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Does enhanced water flow increase or decrease the risk of
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coral bleaching? A review and new working hypothesis
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Scott A. Wooldridge
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Australian Institute of Marine Science, Townsville, QLD, Australia, 4810
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Contact information:
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E-mail:
[email protected]
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Tel. +61 7 47534142
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Fax. +61 7 47725852
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Article type:
Review Article
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Running head:
Water flow and coral bleaching resistance
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Display items:
6 figures, no tables
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Word count:
main text 7,250, abstract 240
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Reference count:
115
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ABSTRACT: Short-term laboratory experiments provide compelling evidence that
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enhanced water flow can help to lower the risk of coral bleaching during periods of thermal
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stress. This conferred benefit has also been noted within natural reef settings. However,
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several quantitative field studies also support the opposing viewpoint - that enhanced flow
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might be likened to an agent provocateur that acts synergistically with temperature in
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reducing the threshold at which thermal anomalies stimulate coral bleaching. Clearly, both
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views can’t hold true – or can they? In this article, I review the physical mechanisms through
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which the action of water flow may alter the thermal stability of the coral-algae symbiosis.
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This leads to the development of a new working hypothesis (conceptual model), which
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explains how both low and enhanced water flow conditions can pre-condition the onset of
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CO2-limitation around the ribulose-1,5-bisphosphate-carboxylase-oxygenase (RUBISCO)
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enzyme of the algal endosymbionts during periods of temperature and light stress. The
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resultant sink-limitation within the photosynthetic electron transport chain has previously
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been identified as a viable cellular mechanism for the classic bleaching sequence of algal
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photoinhibition, oxidative damage, and host cell disruption. The new model predicts that the
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emerging envelope of modern reef seawater conditions – characterised by elevated sea
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surface temperatures (SSTs), rising CO2(aq) concentrations, and increased levels of inorganic
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nutrients – are antagonistic to the beneficial actions of enhanced water flow. Required
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‘global’ and ‘local’ management strategies are indentified which may help to ensure the
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beneficial actions of enhanced water flow.
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KEY WORDS Symbiodinium, mass transfer, acclimatisation
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INTRODUCTION
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The phenomenon of coral bleaching is recognized as one of the key threats to the
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persistence of coral reefs around the globe (reviewed by Hughes et al. 2003). Bleaching
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occurs when the symbiotic relationship between corals and dinoflagellate algae of the genus
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Symbiodinium (‘zooxanthellae’) breaks down, leading to the mass expulsion of zooxanthellae
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from the coral host (Glynn 1996, Brown 1997). For coral colonies, varying the symbiont
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population influences the amount of carbon (energy) that is photosynthetically fixed by the
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symbionts and translocated to the coral host (Hoegh-Guldberg & Smith 1989). Of primary
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concern is the potential for the breakdown of the coral-zooxanthellae symbiosis to cause
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colony mortality (Marshall & Baird 2000, Loya et al. 2001), heighten the susceptibility of
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corals to disease (Muller et al. 2008) and reduce the future reproductive output of colonies
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(Baird & Marshall 2002).
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Though a complete picture of the integrated suite of cellular processes is still emerging,
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the common trigger mechanism in most coral bleaching models is a heat- and light-driven
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disruption of the photosynthetic mechanisms of the zooxanthellae (reviewed by Venn et al.
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2008, Weis 2008). The resultant overproduction of reactive oxygen species (ROS) is then
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understood to initiate the host cell necrosis and apoptosis that underpins zooxanthellae
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expulsion (Gates et al. 1992, Dunn et al. 2002). This disruption sequence is consistent with
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the understanding that the primary environmental agent for large-scale bleaching events is the
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combination of high solar irradiance and anomalously warm SSTs (reviewed by Hoegh-
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Guldberg 1999). Indeed, only relatively short exposure (~1 week) to small increases (1-2°C)
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in SSTs beyond normal summer maxima can trigger the deleterious bleaching response
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(Berkelmans 2008).
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Originally, it was conceived that upper thermal bleaching limits were relatively stable and
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the result of long-term adaptation of the coral symbiosis to its local light and thermal regime
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(see e.g., Fitt et al. 2001, Coles & Brown 2003). More recent research suggests that the ability
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of corals to resist thermal stress may be more dynamic, and includes the possibility that
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conditions ‘local’ to the reef may strongly contribute to the symbiotic attribute of bleaching
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resistance (Wooldridge & Done 2009, Wooldridge 2009a, Carilli et al. 2009a,b, Wagner et al.
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2010). For example, the upper thermal bleaching threshold for reef areas that are regularly
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exposure to poor water quality (as defined by the available flux of dissolved inorganic
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nitrogen; DIN) can be up to ~1-2oC lower than for reef areas with more optimal water quality
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(Wooldridge & Done 2009, Wooldridge 2009a). Another local environmental factor that has
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often been cited to increase bleaching resistance is enhanced water flow (be it driven by
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currents and/or waves) (summarised by West & Salm 2003). In this case, the beneficial action
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is believed to relate to a mass transfer limiting process that can be independent of the thermal
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characteristics of the displacing water (Nakamura & van Woesik 2001). However, this
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reported benefit may not be universal, since several quantitative studies have also
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demonstrated that enhanced water flow can increase the risk and severity of coral bleaching
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(Patterson & Price 1992, McClanahan et al. 2005, Carpenter & Patterson 2007).
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In this paper, I further consider the variable bleaching response profile of symbiotic
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corals in terms of their local flow regime, with a specific focus on identifying additional
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environmental factors that may help to explain the apparent dichotomy. I begin by reviewing
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the underlying physics that control the mass transfer of dissolved substances (e.g. gases and
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inorganic nutrients) across the coral-seawater interface. I utilise this information to consider
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the potential cellular-level (‘mechanistic’) impacts of water flow on the conferred attribute of
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coral bleaching resistance. In so doing, I endeavour to draw together the apparent conflicting
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evidence that presently exists into a new coherent model; with the ultimate aim of 4
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contributing a new level of testable insight into the cellular mechanism(s) that underpin the
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bleaching response. The potential benefit of this new insight for developing local
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management solutions to the threat posed by global climate change is discussed.
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Background theory: Flow enhances the mass transfer of dissolved substances to (and from) the coral surface
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As water passes over a coral, frictional drag forces create a zone in which flow velocity is
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reduced. In the closest several millimetres to the coral surface (where flow velocities
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approach zero) passive diffusion is the dominant mechanism that controls the dispersion of
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solutes. This so-called diffusive boundary layer (DBL) is a common bottleneck for the
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transfer rate of essential dissolved substances (e.g. CO2, O2, NH4+) to (and from) the coral
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surface; with the solute-specific flux rate being an inverse function of the diffusional path
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length (i.e., the thickness of the DBL), and a positive function of the solute concentration
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gradient across it (Fick’s First Law; Denny 1988). The dynamics of this process can be
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described as a first-order reaction with respect to the concentration gradient across the DBL: /
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/
(1)
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where
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is the area over which the flux occurs and
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solute between the surface of the coral and the surrounding fluid. The key step in most mass
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transfer studies is to accurately define
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and the molecular diffusivity (D) of the solute within the DBL.
is the mass exchange rate,
is a boundary layer mass-transfer coefficient, A is the concentration difference of the
, which is dependent on the thickness of the DBL
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Fundamental to the present review, is the fact that the thickness of the DBL is strongly
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modulated by the pattern of fluid movement around the coral, which depends on the
5
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organisms’ size and shape (W) as well as on the characteristics of the moving fluid (e.g.,
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viscosity ( ), density (ρ), speed (U), and turbulence levels). A useful quantitative description
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of this convective regime is provided by the dimensionless Reynolds number (Re):
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(2)
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Another dimensionless index, the Sherwood number (Sh), helps to determine the degree to
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which the convective pattern of fluid movement around the coral enhances mass transfer
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relative to diffusion alone. Sh is calculated from hm, W, and D:
8
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(3)
Patterson (1992) showed that the relationship between Sh and Re follows a power function:
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(4)
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where c is a constant, and d is a flow-size exponent that varies for different geometries and
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whether the boundary layer around the coral surface is laminar or turbulent. By solving
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equations 2 to 4 simultaneously, it is possibly to quantitatively define hm in terms of the
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predicted pattern of fluid movement around the coral:
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(5)
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Based on a uniform solute concentration gradient across the DBL, the graphical outworking
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of Eq. (5) (Fig.1) highlights that the rate of mass transfer (per unit coral surface area) benefits
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from: (i) increased flow speeds, (ii) smaller coral size-dimensions, and (iii) turbulent flow. In
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each case, the result can be understood in terms of the diffusive benefits of a thinner DBL. In
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this same way, mass transfer rates can also altered by the morphological shape of a coral 6
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colony, whether driven by: (i) gross characteristics (e.g., thin branching morphologies have
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higher mass transfer rates than mounding (massive) morphologies (Falter et al. 2007)), or (ii)
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intracolony differences (e.g., the tips of branching corals and the leading edges of plating
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corals are sites of maximal mass transfer (Helmuth et al. 1997a, Baird & Atkinson 1997)).
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The extrapolation of these theoretical generalisations across whole reef tracts is
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complicated by the interaction of the DBL with additional (larger-scale) boundary layers that
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form as ocean currents interact with the overall structure of the benthic environment. For
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example, Shashar et al. (1996) found that flow over a coral reef is often controlled by a ~1 m-
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thick logarithmic benthic boundary layer (BBL), which greatly reduces flow within 20-50 cm
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of the substratum. Thus for a mainstream water velocity of 12 cm s-1, the flow within the
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lower-50 cm region of the BBL could be as low as 2-3 cm s-1 (Shashar et al. 1996). Large
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corals that protrude significantly into the logarithmic BBL will thus benefit from higher flow
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speeds (Lenihan et al. 2008) and associated reductions in the thickness of the DBL. In this
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way, theoretical generalisations about the diffusive benefits of small corals (Fig. 5; Nakamura
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& van Woesik 2001) need to be tempered against the potential action of larger-scale
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influences. Similar arguments have been made about the cumulative importance of the reef
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structure (at-large) for localised (coral head) turbulence levels (Falter et al. 2007).
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Beneficial impacts of enhanced water flow upon coral bleaching resistance
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The importance of water flow for coral metabolism and material exchange has received
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considerable attention (see e.g., Jokiel 1978, Patterson et al. 1991, Atkinson & Bilger 1992,
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Lesser et al. 1994, Thomas & Atkinson 1997). Here, I specifically consider those flow-
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augmented processes which may act to enhance bleaching resistance.
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ROS removal from the coral surface. The potential for water flow to augment the
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passive diffusion of ROS away from the coral tissue, and thereby limit the extent of cellular
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damage, is the most widely cited mechanism by which water flow may provide resistance to
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bleaching (Nakamura & van Woesik 2001, Nakamura et al. 2003, Nakamura et al. 2005).
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Such a mechanism is commensurate with short-term laboratory experiments which highlight
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that corals held in higher flow have lower rates of photoinhibition (Nakamura et al. 2005),
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lower bleaching responses (Nakamura & van Woesik 2001) and faster recovery from
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bleaching (Nakamura et al. 2003). Yet, despite its intuitive appeal, none of these experiments
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provide definitive proof that flow-augmented ROS removal is the dominant mechanism
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responsible. Indeed, a recent experiment that more directly investigated the beneficial impact
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of flow on coral photosynthesis was unable to detect the involvement of ROS removal (Mass
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et al. 2010). Confirmation of this mechanism thus requires further experimental testing.
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Oxygen removal from the coral surface during the day. Emerging research indicates
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that the effect of flow on photosynthesis can operate at the cellular level of the RUBISCO
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enzyme, which is central to the ‘dark’ carbon-fixation reactions (Calvin-Benson cycle) of
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photosynthesis (Mass et al. 2010). Zooxanthellae are unique amongst most oxygenic
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phototrophs in that they utilise a form II RUBISCO enzyme to facilitate photosynthetic
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carbon assimilation (Rowan et al. 1996). This enzyme has a poor ability to discriminate
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between CO2 (photosynthesis) and O2 (photorespiration) (Whitney and Andrews 1998). By
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comparison with the caloric benefits of photosynthesis, photorespiration is an energetically
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wasteful process (one carbon atom being lost for every two O2 fixed). Photorespiration is
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expected to occur when the internal concentration of O2 is sufficiently high to outcompete
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CO2 as the dominant substrate for RUBISCO. The beneficial action of water flow in
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enhancing the rate of O2 efflux from the coral tissue during periods of high photosynthesis is
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thus consistent with the higher rates of photosynthetic efficiency (PE) achieved during short8
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term flow-enhancement studies (Finelli et al. 2006, Mass et al. 2010). Sustained periods of
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higher PE, with its potential to increase photosynthate transfer rates, may be considered
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beneficial for corals in building energy reserves needed to offset periods of phototrophic
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disruption associated with bleaching. Despite this fact, there is currently no evidence that the
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photorespiration pathway contributes directly to the bleaching sequence during periods of
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heat and light stress. Indeed, it has been suggested that one of the evolutionary pressures for
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the maintenance of the photorespiration pathway is that it provides an alternative electron
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acceptor pathway during periods of photo-stress in which the electron transport chain
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becomes over-reduced (Wingler et al. 2000, Ort and Baker 2002). In this way,
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photorespiration may actually provide beneficial photoprotection, all-be-it at a significant
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energetic cost.
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Oxygen transfer to the coral surface during the night. Despite experiencing extreme O2
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supersaturation in the light, the DBL region near the surface of corals is characterised by an
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almost complete nocturnal depletion of O2 in low flow (Shashar et al. 1993). Such O2
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depletion may restrict the rate of dark respiration needed for cellular growth and maintenance
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in both symbiont partners. For this reason, the beneficial action of water flow in raising the
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integrated (coral-zooxanthellae) respiration rate (Patterson et al. 1991, Bruno & Edmunds
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1998) is typically explained in terms of the flow-augmented enhancement of O2 delivery to
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the coral surface. Interestingly, increasing water motion typically causes the integrated
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respiration rate (R) to increase at a faster rate than photosynthesis (P); meaning that the
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autotrophic capacity (P:R) of the symbiosis actually starts to decline with increasing water
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motion (Patterson et al. 1991). For example, tank experiments with the reef coral Galaxea
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fasicularis demonstrate that autotrophic capacity can become negative (P:R < 1) for flow
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speeds beyond 10 cm s-1 (Schutter et al. 2010). A possibility explored later in this review, is
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that part of the flow-augmented increase in respiration rates may be associated with a 9
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detrimental (unconstrained) expansion of the zooxanthellae population, which comes at the
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expense of reduced photosynthate transfer to the coral host.
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Enhanced production of mycosporine-like amino acids (MAAs). The photoprotective
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benefits of MAAs contained in the tissues of reef corals is well established, with numerous
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studies highlighting a strong correlation between exposure to high levels of ultraviolet
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radiation and increased MAA concentrations (reviewed by Shick & Dunlap 2002).
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Significant to present review, is the observation that enhanced water flow is a crucial factor in
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the maintenance of MAAs for some coral species (Jokiel et al. 1997, Kuffner 2002). Though
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the precise mechanism remains untested, it has been proposed that the beneficial action of
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water flow is most-likely related to the enhanced delivery of the necessary substrates (e.g.
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carbon and essential nutrients) required for MAA production (Jokiel et al. 1997, Kuffner
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2002). MAAs are believed to be produced by the zooxanthellae through the shikimate acid
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pathway (Shick & Dunlap 2002), thus anything affecting the delivery rate of essential
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substrates across host and zooxanthellar membranes could slow down the process, leading to
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a substrate-limited state. For example, the seawater supply of important dissolved inorganic
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nutrients for the intact symbiosis is often mass transfer limited (Atkinson & Bilger 1992,
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Thomas & Atkinson 1997).
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Heat removal from the coral surface. In shallow conditions, the mere heating power of
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solar radiation can contribute an additional heat load to the exposed coral tissue (Fabricius
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2006, Jimenez et al. 2008). For example, under high irradiance and low flow conditions (< 6
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cm s-1), shallow-water corals can be 0.2 - 0.6oC warmer than the surrounding water (Fabricius
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2006, Jimenez et al. 2008). This additional heat load has been linked to the presence of a
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thermal boundary layer (TBL) (Jimenez et al. 2008). The TBL at the surface of corals is
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analogous to the DBL in that they both: (i) emerge through the action of viscous forces in the
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fluid and, (ii) limit the exchange of heat and solutes between the surface and the surrounding 10
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fluid. It follows that enhanced water flow contributes to cooling corals by thinning the TBL,
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thereby reducing the resistance to heat transfer toward the surrounding water. In this way, the
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cooling action of higher flows may assist in keeping shallow-water corals below their
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summer bleaching thresholds. However, the thermal exchange efficiency of a coral is clearly
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not the dominant (direct) factor governing coral bleaching resistance. For example, a thin
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(10-mm-diameter) coral branch exchanges heat with the surrounding water twice as
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efficiently as a thicker branch (50 mm in diameter) or a larger hemispherical (50 mm
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diameter) coral when exposed to a uniform water velocity of 1 cm s-1 (Jimenez et al. 2008),
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yet it is well established that branching corals are more sensitive to thermal stress than are
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massive species (Marshall & Baird 2000, Loya et al. 2001).
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Enhanced prey capture rates. Laboratory experiments and field studies highlight that
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many coral species experience particle flux and encounter rate limitations at low flow speeds,
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thereby supporting the suggestion that up to some optimum flow speed, greater flow
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increases potential organic particulate matter and zooplankton (prey) capture rates. For
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example, an increase in flow speed from 5 to 10 cm s-1 results in a two-fold increase in the
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capture rate of zooplankton by Madracis mirabilis (Sebens et al. 1998). Studies on
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heterotrophy show that corals can obtain nitrogen, phosphorus and even carbon, through
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capture of zooplankton and/or ingestion of suspended particulate matter. It has therefore been
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demonstrated that, even under non-stressful conditions, heterotrophy can promote
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photosynthesis, tissue and skeletal growth (reviewed by Houlbrèque & Ferrier-Pagès 2009).
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Food availability may also be very important for coral metabolism during bleaching events
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(Grottoli et al. 2004). In such conditions, the autotrophic capacity of the coral colony is
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greatly reduced, and the coral host is forced to rely more heavily on heterotrophy and/or it
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stored energy reserves (Grottoli et al. 2006). Corals, able to trap zooplankton are less likely to
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die from bleaching than poor plankton consumers (Grottoli et al. 2006). Moreover, there 11
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exists persuasive evidence that heterotrophic feeding can also help to sustain the
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photosynthetic activity of the zooxanthellae during periods of thermal stress, thereby helping
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to forestall the onset of bleaching (Borell & Bischof 2008, Ferrier-Pagès et al. 2010). Thus, to
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the extent that higher flow may aid the heterotrophic capacity of a coral, it may be considered
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a beneficial factor in raising the bleaching resistance of corals.
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Detrimental impacts of enhanced water flow upon coral bleaching
8
resistance
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Despite the potential benefits, a number of quantitative field studies have documented a
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net negative impact of enhanced water flow on coral bleaching resistance. For example,
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McClanahan et al. (2005) found an overall positive association between bleaching intensity
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and enhanced water flow in the reefs surrounding the island of Mauritius (Fig. 2). In order to
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explain this response, the authors called upon the catch-all notion of ‘stress acclimation’ i.e.,
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corals living in reef environments that frequently experience extreme conditions may be more
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resistant to bleaching conditions compared to corals living in more stable physical
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environments (Jokiel & Coles 1990, Glynn 1996, Marshall & Baird 2000). In this case, high
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water flow (by reducing background stress and acclimation) is predicted to result in corals
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that are less tolerant of high temperature anomalies. No physiological evidence was
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forwarded by McClanahan et al. (2005) to confirm the speculation.
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Further evidence for the detrimental impact of enhanced water flow on coral
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bleaching resistance comes from intracolony bleaching patterns (Patterson & Price 1992). In
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this case, colonies of Montastrea annularis and M. cavernosa were observed to bleach faster
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at upstream sections (= higher flow velocities / thinner DBL) than downstream sections (=
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lower flow velocities / thicker DBL). A similar asymmetric pattern was recorded for the 12
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photosynthetic yields of M. annularis colonies subjected to thermal stress (ca. 2 °C above
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ambient), with the upstream side of colonies exhibiting reduced quantum yields (Carpenter &
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Patterson 2007). The authors emphasize their uncertainty of the underlying process(es), but
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speculate that increased flow may lead to increased photosynthesis by upstream polyps
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through the enhanced delivery of dissolved inorganic carbon (DIC; HCO3-/CO2) delivery
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accentuated by the Q10 effect. Local down-regulation of the downstream photosynthetic
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response (decreased quantum yield) might then occur to keep tissue oxygen concentrations
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within tolerable limits. Perhaps most importantly, the authors outline the possible existence of
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an optimal flow threshold (~10 - 15 cm s-1) for photosynthetic performance (and bleaching
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resistance), such that increasing flow speeds up to the threshold are beneficial, whilst flow
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speeds beyond the threshold become increasingly detrimental. This notion of an optimum
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flow threshold (~10 cm s-1) for coral bleaching resistance is commensurate with the bleaching
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response data of McClanahan et al. (2005) (Fig. 2).
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A new hypothesis to explain the variable impact of water flow upon
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coral bleaching resistance
16
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Recently, Wooldridge (2009b) identified the onset of CO2-limitation within the ‘dark’
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reactions (Calvin-Benson cycle) of zooxanthellae photosynthesis as a potential unifying
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cellular mechanism for the classic bleaching sequence of zooxanthellae photoinhibition,
20
oxidative damage, and host cell disruption (Fig. 3). In this case, (1) CO2 substrate limitation
21
of the RUSBICO enzyme stalls the consumption of ‘light’ reaction products (ATP and
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NADPH), which blocks the photosynthetic electron transport chain (= sink limitation); (2)
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continued funnelling of excitation energy into the over-reduced electron transport chain
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damages essential photosynthetic components (principally photosystem II, PSII), and 13
1
generates damaging ROS; and (3) the excess production of ROS beyond the antioxidant
2
defence strategies of the coral host (and zooxanthellae) initiates the host cell necrosis and
3
apoptosis that underpins zooxanthellae expulsion.
4
From the standpoint of the ‘CO2-limitation coral bleaching model’, any biophysical factor
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that causes the demand for CO2 to exceed supply within the coral’s intracellular milieu is
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identified as a bleaching risk factor (Wooldridge and Done 2009; Wooldridge 2010). From
7
this new standpoint, I explain here how both low and high water flow rates can pre-condition
8
the onset of intracellular CO2-limitation, and thereby lower thermal bleaching resistance.
9
Low water flow (= low intracellular supply of seawater CO2). The intracellular location
10
of the zooxanthellae dramatically affects the source and reliability in supply of CO2 needed
11
for photosynthesis. Although respiratory CO2 is available from both zooxanthellae and
12
animal pathways, it accounts for only ~50% of the carbon needed by the algae during high
13
rates of photosynthesis (Muscatine et al. 1989). High rates of photosynthesis place strong
14
(additional) demands upon a seawater supply of CO2. This in turn, typically requires the
15
conversion of abundant seawater bicarbonate (HCO3-) into readily diffusible CO2, which is
16
facilitated by active host CO2-concentrating mechanisms (CCMs) (Fig. 4).
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The host CCMs are very effective at raising the intracellular CO2 pool. For example, Furla
18
et al. (2000b) demonstrated a 61-fold increase in DIC upon activation. Yet the CCMs do
19
introduce a significant source of vulnerability to the CO2 supply chain of the zooxanthellae
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population. As outlined by Wooldridge (2009b), if the CCMs were to become disrupted,
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especially during periods of high photosynthetic demand for CO2, then the likelihood of the
22
zooxanthellae experiencing CO2-limitation around RUBISCO would be real, and the resultant
23
cellular outcome could be the classic symptoms of coral bleaching (Fig. 3). Crucially, the
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efficient functioning of the host CCMs remains dependent upon the passive diffusion of
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HCO3-/CO2 across the unstirred DBL. The possibility therefore exists that during periods of 14
1
low flow, the operation of the host CCMs could become mass transfer limited; thereby
2
dramatically reducing their effectiveness. Indeed, the experimental findings of Lesser et al.
3
(1994) confirm that the CCMs of the reef coral Pocillopora damicornis were unable to fully
4
compensate for the thicker DBL encountered under low flow (< 5 cm.s-1) conditions for a
5
fixed morphology. More generally, even with finely-branched morphologies, mass-transfer
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limitation of photosynthesis can persist until flow speeds exceed ~10 cm.s-1 (Rex et al. 1995).
7
In this way, low ambient flow rates (< 10 cm.s-1) are predicted to increase the bleaching
8
susceptibility of corals during periods of high irradiance and temperature, which is consistent
9
with the ‘low-flow’ range of field observations from McClanahan et al. (2005) (Fig. 2).
10
High water flow (= excessive biological demand for intracellular CO2). In considering
11
the wider implications of the CO2-limitation bleaching model, Wooldridge (2009b) outlined a
12
possible role for irradiance-driven competition of CO2 in setting upper (permissible) limits
13
for symbiont densities, i.e., provided essential nutrients are not limiting to growth,
14
zooxanthellae densities are predicted to balance around the equilibrium (supply = demand)
15
state for intracellular CO2. The commonly reported inverse relationship between
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zooxanthellae densities and seasonal irradiance levels is consistent with such an equilibrating
17
mechanism (Stimson 1997, Fitt et al. 2000).
18
As a logical extension of this idea, it follows that enhanced mass transfer rates of CO2 may
19
permit increased zooxanthellae densities; largely facilitated by an increase in the number of
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zooxanthellae per host gastroderm cell. Several lines of evidence support this prediction,
21
subject to the conditional proviso that observations are carried out under ambient (benign)
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irradiance and temperature conditions. Firstly, laboratory and field-based studies indicate that
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high flow treatments support higher zooxanthellae densities (Nakamura et al. 2003, Mass &
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Genin 2008). Secondly, coral morphologies that favour high mass transfer rates (e.g., high
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surface area: volume ratios) support higher zooxanthellae densities (Fig. 5; Patterson et al.
15
1
1991, Helmuth et al. 1997b, Strychar et al. 2004). Finally, experimental manipulations that
2
increase the background seawater concentration of CO2 permit enlarged zooxanthellae
3
densities (Reynaud et al. 2003, Rodolfo-Metalpa et al. 2010). In each case, the observations
4
highlight the potential for enhanced CO2 mass transfer to at least double the standing stock of
5
zooxanthellae.
6
Far from being unequivocally beneficial, the CO2-limitation bleaching model predicts that
7
an enlarged zooxanthellae population may actually become a metabolic burden to the coral
8
host during periods of heat and light stress, ultimately leading to increased bleaching
9
susceptibility (Wooldridge 2009b, 2010). To understand this paradox, it is necessary to
10
consider the impact of enlarged zooxanthellae densities on the stability and functioning of the
11
host CCMs. In this case, as densities increase, the photosynthetic capacity per zooxanthellae
12
(P) progressively decreases (possibly due to increased self-shading within the host cell) whist
13
the associated respiratory/maintenance cost to the symbiosis (R) increases (linearly) per
14
zooxanthellae added (Anthony et al. 2009, Hoogenboom et al. 2010). In this way, it is
15
understood that there exists an optimum zooxanthellae density that maximises autotrophic
16
capacity (P:R), i.e., every zooxanthellae added beyond this optimum conspires to reduce the
17
energy (ATP) transferred to the coral host. Similarly, the maximum efficiency of the ATP-
18
dependent CCMs will be linked to this optimum zooxanthellae density, i.e., every
19
zooxanthellae added beyond the optimum conspires to reduce the efficiency of the host
20
CCMs. Notably, the standing stock of zooxanthellae within both tropical and temperate corals
21
can be more than double the predicted optimum zooxanthellae density (Fig. 6; Anthony et al.
22
2009, Hoogenboom et al. 2010). This reveals two crucial details about the modern coral-algae
23
symbiosis: (i) under ambient (benign) conditions, the loss in autotrophic capacity per
24
zooxanthellae added beyond the optimum density must be relatively small, thus permitting
25
large changes in zooxanthellae densities to occur between (P:R)optimum and the symbiosis 16
1
breakpoint where autotrophic capacity is completely lost (P:R < 1), and (ii) the addition of
2
zooxanthellae beyond the optimum operation of the host CCMs must be primarily facilitated
3
by the passive diffusion of seawater CO2 and not the active (ATP-dependent) dehydration of
4
seawater HCO3-.
5
An easily identified problem for an enlarged zooxanthellae population (especially one that
6
is heavily reliant upon a passive supply of seawater CO2) is the potential for significant
7
instability (zooxanthellae expulsion) in the event of: (i) a sudden irradiance-driven increase in
8
CO2 demand, or (ii) a sudden flow-mediated decrease in CO2 supply. Moreover, the worst
9
case scenario is the combination of high irradiance and low flows; which is a characteristic
10
feature of the ‘doldrum’ conditions that normally precede mass bleaching events (Gleason &
11
Wellington 1993). However, as explained by Wooldridge (2009b), it is not the initial
12
(equilibrating) loss of zooxanthellae that is the problem pe se. Rather, the more damaging
13
situation occurs when the large number of zooxanthellae expelled (.day-1) is matched with
14
warm (possibly nutrient-replete) seawater conditions that favour rapid regrowth (.day-1) from
15
the remnant zooxanthellae. In this case, although P may remain stable, the high respiratory
16
cost of regrowth can lead to a negative autotrophic carbon balance (P:R < 1), wherein more
17
carbon per day is directed into new cell production than is transferred to the host.
18
Significantly, an extended (several days – weeks) run of diminished autotrophic capacity is
19
proposed to underpin a self-enhancing disruption (cessation) of the ATP-dependent host
20
CCMs - leading to the mass expulsion of the bulk zooxanthellae compliment (Wooldridge
21
2009b, 2010).
22
In this way, enhanced ambient flow rates (>10 cm.s-1) are predicted to increase the
23
bleaching susceptibility of corals during periods of high irradiance and temperature, which is
24
consistent with the ‘high-flow’ range of field observations from McClanahan et al. (2005)
25
(Fig. 2). Several lines of evidence support the proposed symbiosis disruption mechanism: (i) 17
1
zooxanthellae within corals exposed to high flow rates have low cellular ratios of carbon-to-
2
nitrogen (C:N) (Stambler et al. 1991, Lesser et al. 1994), which is a characteristic feature of
3
rapidly dividing algal cells (Hoegh-Guldberg 1994, Berner & Izhaki 1994), (ii) the known
4
reduction in autotrophic capacity (P:R) at progressively higher (suboptimal; >28°C)
5
temperatures proceeds at a faster rate in coral communities that are routinely exposed to
6
higher flow rates (Castillo & Helmuth 2005). More generally, the mechanism fits with the
7
understanding that: (i) corals which experience high zooxanthellae turnover rates are more
8
susceptible to bleaching (Stimson et al. 2002, Grimsditch et al. 2008), and (ii) corals which
9
experience high mass transfer rates, whether facilitated by flow or morphology, are most at
10
risk from high zooxanthellae turnover rates (Stambler et al. 1991, Stimson et al. 2002,
11
Grimsditch et al. 2008).
12 13
DISCUSSION
14
15
A reassessment of the experimental evidence. The new hypothesis offers important
16
criteria for (re)assessing the impact of enhanced water flow (> 10 cm s-1) on thermal
17
bleaching resistance. The criteria are based on whether the in hospite zooxanthellae
18
population has had: (i) the sufficient time (days - several weeks), and (ii) access to the
19
necessary inorganic nutrients (e.g. NH4+) to establish the CO2-equilibrating (flow-dependent)
20
density. Failure to meet either criterion ensures that enhanced flow rates are experienced as
21
an effective increase in CO2 per zooxanthellae; presumed beneficial for both carbon fixation
22
and bleaching resistance. This stands in direct contrast to the outlined situation in which both
23
criteria are met, and enhanced flow rates are matched with enlarged zooxanthellae
24
populations that are increasingly reliant on the passive supply (diffusion) of seawater CO2;
25
presumed detrimental for both optimum carbon fixation and bleaching resistance. The 18
1
identified criteria thus help to rationalise previous experimental findings which suggest that
2
enhanced water flow can be both beneficial and detrimental to the symbiotic attribute of
3
bleaching resistance. Mass transfer limited flow (i.e.,
