximum Layers: Enduring Enigma or
Mystery Solved?
John J. Cullen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 207
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Cell Size as a Key Determinant of Phytoplankton Metabolism and
Community Structure
Emilio Marañón p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 241
Phytoplankton Strategies for Photosynthetic Energy Allocation
Kimberly H. Halsey and Bethan M. Jones p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 265
Techniques for Quantifying Phytoplankton Biodiversity
Zackary I. Johnson and Adam C. Martiny p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 299
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Molecular Mechanisms by Which Marine Phytoplankton Respond to
Their Dynamic Chemical Environment
Brian Palenik p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 325
The Molecular Ecophysiology of Programmed Cell Death in Marine
Phytoplankton
Kay D. Bidle p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 341
Microbial Responses to the Deepwater Horizon Oil Spill: From Coastal
Wetlands to the Deep Sea
G.M. King, J.E. Kostka, T.C. Hazen, and P.A. Sobecky p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 377
Denitrification, Anammox, and N2 Production in Marine Sediments
Allan H. Devol p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 403
Rethinking Sediment Biogeochemistry After the Discovery of Electric
Currents
Lars Peter Nielsen and Nils Risgaard-Petersen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 425
Mussels as a Model System for Integrative Ecomechanics
Emily Carrington, J. Herbert Waite, Gianluca Sarà, and Kenneth P. Sebens p p p p p p p p p p 443
Infectious Diseases Affect Marine Fisheries and
Aquaculture Economics
Kevin D. Lafferty, C. Drew Harvell, Jon M. Conrad, Carolyn S. Friedman,
Michael L. Kent, Armand M. Kuris, Eric N. Powell, Daniel Rondeau,
and Sonja M. Saksida p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 471
Diet of Worms Emended: An Update of Polychaete Feeding Guilds
Peter A. Jumars, Kelly M. Dorgan, and Sara M. Lindsay p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 497
Fish Locomotion: Recent Advances and New Directions
George V. Lauder p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 521
There and Back Again: A Review of Residency and Return Migrations
in Sharks, with Implications for Population Structure and
Management
Demian D. Chapman, Kevin A. Feldheim, Yannis P. Papastamatiou,
and Robert E. Hueter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 547
Contents
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Whale-Fall Ecosystems: Recent Insights into Ecology, Paleoecology,
and Evolution
Craig R. Smith, Adrian G. Glover, Tina Treude, Nicholas D. Higgs,
and Diva J. Amon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 571
Errata
Annu. Rev. Marine. Sci. 2015.7:43-66. Downloaded from www.annualreviews.org
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An online log of corrections to Annual Review of Marine Science articles may be found
at http://www.annualreviews.org/errata/marine
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Contents